How Many Peas in a Pod? Legume Genes Responsible for Mutualistic Symbioses Underground

Hiroshi Kouchi; Haruko Imaizumi-Anraku; Makoto Hayashi; Tsuneo Hakoyama; Tomomi Nakagawa; Yosuke Umehara; Norio Suganuma; Masayoshi Kawaguchi

doi:10.1093/pcp/pcq107

How Many Peas in a Pod? Legume Genes Responsible for Mutualistic Symbioses Underground

Kouchi, Hiroshi; Imaizumi-Anraku, Haruko; Hayashi, Makoto; Hakoyama, Tsuneo; Nakagawa, Tomomi; Umehara, Yosuke; Suganuma, Norio; Kawaguchi, Masayoshi 2010-07-21 00:00:00 Special Issue – Mini Review How Many Peas in a Pod? Legume Genes Responsible for Mutualistic Symbioses Underground 1, 1 1 1,4 Hiroshi Kouchi * , Haruko Imaizumi-Anraku , Makoto Hayashi , Tsuneo Hakoyama , 1 1 2 3 Tomomi Nakagawa , Yosuke Umehara , Norio Suganuma and Masayoshi Kawaguchi Department of Plant Sciences, National Institute of Agrobiological Sciences, Tsukuba, 305-8602 Japan Department of Life Science, Aichi University of Education, Kariya, 448-8542 Japan Department of Evolutionary Biology and Biodiversity, National Institute for Basic Biology, Okazaki, 444-8585 Japan Present address: Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, 113-8657 Japan * Corresponding author: E-mail, [email protected] ; Fax, + 81-29-838-8347 (Received May 28, 2010; Accepted July 17, 2010) The nitrogen-ﬁ xing symbiosis between legume plants and Rhizobium , in which endosymbiotic rhizobia ﬁ x atmospheric Rhizobium bacteria is the most prominent plant–microbe nitrogen. Our understanding of this agriculturally important endosymbiotic system and, together with mycorrhizal fungi, endosymbiosis has been greatly advanced during the last has critical importance in agriculture. The introduction of two decades. The discovery of rhizobial symbiotic signal two model legume species, Lotus japonicus and Medicago molecules [Nod factors (NFs)] in the early 1990s was a signiﬁ - truncatula , has enabled us to identify a number of host cant breakthrough which led to elucidation of the basic legume genes required for symbiosis. A total of 26 genes scheme of rhizobial nodulation ( Nod ) gene functions (for a have so far been cloned from various symbiotic mutants review, see Spaink 1995 ). NFs are chitin ( N -acetylglucosamine of these model legumes, which are involved in recognition oligomers) derivatives, of which the non-reducing end is of rhizobial nodulation signals, early symbiotic signaling N -acylated and the reducing end is modiﬁ ed by various cascades, infection and nodulation processes, and regulation molecules. These speciﬁ c NF structures determine the strict of nitrogen ﬁ xation. These accomplishments during the speciﬁ city between Rhizobium and host legume species, and past decade provide important clues to understanding not elicit both the rhizobial infection process and the initiation only the molecular mechanisms underlying plant–microbe of nodule primordia in the roots of the compatible host endosymbiotic associations but also the evolutionary aspects legumes. of nitrogen-ﬁ xing symbiosis between legume plants and Molecular identiﬁ cation of NFs and successive vast progress Rhizobium bacteria. In this review we survey recent progress in understanding the functions of bacterial Nod genes have in molecular genetic studies using these model legumes. promoted investigation into host legume genes essential for endosymbiosis, including mycorrhizal symbiosis, which is evo- Keywords: Lotus japonicus • Medicago truncatula • Model lutionarily related to the legume– Rhizobium symbiosis. To this legumes • Nitrogen ﬁ xation • Nodules • Plant–microbe aim, utilization of two model legume species, Lotus japonicus symbiosis . and Medicago truncatula , was proposed, because they are self- Abbreviations : AM , arbuscular mycorrhizal ; AON , fertile diploids with relatively small genome size and short autoregulation of nodulation ; CaM , calmodulin ; CCaMK , generation periods, and are capable of molecular transfection 2 + Ca - and calmodulin-dependent protein kinase ; CCD , ( Barker et al. 1990 , Handberg and Stougaard 1992 ). On the cortical cell division ; CSP , common symbiosis pathway ; HCS , basis of the resources established for genome research in homocitrate synthase ; IT , infection thread ; Lb , leghemoglobin ; these model legumes, a number of host legume genes LRR , leucine-rich repeat ; LysM-RK , LysM receptor-like kinase ; involved in NF perception and subsequent symbiotic signal NCR , nodule-speciﬁ c cysteine-rich ; NF , Nod factor ; PBM , transduction, bacterial infection and nodule organogenesis, peribacteroid membrane ; RN , root nodule. and regulation of nitrogen ﬁ xation have been identiﬁ ed in the past decade ( Table 1 ). In this review, we present a survey of the current status of our knowledge about host legume genes Introduction and mechanisms underlying the mutualistic endosymbiotic Legume plants are able to form root nodules (RNs) by associations with microbes, focusing mainly on nitrogen-ﬁ xing symbiotic association with soil bacteria collectively termed symbiosis between legume plants and rhizobia. For mycorrhizal Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107, available online at www.pcp.oxfordjournals.org © The Author 2010. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.5), which permits unrestricted non-commercial use distribution, and reproduction in any medium, provided the original work is properly cited. Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. 1381 H. Kouchi et al. Table 1 Cloned genes involved in legume– Rhizobium symbiosis Genes in model Mutant phenotypes Gene product Possible function Legume orthologs References legumes b c d Inf Nod EC LjNFR1 , MtLYK3 − − − LysM receptor kinase NF receptor PsSYM37 1, 2, 3 LjNFR5 , MtNFP − − − LysM receptor kinase NF receptor GmNFR5 , PsSYM10 1, 4, 5 LjSYMRK , MtDMI2 − − − LRR receptor kinase CSP MsNORK , PsSYM19 6, 7 2 + LjCASTOR − − − Ca -gated ion channel CSP 8 2 + LjPOLLUX , MtDMI1 CSP PsSYM8 8,9 − − − Ca -gated ion channel LjNUP133 − − − Nucleoporin CSP 10 LjNUP85 Nucleoporin CSP 11 − − − 2 + 2 + LjCCaMK , MtDMI3 − − − Ca /CaM-dependent CSP (putative Ca signal PsSYM9 12, 13 kinase decoder) LjCYCLOPS , MtIPD3 ± ± − Nuclear protein CSP (CCaMK interactor) 14, 15 IT growth LjNIN , MtNIN − − − Putative transcription Infection, CCD PsSYM35 16, 17, 18 factor LjNSP1 , MtNSP1 GRAS family transcription Infection, CCD 19, 20 − − − regulator LjNSP2 , MtNSP2 − − − GRAS family transcription Infection, CCD PsSYM7 19, 20, 21 regulator LjLHK1 , ( MtCRE1 ) + ± − Cytokinin receptor kinase Nodule organogenesis 22, 23, 24 LjNAP1 ± ± − Component of F-actin IT growth 25 condensing complex LjPIR1 ± ± − Component of F-actin IT growth 25 condensing complex LjHAR1 , MtSUNN LRR receptor kinase AON GmNARK, PsSYM29 26, 27, 28 + + + + + MtSICKLE + + + + + + EIN2 (ethylene-insensitive) Regulation of IT growth 29 LjASTRAY + + + + bZIP transcription factor Regulation of nodulation 30 LjCERBERUS , MtLIN ± ± − Putative E3 ubiquitin ligase IT growth 31, 32 MtERN1 ± ± − ERF transcription factor IT growth 33 MtRPG Novel coiled-coil protein IT growth 34 ± ± − MtNIP/LATD + ± ± NTR1 transporter IT growth 35 LjFEN1 + + + Homocitrate synthase Nitrogenase biosynthesis GmN56 36, 37 LjIGN1 + + + Ankyrin repeat membrane Bacteroid maintenance 38 protein LjSST1 + + + Sulfate transporter Transport SO to bacteroids 39 MtDNF1 + + + Signal peptidase subunit Symbiosome and/or 40 bacteroid differentiation Only the genes identiﬁ ed by forward genetics are listed in this table. Many other genes have been demonstrated or suggested to be involved in symbiosis by the reverse genetics approach and/or expression proﬁ les (see details in the text). Lj and Mt at the beginning of the gene names indicate Lotus japonicus and Medicago truncatula , respectively. Inf = formation of infection threads (ITs) penetrating into the cortex. ± indicates occasional IT formation within root hair cells. Nod = nodule formation. ± indicates the formation of bumps (arrest of nodule development). EC = endocytosis of rhizobia inside nodules. ± indicates development of nodule-infected cells at low frequency compared with the wild type nodules. Ps, Pisum sativum ; Gm, Glycine max ; Ms, Medicago sativa . Common symbiosis pathway. Cortical cell division. Autoregulation of nodulation References: 1, Radutoiu et al. (2003) ; 2, Limpens et al. (2003) ; 3, Smit et al. (2007) ; 4, Madsen et al. (2003) ; 5, Arrighi et al. (2006) ; 6, Stracke et al. (2002) ; 7, Endre et al. (2002) ; 8, Imaizumi-Anraku et al. (2005) ; 9, Anè et al. (2004) ; 10, Kanamori et al. (2006) ; 11, Saito et al. (2007) ; 12, Tirichine et al. (2006) ; 13, Levy et al. (2004) ; 14, Yano et al. (2008) ; 15, Messinese et al. (2007) ; 16, Schauser et al. (1999) ; 17, Marsh et al. (2007) ; 18, Borisov et al. (2003) ; 19, Heckmann et al. (2006) ; 20, Kalo et al. (2005) ; 21, Murakami et al. (2006) ; 22, Murray et al. (2007) ; 23, Tirichine et al. (2007) ; 24, Gonzalez-Rizzo et al. (2006) ; 25, Yokota et al. (2009) ; 26, Nishimura et al. (2002a) ; 27, Krusell et al. (2002) ; 28, Schnabel et al. (2005) ; 29, Penmetsa et al. (2008) ; 30, Nishimura et al. (2002b) ; 31, Yano et al. (2009) ; 32, Kiss et al. (2009) ; 33, Middleton et al. (2007) ; 34, Arrighi et al. (2008) ; 35, Yendrek et al. (2010) ; 36, Hakoyama et al. (2009) ; 37, Kouchi and Hata (1995) ; 38, Kumagai et al. (2007) ; 39, Krusell et al. (2005) ; 40, Wang et al. (2010) . 1382 Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. Legume genes involved in symbiosis symbiosis, the most up to date knowledge was presented in detail in a recent review by Hata et al. (2010) . Perception of microbial signals Putative NF receptors have been identiﬁ ed in various legume species: NFR1 and NFR5 from L. japonicus ( Madsen et al. 2003 , Radutoiu et al. 2003 ) and from Glycine max ( Indrasumunar et al. 2010 ); LYK3 and NFP from M. truncatula ( Limpens et al. 2003 , Arrighi et al. 2006 ); and SYM37 and SYM10 from Pisum sativum ( Zhukov et al. 2008 ). These putative NF receptors have a common structure composed of a single-pass trans- membrane domain anchored to an extracellular lysin motif (LysM) receptor domain and an intracellular kinase domain, and are thus termed LysM receptor-like kinases (LysM-RKs). Most of their loss-of-function mutants lack any of the responses to rhizobial inoculation as well as to puriﬁ ed NFs. The LysM domain is known to be involved in binding peptidoglycan and/or structurally related molecules, such as chitin oligosac- charides. At present, however, no structural study has been carried out on the interactions of LysM domains with speciﬁ c NF structures. In L. japonicus , NFR1 and NFR5 are thought to form a recep- tor complex (most possibly a heterodimer) responsible for speciﬁ c recognition of NFs secreted from Mesorhizobium loti , a Rhizobium species compatible with L. japonicus ( Fig. 1 ), because their co-transformation has been shown to be able to extend the host range of M. loti to the heterologous plant Fig. 1 Recognition of Nod factors by NFR1 and NFR5 in L. japonicus . species ( Radutoiu et al. 2007 ). Since the intracellular domain of Extracellular LysM domains are thought to be responsible for binding LjNFR5 has been shown to lack the kinase activity ( Madsen Nod factors, and then transduce the symbiotic signals through the et al. 2003 ), LjNFR1 could be crucial for transmitting the intracellular kinase of NFR1 to downstream signaling cascades, leading intracellular signal to downstream symbiotic signaling path- to rhizobial infection and nodulation. PM, plasma membrane. ways. Indeed, the kinase activity of NFR1 was demonstrated to be essential for activating downstream symbiotic signaling pathways in L. japonicus (T. Nakagawa, unpublished result). however, it should be noted that legume plants have a large In M. truncatula , NFP is thought to be an ortholog of NFR5 number of LysM-RKs compared with non-legumes. For exam- ( Arrighi et al. 2006 ) and its mutant shows no response to ple, the L. japonicus genome contains at least 17 LysM-RKs and NFs puriﬁ ed from Sinorhizobium meliloti , a Rhizobium species they are all expressed, while Arabidopsis and rice have ﬁ ve and compatible with Medicago plants ( Amor et al. 2003 ). However, six LysM-RK genes in their genome, respectively ( Lohmann et al. the M. truncatula hcl mutant of LYK3 , which is proposed 2010 ). Analysis of the whole-genome sequences suggested that to be an ortholog of NFR1 , retains the earliest responses upon the LysM-RK gene family has further diversiﬁ ed by tandem and 2 + inoculation with S. meliloti , such as Ca spiking and root hair segmental duplication in legumes (Zhang et al. 2007, Lohmann deformation ( Wais et al. 2000 , Catoira et al. 2001 , Smit et al. et al. 2010 ). These ﬁ ndings raise the possibility that NF percep- 2007 ). Therefore, the positions of NFR1 and LYK3 in symbiotic tion and subsequent intracellular signaling are mediated by signaling appear not to be identical. In Medicago plants, complex combinations of multiple LysM-RKs including those a model composed of two distinct NF receptors, i.e. signaling other than NFR1 and NFR5 ( Oldroyd and Downie, 2008 ). and entry receptors, has been proposed ( Ardourel et al. 1994 , Thus the exact mechanisms of the host recognition of NFs are Smit et al. 2007 ). These two receptors (or receptor complexes) still elusive. are postulated to have different levels of requirements with It is intriguing that a chitin receptor, CERK1, in Arabidopsis regard to NF structures, and to be responsible differentially has been demonstrated to be essential to induce plant innate for infection thread (IT) formation and nodule organogenesis. immunity against fungal pathogens ( Miya et al. 2007 ), because In L. japonicus , a single receptor complex composed of NFR1 CERK1 is a LysM-RK which belongs in the same phylogenic and NFR5 appears to be responsible for the activation of clade as NF receptors such as NFR1 and LYK3. In particular, both infection and nodulation processes ( Hayashi et al. 2010 , its intracellular kinase domain shows high similarity (approxi- Madsen et al. 2010 ; see details in the next section). In this regard, mately 67 % identity) to that of NFR1. Based on the structural Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. 1383 H. Kouchi et al. similarity together with the microsynteny in the Arabidopsis organogenesis ( Kevei et al. 2007 ). SIP is a novel DNA-binding and Lotus genome around CERK1 and NFR1, it has been pro- protein with an AT-rich domain (ARID), which speciﬁ cally posed that these LysM-RKs are the descendants of a common binds to the promoter of NIN ( Zhu et al. 2008 ). These results ancestor ( Zhu et al. 2006 ). Indeed, NFR1 has been shown to suggest that SYMRK also participates directly or indirectly in retain the ability to activate transiently defense-related genes nodulation-speciﬁ c pathways that follow the CSP. 2 + in response to puriﬁ ed NFs (T. Nakagawa, unpublished results). CASTOR and POLLUX , both of which encode Ca -gated It is of great interest to elucidate how these structurally related cation (most probably potassium) channel proteins, have been LysM-RKs induce apparently opposite biological responses in identiﬁ ed as members of the CSP in L. japonicus ( Imaizumi- their host plants; one induces endosymbiotic association and Anraku et al. 2005 , Charpentier et al. 2008 ). Despite their high the other induces defense reactions. Addressing this question structural similarity, a single mutation of CASTOR or POLLUX in more detail would provide new direction in the analysis of caused symbiosis-defective phenotypes, indicating that they the evolutionary process of the legume– Rhizobium symbiosis. fulﬁ ll a symbiotic function(s) in combination. In contrast, only DMI1 , an ortholog of POLLUX , has been identiﬁ ed from symbi- osis-defective mutants of M. truncatula ( Anè et al. 2004 ). It is Early symbiotic signaling noteworthy that in rice, a monocotyledonous mycorrhizal About half of the non-nodulating legume mutants isolated so plant, the requirement for both OsCASTOR and OsPOLLUX far are also defective in arbuscular mycorrhizal (AM) symbiosis, in AM symbiosis has been proven ( Banba et al. 2008 , Gutjahr implying that the genes responsible for those mutants are et al. 2008 , Chen et al. 2009 ). Similarly to L. japonicus , a single required for both RN and AM symbioses. Thus, the signal trans- mutation of either OsCASTOR or OsPOLLUX results in the duction pathway mediated by those genes is termed the abortion of AM infection, indicating that functional collabora- ‘common symbiosis pathway’ (CSP). In L. japonicus , seven genes tion between these ‘twin’ genes is also the case in rice. Thus, so far have been positioned in the CSP ( Table 1 ). The range of considering the requirement for CASTOR and POLLUX, which symbiosis-defective phenotypes of the CSP genes indicates are very closely structurally related to each other, in Lotus , rice that they are grouped into two categories; one is positioned and probably in the ancestral lineage of mycorrhizal plants, it upstream (upstream genes) and the other is downstream of appears intriguing that in Medicago , DMI1 probably has been 2 + Ca spiking, which is a central physiological reaction in the endowed during evolution with a function which integrates CSP ( Ehrhardt et al. 1996 , Miwa et al. 2006 ). these ‘twin’ channel proteins. It is still an open question how Following the perception of NFs through LysM-RKs (see CASTOR and POLLUX share their functions in symbiotic signal- 2 + 2 + above), biphasic Ca signaling is induced in root hair cells, i.e. ing processes leading to generation of Ca spiking. The cellular 2 + a rapid inﬂ ux of Ca into the root hair cells and then periodical localization of these components is something of a mystery 2 + oscillation of cytosolic Ca concentrations at the perinuclear at present. They have been reported to be localized in the 2 + 2 + region (Ca spiking). Ca spiking is also induced in response nuclear envelope ( Riely et al. 2007 , Charpentier et al. 2008 ), to AM infection, and is critical for AM symbiosis as well as RN while L. japonicus CASTOR and POLLUX have a signal peptide symbiosis ( Kosuta et al. 2008 ). In L. japonicus , ﬁ ve out of seven which is predicted to be a plastid targeting signal, and have CSP genes, SYMRK , CASTOR , POLLUX , NUP85 and NUP133 , are been shown to be in plastids when expressed under the 2 + required for the induction of Ca spiking ( Stracke et al. 2002 , control of the cauliﬂ ower mosaic virus (CaMV) 35S promoter Imaizumi-Anraku et al. 2005 , Kanamori et al. 2007, Saito et al. ( Imaizumi-Anraku et al. 2005 , Charpentier et al. 2008 ). Further 2007 ), whereas CCaMK and CYCLOPS are positioned down- evaluation of the spatio-temporal gene expression and cellular 2 + stream of Ca spiking ( Tirichine et al. 2006 , Yano et al. 2008 ), localization of CASTOR and POLLUX is required. and thus they have been thought to play important roles in Both nup85 and nup133 mutants show temperature-sensitive 2 + transmitting symbiotic signals mediated by Ca signals to the symbiosis-defective phenotypes. Rhizobial and AM infections downstream RN- and AM-speciﬁ c pathways. are aborted in the epidermis at high temperature, while normal SYMRK and DMI2 , which encode LRR (leucine-rich repeat)- invasion of the microsymbionts occurs on the roots of both receptor kinases, have been isolated from L. japonicus and mutants under the normal temperature regime ( Kanamori M. truncatula , respectively ( Endre et al. 2002 , Stracke et al. 2002 ). et al. 2006 , Saito et al. 2007 ). Based on the sequence similarity Because of their cellular localization in the plasma membrane to mammalian nucleoporins, both NUP85 and NUP133 are ( Limpens et al. 2005 ), SYMRK/DMI2 are believed to be the predicted to be the components of the NUP107–NUP160 sub- starting point of the CSP, although the ligand(s) of their complex, which is located on both sides of the nuclear pore extracellular receptor domains are still unknown. Screening ( Meier and Brkljacic 2009 ). Because symbiotic NF-responsive 2 + of interacting factors with SYMRK/DMI2 kinase domains Ca spiking is associated with the root hair cell nucleus, NUP85/ resulted in isolation of HMGR1 from M. truncatula and SIP NUP133 are postulated to be involved in transport or localiza- 2 + from L. japonicus . HMGR1 encodes a putative mevalonate tion of the factor(s) needed for the induction of Ca spiking. 2 + synthase which is involved in the synthesis of isoprenoid Ca - and calmodulin (CaM)-dependent protein kinase, compounds. Knock-down analysis of HMGR1 suggested its CCaMK, consists of three functional domains, i.e. a serine/ involvement in the rhizobial infection process and nodule threonine-kinase domain, a CaM-binding (autoinhibitory) 1384 Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. Legume genes involved in symbiosis T265D domain (CaMBD) and a domain of three EF hands which inter- CCaMK or kinase-only CCaMK mimic the activated status 2 + 2 + act with Ca ions. As its name and domain organization sug- of CCaMK in response to Ca spiking in vivo, these data sug- 2 + gest, CCaMK is a putative decoder of Ca signals. CCaMK was gest a possible function for CCaMK as the connecting point of ﬁ rst isolated from lily ( Lilium longiﬂ orum ), and biochemical two signaling pathways which are split from the NF receptors. analyses have shown that its kinase activity is dependent on An intriguing subject for the future will be to address the 2 + 2 + 2 + interactions with Ca and CaM ( Patil et al. 1995 ). However, hypothesis that two different Ca signals, i.e. Ca inﬂ ux and 2 + CCaMK function during plant growth has remained elusive Ca spiking, are prerequisite in order to exceed the threshold for a long time. Isolation and characterization of dmi3/ of CCaMK activity required for intracellular infection of snf1/ccamk mutants produced an answer to the question. rhizobia. M. truncatula dmi3 and L. japonicus ccamk mutants are defec- Recently, Lefebvre et al. (2010) isolated a symbiotic remorin, 2 + tive in both RN and AM symbioses, though Ca spiking is MtSYMREM1 from M. truncatula , which is exclusively expressed induced in response to rhizobial inoculation and to NF applica- in the nodulation process. Remorins are the ﬁ lamentous pro- tion in these mutants ( Levy et al. 2004 , Tirichine et al. 2006 ). teins that have been implicated to have scaffolding functions Furthermore, spontaneous nodulation in the absence of rhizo- generally in the cell membrane, and some members of this bia was induced by gain-of-function mutation of CCaMK, in multigene family have been described to be involved in biotic which Thr265 at the autophosphorylation site of the kinase interactions in plants ( Lefebvre et al. 2010 ). The most promi- domain is substituted by isoleucine ( snf1 , Tirichine et al. 2006 ) nent feature of MtSYMREM1 is that it interacts with LYK3, NFP or aspartate ( Gleason et al. 2006 ), indicating a pivotal role for and DMI2, which are the orthologs of NFR1, NFR5 and SYMRK CCaMK in nodule organogenesis. in L. japonicus , respectively. In nodulated roots of Medicago , Recent studies showed that introduction of the snf1 genetic MtSYMREM1 was localized in the plasma membrane enclosing T265D background or CCaMK into L. japonicus mutants of the ITs as well as in the symbiosome membrane. These ﬁ ndings CSP genes ( SYMRK , CASTOR , POLLUX , NUP85 and NUP133 ), suggest that SYMREM1 plays a role in retaining LysM-RKs and 2 + which are positioned upstream of Ca spiking, suppressed loss- SYMRK in the plasma membrane at the growing IT tips, thus 2 + of-function mutation of these mutants, not only rhizobial but enabling continuous operation of Ca signaling mediated by also AM infection ( Hayashi et al. 2010 , Madsen et al. 2010 ). LysM-RKs and CSP components. Such continuation of the 2 + This indicates that these upstream genes are solely required Ca signaling at the interface with rhizobia allows the host 2 + for the generation of Ca spiking. In contrast, expression of cells to support the IT elongation and penetration into cortical T265D CCaMK in either nfr1 or nfr5 did not alter their infection cells ( Fig. 2B ). defects, although it could induce nodule organogenesis in The RN symbiosis is presumed to have its evolutionary origin these mutants irrespective of the presence or absence of in the more ancient AM symbiosis and to have evolved by M. loti ( Hayashi et al. 2010 ). The snf1/nfr1/nfr5 triple mutants recruiting the pre-existing CSP genes ( Markmann and Parniske allowed rhizobia to invade through an ‘intercellular’ route 2009 ). Given the fact that CSP regulates two different symbiosis (so-called ‘crack entry’) at a very low frequency, but in that case systems in legumes, it is plausible that the CSP has retained its 2 + rhizobial infection was not accompanied by the formation of functions, i.e. a generator and transmitter of Ca spiking for ITs within root hairs ( Madsen et al. 2010 ). Thus the gain-of- the establishment of AM symbiosis, during acquisition of RN function form of CCaMK alone is sufﬁ cient to induce nodule symbiosis in legume plants. Indeed, rice orthologs of CASTOR, organogenesis, while intracellular accommodation of rhizobia POLLUX, CCaMK and CYCLOPS, which all have conserved through root hair ITs requires an additional signaling pathway domain structures between Lotus and rice, could restore the derived from NFR1 and NFR5, which is distinct from that defects in rhizobial infection of the corresponding Lotus mutant 2 + involving Ca spiking mediated by the CSP upstream genes lines, indicating the functional conservation of these CSP genes 2 + ( Fig. 2A ; Hayashi et al. 2010 ). In this regard, Ca inﬂ ux is a pos- in legumes and non-legumes ( Banba et al, 2008 , Yano et al. sible candidate for involvement in this additional signaling 2008 ). One exception is SYMRK; a monocot SYMRK from rice 2 + pathway, because generation of Ca inﬂ ux is dependent on has only one LRR and a non-legume dicot SYMRK from tomato NFR1/NFR5, but not on the CSP genes ( Miwa et al. 2006 ). As has two LRRs, while legume SYMRKs and those of actinorhizal shown in Fig. 2A , the integration point of the two pathways is plants which are involved in nitrogen-ﬁ xing symbiosis with postulated to be at or around CCaMK. The essentiality of the the actinomycetes Frankia have three LRRs. In addition, rice 2 + Ca binding capacity of CCaMK for rhizobial infection has SYMRK lacks an extended N-terminal domain of unknown also been shown by kinase-only CCaMK which lacks both the function. Cross-species complementation tests demonstrated CaMBD and EF hands. Introduction of the kinase-only CCaMK that the shorter version of SYMRK could restore the defect in into M. truncatula dmi3 mutants resulted in induction of spon- AM symbiosis but not RN symbiosis in Lotus symrk mutants, taneous nodulation, while rhizobial infection did not occur while a ‘full-length’ version from the nodulating clade could upon inoculation with S. meliloti ( Gleason et al. 2006 ), suggest- restore both AM and RN symbioses ( Markmann et al. 2008 ). 2 + ing that binding of Ca ions to CCaMK per se, or the activated Therefore, there are divergent evolutionary pathways among 2 + status of CCaMK through Ca signaling, is prerequisite for the CSP genes, and SYMRK has a distinctive position as an rhizobial infection. Although it remains unclear to what extent adaptive factor for the evolution of RN symbiosis in legumes. Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. 1385 H. Kouchi et al. Fig. 2 A current model of early symbiotic signaling pathways. (A) The gene cascades in early symbiotic signaling (modiﬁ ed from Hayashi et al. 2010 ). In response to Nod factors, the signal generated by NFR1/NFR5 splits into two pathways; one ﬂ ows into the common symbiosis pathway (CSP, blue line) and the other (pink line) is prerequisite for successful infection of rhizobia. The genes of CSP components are indicated by green 2 + letters. (B) The proposed roles of Ca signaling and CCaMK activation in infection thread formation and growth. The exact localization and composition of the NF receptor complex(es) have not yet been determined. 2 + Since it has been shown that Ca spiking has different signa- to internal and external cues. An important internal cue is tures dependent on RN or AM symbiotic interactions ( Kosuta a systemic feedback regulatory system involving long-distance et al. 2008 ), such diversiﬁ cation of SYMRK as the entrance to root–shoot signaling, termed autoregulation of nodulation the CSP may lead to the transmission of RN- and AM-speciﬁ c (AON), which is shown to be closely linked with early symbiotic signals to the downstream pathways through the activation signaling triggered by NFs ( Caetano-Anollés and Gresshoff 1991 , 2 + status of CCaMK mediated by different Ca signatures. Con- Oka-kira and Kawaguchi 2006 ). AON is believed to consist of versely, CSP genes other than SYMRK have basically kept their two presumptive long-distance signals, i.e. root-derived and functions throughout the evolution of the RN symbiosis in shoot-derived signals. The root-derived signal is generated in legumes, and thus constituted the foundation of the CSP in roots in response to rhizobial NFs and then translocated to the the course of evolution ( Banba et al. 2008 ). shoot, while the shoot-derived signal is generated in shoots and then translocated to the root to restrict further nodulation ( Fig. 3 ; Magori and Kawaguchi 2009 ). Mutants defective in AON, such as G. max nts / nark , L. japonicus har1 , M. truncatula Systemic regulation of symbiosis sunn and P. sativum sym29 , display a so-called ‘hypernodula- Although symbiotic nitrogen ﬁ xation is highly beneﬁ cial to tion’ phenotype ( Carroll et al. 1985 , Sagan and Duc 1996 , Wop- legume hosts, excessive nodulation interferes with plant ereis et al. 2000 , Penmetsa et al. 2003 ). Grafting experiments growth because nodulation and nitrogen ﬁ xation require a high indicated that these mutants are defective in the production of energy cost. To balance the symbiosis, legume plants develop shoot-derived signals. The responsive genes have been shown speciﬁ c mechanisms to control the nodule number in response to encode an LRR receptor-like kinase ( Krusell et al. 2002 , 1386 Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. Legume genes involved in symbiosis HAR1 (H. Miyazawa et al. unpublished data). Thus, KLV and HAR1 are likely to function coordinately to receive the root- derived signal in the shoot. The shoot-regulated hypernodula- tion and fasciated stem phenotypes of klv are shared with P. sativum sym28 and nod4 ( Sagan and Duc 1996 , Sidorova and Shumnyi 2003 ). Molecular identiﬁ cation of these genes might shed light on a common mechanism to connect RN- and legume-speciﬁ c shoot apical meristem regulation. The next important question is the molecular nature of the root-derived signal(s). There is evidence that receptor-like kinases such as HAR1 show a high similarity to Arabidopsis CLV1 . It has been shown recently that an extracellular domain of CLV1 directly binds to a modiﬁ ed CLE peptide processed from CLAVATA3 (CLV3) ( Ogawa et al. 2008 ). The CLE gene encodes a small secreted peptide composed of 12–13 amino acids. In Arabidopsis, the CLE genes constitute a family of at least 31 peptide ligand genes including CLV3 ( Sawa et al. 2006 ). In L. japonicus , at least 39 potential CLE genes have been identi- ﬁ ed in its genome. Among them, small peptides derived from two CLE genes (LjCLE-RS1 and LjCLE-RS2) have been proposed as strong candidates for the root-derived signal ( Okamoto et al. 2009 ), based on the following observations: (i) CLE-RS1/2 are rapidly and signiﬁ cantly up-regulated in response to rhizo- Fig. 3 A model for LRR receptor-like kinase-mediated autoregulation bial inoculation; (ii) perception of NFs and successive compo- of nodulation (AON). (1) Perception of the rhzobial Nod factor nents of the symbiotic signaling pathway such as CASTOR and initiates nodulation but also the production of a long-distance CCaMK are essential for CRE-RS1/2 up-regulation; (iii) overex- inhibitor called the root-derived signal. (2) L. japonicus CLE-RS1 and pression of CLE-RS1/2 in a hairy root system strongly suppresses -RS2 peptides as strong candidates of the root-derived signal may be nodulation; (iv) this inhibitory effect travels systemically from transported to the shoot, and (3) elicit the production of the transformed roots to untransformed roots; and (v) HAR1 is shoot-derived signal. Legume CLV1-like receptor-like kinases such as required for CLE-RS1/2 -mediated suppression of nodulation. HAR1/NARK/SUNN/SYM29 and KLAVIER mediate this process. The entire similarity of CLE-RS1/2 genes is not obvious, but (4) The shoot-derived signal(s) is translocated to the root and the 12 amino acids (PLSPGGPDPQHN) constituting the CLE negatively regulates nodulation via TML/RDH1. Pisum sativum NOD3 domain are identical ( Okamoto et al. 2009 ). Thus, HAR1 may and M. truncatula RDN that function in the root have a role in either the transmission of the root-derived signal or the perception of the perceive one modiﬁ ed CLE peptide derived from two CLE genes shoot-derived signal. in the shoot. In M. truncatula , two CLE genes ( MtCLE12 and MtCLE13 ), which suppress local and systemic nodulation, have been reported ( Mortier et al. 2010 ). Differently from Lotus , the Nishimura et al. 2002a , Schnabel et al. 2005 ), and have high MtCLE12/13 genes are not required for SUNN receptor-like similarity to CLAVATA1 ( CLV1 ) of Arabidopsis ( Clark et al. kinase, suggesting that the other receptor(s) is responsible for 1997 ) and FON1 of rice ( Suzaki et al. 2004 ). CLV1 and FON1 AON-mediated CLE signaling in M. truncatula . are speciﬁ cally expressed in shoot and ﬂ oral meristems, and The perception of the root-derived signal by legume CLV1- restrict their sizes by receiving a CLE peptide derived from the like receptor kinase is then presumed to initiate the production stem cell region ( Miwa et al. 2009 ). In contrast, the legume of the shoot-derived signal(s). Although the chemical nature of genes represented by L. japonicus HAR1 are widely expressed the shoot-derived signal is unknown, foliar application of plant in various organs but not in the shoot apex, suggesting that hormones has produced results indicating that brassinolide these genes uniquely evolved in legumes to produce the and methyl jasmonate may function as the shoot-derived shoot-derived inhibitor of nodulation by receiving the root- signal ( Nakagawa and Kawaguchi 2006 , Terakado et al. 2006 ). derived signal. Alternatively, polar auxin transport has been postulated to Together with HAR1 receptor-like kinase, KLAVIER ( KLV ) is play an important role in long-distance control of nodulation also indispensable for AON signaling in L. japonicus ( Oka-kira ( van Noorden et al. 2006 ). However, the involvement of these et al. 2005 ). The mutation exhibits stem fasciation as well as plant hormones in AON remains elusive, because of the lack of a hypernodulation phenotype. A double mutation analysis a uniﬁ ed explanation. The most reliable strategy to deﬁ ne the indicated that KLV functions in the same genetic pathway as shoot-derived signal would be to ﬁ nd the regulatory factors HAR1 . KLV encodes an LRR receptor-like kinase and is speciﬁ - from leaf extracts using a bioassay system. To characterize the cally expressed in the leaf vascular tissues, as with the case of signal, two research groups have developed novel bioassay Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. 1387 H. Kouchi et al. systems by feeding aqueous leaf extracts directly into the nodulation, and hypernodulation mutants such as nts , har1 , petiole of wild-type and supernodulation nark / NOD1-3 mutant klv and nod3 exhibit more or less nitrate-tolerant phenotypes plants of G. max ( Lin et al. 2010 , Yamaya and Arima 2010 ). Both ( Carroll et al. 1985 , Postma et al. 1988 , Wopereis et al. 2000 , groups succeeded in detecting nodulation suppression activity, Oka-Kira et al. 2005 ). Very recently it has been shown that but their results partly differ. Yamaya and Arima (2010) showed L. japonicus CLE-RS2 is strongly up-regulated in roots in that the suppressive activity of nodulation is constantly response to nitrate ( Okamoto et al. 2009 ). As CLE-RS2 -mediated detected irrespective of Bradyrhizobium japonicum inocula- suppression of nodulation is not observed in the har1 mutants, tion, whereas Lin et al. (2010) showed that the activity is promi- the nitrate-induced CLE-RS2 peptide is likely to suppress nently observed in a B. japonicum -secreted NF-dependent nodulation through HAR1. According to this model, nitrate manner. Further studies using the petiole feeding assay will be tolerance of the hypernodulation mutants can be explained needed to identify the signal molecule(s). because the mutations in NTS and HAR1 lead to defective CLE Root-speciﬁ c hypernodulation mutants have been isolated peptide perception in the presence of nitrate. Thus, CLE-RS2 in P. sativum nod3 ( Postma et al. 1988 ), L. japonicus rdh1 and is most probably a key regulator in nitrogen signaling and tml ( Ishikawa et al. 2008 , Magori et al. 2009 ) and M. truncatula develop mental plasticity that adapts to environmental nitro- rdn (J.A. Frugoli et al. unpublished data). These mutants are gen conditions. thought to be impaired in the translocation of the root- derived signal or in the perception of the shoot-derived signal Infection process and nodule organogenesis if they participate in long-distance root–shoot communication. Among them, L. japonicus TML has been shown by double Infection of rhizobia initially takes place at the root epidermis mutation and grafting analyses to function in the same genetic (root hair cells). The response of root hairs to NFs is restricted pathway as HAR1 . Furthermore, inverted-Y grafting experi- to a particular axial region of roots, the infection zone, where ments revealed that the suppressive effect of TML on nodula- root hairs develop. In order to incorporate rhizobia efﬁ ciently, tion cannot be transmitted systemically from wild-type roots many legumes have evolved a structural pathway for invasion, to the tml roots. These results suggest that TML is likely to func- i.e. ITs ( Sprent 2007 ). The IT is a tubular structure ﬁ rst initiated tion downstream of HAR1, possibly as a receptor or a mediator in the root hair, where it elongates by cell wall deposition and of the as yet unidentiﬁ ed shoot-derived signals ( Magori and ramiﬁ es the root cortex towards the nodule primordium that Kawaguchi 2009 , Magori et al. 2009 ). developed from the pericycle ( Gage and Margolin 2000 ). Independentoly of AON, the role of ethylene is well charac- Initiation of ITs requires several sequential steps; attachment terized as a negative regulator of nodulation. In M. truncatula , of bacteria on the root hairs, root hair curling and bacterial the numbers of successful bacterial infections and nodules colonization at the tip of distorted (curled) root hairs. Puriﬁ ed are substantially increased in the ethylene-insensitive mutant, NFs alone can induce a nodule meristem, but no root hair curl- sickle ( Penmetsa and Cook 1997 ). The SICKLE gene has been ing, indicating that the latter requires the presence of bacteria demonstrated to encode an M. truncatula ortholog of the at the surface of a root hair tip. However, not all root hairs Arabidopsis ethylene signaling protein, EIN2 ( Penmetsa et al. with attached bacteria in the infection zone exhibit root hair 2008 ). Inhibition of ABA biosynthesis and signaling through curling, suggesting the presence of a cell-speciﬁ c determinant(s) the use of a speciﬁ c inhibitor or a dominant-negative allele for susceptibility to rhizobial infection. Root hair curling is of ABSCISIC ACID INSENSITIVE1 leads to a hypernodulation characteristic of root nodule symbiosis: the normal polar tip phenotype, indicating that endogenous ABA is also involved growth of root hair development is disrupted, resulting in the in the negative regulation of nodulation ( Suzuki et al. 2004 , enclosure of attached bacteria inside a curl, where bacteria Ding et al. 2008 ). proliferate, colonize and express cell wall-degrading enzymes In addition to internal signaling represented by AON, host to penetrate to the root hair plasma membrane. The root hair legumes also control nodulation by sensing external signals. tip growth system is diverted to the focus of degradation to Light irradiation on roots strongly inhibits nodulation, but deposit the IT wall. This growth and direction of the IT is con- the roots of L. japonicus astray mutants can nodulate even in trolled by the presence of the nucleus and the rearrangement the light. The nodulation zone of astray is wider than that of microtubules and the actin cytoskeleton. The pathway of of the wild type, although the overall nodule density is com- IT development is paved by formation of pre-infection threads parable with that of the wild type. ASTRAY is closely related or cytoplasmic bridges ( van Brussel et al. 1992 ), which is analo- to Arabidopsis HY5 , a bZIP transcription factor. Interestingly it gous to the cytoplasmic strand formed during cell division. has a RING-ﬁ nger motif and an acidic region in its N-terminal Concomitantly with IT formation in the root hair, differen- half ( Nishimura et al. 2002b ). This type of transcription factor tiated cells at the root cortex (and then pericycle) start to is found in G. max and Vicia faba , but not in non-legumes, divide to develop a nodule meristem [cortical cell division indicating that this combination of motifs appears to be char- (CCD)]. This coordinated development between the infection acteristic of legumes. process and nodule organogenesis is believed to be crucial Another major external signal is soil nitrogen. High con- for successful nitrogen-ﬁ xing nodule formation ( Oldroyd and centrations of nitrogen such as nitrate or ammonia abolish Downie 2008 ). In L. japonicus , as well as in soybean and bean, 1388 Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. Legume genes involved in symbiosis the activity of the nodule meristem is restricted at the early drastically induced in the epidermis soon after NF perception, stages of nodule development. The developed nodule does not and is conﬁ ned to the infection zone ( Radutoiu et al. 2003 ). have a persistent meristem and is a spherical shape (determi- This induction requires NSP2 (Murakami et al. 2007), CYCLOPS nate nodules). In contrast, M. truncatula , as well as pea and ( Yano et al. 2008 ) and CERBERUS ( Yano et al. 2009 ). The cis - clover, has a persistent meristem at the tip of elongated nodule motifs for NIN binding have not yet been reported. structures even after full maturation (indeterminate nodules). CERBERUS and its Medicago ortholog, LIN , encode a U-box In this case, ITs remained in the nodule and continuously release protein with WD-40 repeats which is postulated to be an E3 bacteria for endosymbiosis. ubiquitin ligase ( Kiss et al. 2009 , Yano et al. 2009 ). CERBERUS is So far 11 genes have been cloned and reported to be necessary for IT initiation in addition to CYCLOPS and ERN1 . essential for coordinative progression of IT growth and nodule ERN1 encodes an ERF transcription factor, which contains an organogenesis ( Table 1 ). Intracellular signal transduction AP2 DNA-binding domain ( Middleton et al. 2007 ). In contrast through so-called common symbiosis genes following NF per- to CYCLOPS and CERBERUS , ERN1 is essential for spontaneous ception (see above sections) is a prerequisite to triggering nodulation by a gain-of-function CCaMK ( Middleton et al. this stage of symbiosis development. The only exception is 2007 ). Due to the facts that both CYCLOPS and CERBERUS are CYCLOPS , which is also required for symbiosis with arbuscular not required for spontaneous nodule formation but are neces- mycorrhiza, and thus is a member of the CSP genes, but its loss- sary for NIN induction in epidermis, and that NIN is essential for of-function mutant forms nodule primordia (which appear as CCD but CYCLOPS and CERBERUS are not ( Yano et al. 2008 , small bumps) upon inoculation of M. loti without any success- Yano et al. 2009 ), regulation of NIN expression in the epidermis ful infection events ( Yano et al. 2008 ). CYCLOPS is a nuclear- and cortex may differ in terms of their signaling cascades. localized protein and has been shown to be phosphorylated by Rearrangement of the cytoskeleton is important in biotic CCaMK in vitro ( Yano et al. 2008 ), and its Medicago ortholog, interaction in plants ( Takemoto and Hardham 2004 ). NAP1 and IPD3, has been shown to interact with DMI3 (CCaMK) in planta PIR1 have been shown to play such a role in rhizobial infection, by ( Messinese et al. 2007 ). Since the loss-of-function mutants of their involvement in actin polymerization, but are not involved CCaMK display neither root hair curling nor CCD, CYCLOPS is in CCD ( Yokota et al. 2009 ). They are also essential for trichome thought to be important for the function of CCaMK in the development like CRINKLE , which has been identiﬁ ed as a locus rhizobial infection process (see above section). required for both IT growth and normal trichome development Plant hormones are involved in various aspects of plant through actin cytoskeleton rearrangement ( Tansengco et al. development. In RN symbiosis, several hormones are reported 2003 , Tansengco et al. 2004 ). Microtubules have been shown to to be important. Among them, cytokinin has been shown play an important role in IT development ( Timmers et al. 1999 , genetically to be essential for nodule organogenesis. LHK1 in Vassileva et al. 2005 ), but their function in IT formation has not L. japonicus , which encodes a cytokinin receptor kinase, is yet been deﬁ ned genetically. only involved in nodule organogenesis in the cortex, not in IT RPG encodes a putative coiled-coil protein, which is local- formation. The loss-of-function mutant hit1 forms excessive ized in the nucleus ( Arrighi et al. 2008 ). In the loss-of-function ITs penetrating into the root cortex without inducing timely mutant, development of ITs is abnormal and is arrested mostly CCD after rhizobial inoculation ( Murray et al. 2007 ). In accor- in the root epidermis. LATD/NIP encodes a putative transporter dance with this ﬁ nding, a Lotus snf2 , which is a gain-of-function of the NRT1 (nitrate transporter) family ( Yendrek et al. 2010 ). mutant of LHK1 , exhibits spontaneous nodulation in the Mutation in LATD/NIP shows developed but abnormal ITs, and absence of rhizobia, indicating the crucial role of LHK1 in nodule bacterial release from ITs is aborted. The mutation also affects organogenesis ( Tirichine et al. 2007 ). Spontaneous nodule for- primary and lateral root development by meristem arrest. mation in snf2 requires NSP2 and NIN , but not CYCLOPS , so that The genes described above are mostly essential for IT initia- LHK1 functions in nodule organogenesis upstream of NSP2 tion and/or its growth, but not for induction of CCD per se, and NIN , but it is positioned downstream of or in a separate except for LHK1 . However, they are also involved in the pathway from CYCLOPS ( Tirichine et al. 2007 ), consistent with nodule organogenesis program, directly or indirectly. At least the observation that in the cyclops mutants nodule organo- in L. japonicus mutants, the infection process and nodule genesis is initiated ( Yano et al. 2008 ). organogenesis seem to be developmentally coupled ( Fig. 4 ; NSP2 encodes a GRAS family transcription regulator, and is in the case of pea, see Tsyganov et al. 2002 ). The mutants, required for CCD and root hair curling. NSP2 is localized in the which show no or aberrant root hair curling, fail to induce any nucleus and interacts with another GRAS family transcription CCD ( nsp1 , nsp2 and nin ). Abortion of IT initiation after regulator, NSP1 ( Hirsch et al. 2009 ). This interaction is neces- root hair curling and bacterial colonization coincides with sary for nodule organogenesis, and NSP1 associates with the formation of small bumps which are impaired in their develop- promoters of early nodulin genes, such as ENOD11 , NIN and ment into mature nodule structures ( cyclops and cerberus ). ERN1 ( Hirsch et al. 2009 ). NIN is a putative transcription regula- When ITs are developed in the root epidermis ( crinkle , alb1 tor that is also required for CCD and controlling root hair curl- and pir1-3 ), the arrest of nodule development is at a much ing ( Schauser et al. 1999 ). Its loss of unction results in unusually later stage, resulting in occasional abnormal bacterial release extensive root hair curling but no IT initiation. NIN expression is from developed ITs into infected cells in aberrant nodules Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. 1389 H. Kouchi et al. Host regulation of nitrogen ﬁ xation activity Almost concurrently with the emergence of nodules, rhizobia are released from ITs into the nodule cells, and they are then present in the host cell cytoplasm enclosed by the peribacte- roid membrane (PBM) which is derived from the host plasma membrane. They differentiate into a symbiosis-speciﬁ c form, the bacteroid, and then develop nitrogen-ﬁ xing activity. Bacte- roids at full maturation cease cell division, and PBM-enclosed bacteroids are essentially a nitrogen-ﬁ xing intracellular organ- elle, termed the ‘symbiosome’. Most Rhizobium species are unable to ﬁ x nitrogen in the free-living state. Housing within the nodule cells and differentiation into bacteroids is essential for rhizobial nitrogen ﬁ xation. Therefore, bacteroid differentia- tion and their nitrogen ﬁ xation are under strict control with complex interactions between the host legume cells and the intracellular bacteria; however, the mechanisms underlying differentiation of endosymbiotic rhizobia in symbiosomes to the bacteroid form are still largely unknown. In the indetermi- Fig. 4 Developmental regulation of the infection process and nodule organogenesis. The infection process and nodule organogenesis are nate nodules formed on legumes of the galegoid clade such sequentially (from left to right) drawn schematically. Genes essential as M. truncatula , recent evidence indicates that rhizobial for each step are indicated below the picture. (1) Attachment of a proli feration is terminated by DNA endoreduplication trig- bacterium on the surface of a root hair. (2). Root hair curling and the gered by host plant factors, which have been suggested to be following colonization of bacteria in the tight curl. (3) Infection thread nodule-infected cell-speciﬁ c cysteine-rich peptides ( Mergaert development in a root hair. A nodule primordium is initiated. (4) et al. 2006 ; see below), and BacA protein in rhizobia is shown Infection thread development into the nodule primordium. The to be involved in the uptake of the host-derived peptides nodule primordium is developed. The lower panel shows the ( Marlow et al. 2009 ). In the determinate nodules formed microphotographs of L. japonicus roots after inoculation with LacZ - on non-galegoid clade legumes, such as L. japonicus , however, labeled M. loti corresponding to steps 2, 3 and 4 from left to right. NP, the host mechanisms controlling rhizobial proliferation are nodule primordium. Bars = 100 µm. totally unknown. The bacteroids become slightly larger than the free-living (so-called ‘type II’ nodules; Yano et al. 2006 ). Because NFs from rhizobia in determinate nodules, whereas in indeterminate rhizobia are supposed to be initially recognized at the surface nodules they undergo much more remarkable morphological of the epidermis, there can be infection signal(s) transmitted changes such as cell elongation and/or Y-shaped transforma- from the epidermis downward to the cortex in order to tion. In addition, terminally differentiated bacteroids in inde- activate and regulate nodule organogenesis. This is consistent terminate nodules are functional but not viable, while the with the fact that only a small portion of ITs formed correlate bacteroids in determinate nodules have been shown to survive with CCD, and competence for CCD seems to be regulated in a reversed fashion, i.e. reverting to the free-living state by another signal(s) such as AON (see above section). As the when released in the soil from senesced and collapsed nodules. stages of nodule developmental arrest differ among the Therefore, the mechanisms of bacteroid differentiation and the different mutants, as described above, the regulation seems to situation of bacteroids inside nodule cells may be considerably involve multiple steps, so that there are probably several kinds different between indeterminate and determinate nodules. of signals from epidermis to cortex. One such transmitted A number of host legume genes (nodulin genes) speciﬁ cally signal may be cytokinin ( Oldroyd 2007 ). There may also be expressed during the nodulation process have been identiﬁ ed signals from cortex to epidermis to regulate the infection pro- from various legume species by differential or subtractive cess, because ITs that do not accompany CCD are aborted hybridization techniques ( Legocki and Verma 1980 , Kouchi and in the epidermis. Since the study of tissue-speciﬁ c expression Hata 1993 ). More recently, comprehensive analyses by means (epidermis or cortex) of the genes above described is quite of cDNA or oligo arrays and proteomics have revealed that limited, it is largely unknown whether those symbiosis genes more than a thousand genes are speciﬁ cally induced or highly are functional in epidermis or cortex, or in both. Analysis such enhanced in nodules ( Weinkoop and Saalbach 2003 , Colebatch as spatio-temporal expression of symbiosis genes in various et al. 2004 , Kouchi et al. 2004 , Tesfaye et al. 2006 , Larrainzar mutant backgrounds and gain-of-function studies with symbi- et al. 2007 , Benedito et al. 2008 , H ø gslund et al. 2009 ). Among osis genes including genes other than CCaMK and LHK1 is these genes, late nodulin genes, which are induced just before necessary to dissect the ﬁ ne-tuning of coordination of infection the onset of nitrogen ﬁ xation, have been implicated as being and nodule organogenesis programs. involved in the host regulation of nitrogen ﬁ xation. However, the 1390 Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. Legume genes involved in symbiosis experimental evidence regarding the exact functions of those genes is very limited. One example is leghemoglobin (Lb). Lb is nodule-speciﬁ c oxygen-binding protein, and has been thought to play the role both of keeping a low oxygen concentration in the nodule-infected cells and of facilitating O supply to the bacteroids for their aerobic respiration. RNA interference (RNAi) knock-down of Lb in L. japonicus was shown to result in almost complete loss of nitrogen-ﬁ xing activity, indicating an indispensable role for Lb to support rhizobial nitrogen ﬁ xation ( Ott et al. 2005 ). In regard to carbon metabolism, nodule-enhanced sucrose synthase, which is the ﬁ rst enzyme to break down photosynthate translocated to nodules from shoots, has been demonstrated to be crucial for nitrogen ﬁ xa- tion by means of the antisense technique ( Baier et al. 2007 ). In a similar way, a nodule-enhanced isoform of phosphoe- nolpyruvate carboxylase has been proven to be involved in the carbon and nitrogen ﬂ ux in nodules, and thus is essential for symbiotic nitrogen ﬁ xation ( Nomura et al. 2006 ). Although Fig. 5 A schematic representation showing the functions of SST1, FEN1 a number of nodule-speciﬁ c putative transporters such as and IGN1 for nitrogen-ﬁ xing symbiosis in L. japonicus nodules. SST1 is aquaporin (nodulin 26) have been identiﬁ ed in the PBM of a sulfate transporter localized in the peribacteroid membrane (PBM) L. japonicus nodules ( Wienkoop and Saalbach 2003 ), their 2 − and transfers SO from plant cytosol to bacteroids (B). FEN1 is exact functions in symbiosis have not yet been resolved. homocitrate synthetase which supplies homocitrate to bacteroids to Studies using various rhizobial mutants have demonstrated support synthesis of the nitrogenase complex. IGN1 is localized in the that transport of dicarboxylates and some amino acids to plasma membrane (PM) and is thought to function in symbiosome (S) bacteroids from the host plant cells is essential for nitrogen and/or bacteroid differentiation and maintenance. ﬁ xation and/or nodule persistence ( Ronson et al. 1981 , Prell et al. 2009 ). Nevertheless, the transporters responsible for those compounds across the PBM remain to be clariﬁ ed. Fix mutants are host plant mutants that form morphologi- The fen1 mutant was isolated and characterized by a system- cally normal nodules with endosymbiotic rhizobia, but exhibit atic effort to screen symbiotic mutants of L. japonicus , and it very low or no nitrogen-ﬁ xing activity, and thus are unable to forms pale pink, small nodules with very low nitrogen-ﬁ xing grow solely dependent on atmospheric nitrogen. Identiﬁ cation activity ( Imaizumi-Anraku et al. 1997 ). The causal gene, FEN1 , of the causal genes of Fix mutants provides important clues was cloned and demonstrated to encode homocitrate synthase for unraveling the host regulation mechanisms of symbiotic (HCS) which is expressed speciﬁ cally in nodule-infected cells nitrogen ﬁ xation. Three L. japonicus genes, SST1 , FEN1 and IGN1 , ( Hakoyama et al. 2009 ). Homocitrate is a quite unusual com- and one M. truncatula gene, DNF1 , have been identiﬁ ed by pound in the higher plant kingdom, and indeed it was found analyses of Fix mutants ( Table 1 ). abundantly only in legume nodules, whereas it is barely detect- A symbiotic sulfate transporter ( SST1 ) gene was found by able in nodules formed on the fen1 mutants. Homocitrate is map-based cloning from an L. japonicus Fix mutant sst1 known to be a component of iron–molybdenum cofactor ( Krusell et al. 2005 ). Expression of the SST1 gene is speciﬁ c to (FeMo-co) in the nitrogenase complex, on which nitrogen ﬁ xa- nodule-infected cells and its product is found to function as tion is thought to occur ( Hoover et al. 1987 ). NIFV , which a high afﬁ nity sulfate transporter by its ability to complement encodes HCS, has been identiﬁ ed from many diazotrophs and a Saccharomyces cerevisiae sulfate transporter mutant. SST1 shown to be essential for their nitrogenase activity ( Hoover has been shown to be localized in the PBM ( Wienkoop and et al. 1987 , Zheng et al. 1997 ). However, the NIFV orthologs are Saalbach 2003 ). Sulfur has special importance in bacteroids as not found in most of the Rhizobium species which exert highly a component of metal–sulfur clusters within the nitrogenase efﬁ cient nitrogen ﬁ xation only in symbiotic association with complex and the related electron transfer proteins. Thus SST1 compatible host legumes. Therefore, it is very likely that nodule- could meet the high demand for sulfur by bacteroids inside speciﬁ c HCS encoded in the host legume genome could com- symbiosomes to support nitrogen ﬁ xation ( Fig. 5 ). Other sulfate pensate for the lack of NIFV in endosymbiotic rhizobia by transporter genes are also expressed in nodules of L. japonicus , supplying homocitrate to bacteroids from the host cell cyto- but none of them can compensate for the defect in SST1 plasm ( Fig. 5 ). This hypothesis was conﬁ rmed by the fact that function in the sst1 mutants. This indicates that acquisition of M. loti carrying the FEN1 gene or an authentic NIFV from a specialized form of symbiotic sulfate transporter by legumes Azotobacter vinelandii perfectly rescued the defect in nitrogen during evolution allowed legumes to fulﬁ ll efﬁ cient nitrogen ﬁ xation of the fen1 mutants. These ﬁ ndings highlighted the ﬁ xation activity by symbiotic rhizobia. complementary and indispensable partnership between legumes Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. 1391 H. Kouchi et al. and rhizobia in symbiotic nitrogen ﬁ xation. Furthermore, this provides impetus for exploring the co-evolution of legume plants and Rhizobium bacteria ( Hakoyama et al. 2009 ). In general, nodules formed on Fix mutants show more or less premature senescence, such as highly vacuolated infected cells and irregularly enlarged symbiosomes. The nodules formed on an L. japonicus Fix mutant ign1 are characterized by very rapid and severe premature senescence, followed by disruption of the integrity of the whole infected cell. The causal gene, IGN1 , encodes a novel ankyrin-repeat membrane protein, and is shown to be present in the plasma membrane ( Kumagai Fig. 6 A model for a nodule-specific secretory pathway of NCR et al. 2007 ). IGN1 expression is not speciﬁ c to nodules, but is peptides to direct symbiosome development and terminal also detected in all organs of L. japonicus plants at low levels. differentiation of bacteroids in indeterminate nodules. A signal Nevertheless, the mutant phenotype appears only with the peptidase complex (SPC), a component of which has been identiﬁ ed symbiotic defect, suggesting a role for IGN1 in surveillance or as DNF1, is required for targeting the nodule-speciﬁ c cysteine-rich control of responses to biotic infection. Based on these results, (NCR) peptides to the symbiosome. NCR peptides are thought to be it has been hypothesized that IGN1 is required for preventing incorporated into bacteroids, leading to terminal differentiation of the host plant cells from inappropriately invoking a defense bacteroids. CW, cell wall; PM, plasma membrane; ER, endoplasmic system against compatible microsymbionts, thus being essen- reticulum; IT, infection thread. tial for differentiation and/or persistence of bacteroids and symbiosomes, although the exact biochemical function of IGN1 is still to be elucidated. In M. truncatula , nodule-speciﬁ c cysteine-rich (NCR) pep- in the near future is the establishment of an efﬁ cient gene tagging tides were shown to be the host plant factors which direct system using endogenous retrotransposons represented by symbiotic rhizobia into terminal bacteroid differentiation LORE1 in L. japonicus ( Fukai et al. 2010 ), which could be ( Van de Velde et al. 2010 ). The NCR peptides are most similar applicable for both forward and reverse genetics. to defensin-type antimicrobial proteins, and have a signal pep- There has been remarkable progress in our understanding of tide which targets them into the secretory pathway. DNF1 , the host regulation of endosymbiosis with microbes in recent which encode a component of the signal peptidase complex, years. However, our current knowledge still remains, as a whole, was identiﬁ ed as the causal gene of an M. truncatula Fix mutant at the stage of the identiﬁ cation of individual components dnf1 and was shown to be highly expressed in nodules ( Wang involved in symbiotic signaling and/or functions. Deﬁ nition of et al. 2010 ). In the dnf1 mutants, differentiation of rhizobia to the exact biochemical functions of the gene products identiﬁ ed bacteroids and symbiosome organogenesis are both blocked and analyses of their spatio-temporal regulation, their epistatic/ at early stages of nodule development. Interestingly, in the hypostatic relationships and of their interactions, including dnf1 mutants, an NCR peptide was not properly targeted to the search for novel interactors, are required to clarify the basic the bacteroids ( Van de Velde, 2010 ). These results indicate scheme of gene networks that govern the symbiotic process that the host plants control the differentiation of rhizobia from mutual recognition, rhizobial infection, nodule formation into bacteroids by targeting NCR peptides through the and establishment of a functional (nitrogen-ﬁ xing) symbiosis. nodule-speciﬁ c protein secretory system in indeterminate To investigate these aspects in greater detail, cytological nodules ( Fig. 6 ). In contrast, no NCR genes have been found (including bio-imaging analyses), biochemical (protein–protein in the genomes of legumes that form determinate nodules, interactions) and physiological (metabolism and transport implying that alternative host plant mechanism(s) may be in nodules) approaches will have even greater importance in responsible for regulating bacteroid differentiation in these future studies. In addition, phylogenetic and comparative legume species. genomics approaches promise better understanding of how legumes have elaborated such a sophisticated association with soil bacteria. Now that the basic infrastructures for whole- genome sequencing, and the innovative tools for transcrip- Concluding remarks and prospects tome, proteome and metabolome analyses and their databases, Based on the establishment of genetic resources of the model are being established very rapidly, not only for the model legumes, > 40 host legume genes or loci essential for microbial legumes but also for the most important legume crop, soybean, endosymbiosis have been identiﬁ ed so far (this review; see also research on plant–microbe symbiotic interactions will move Sandal et al. 2006 , Oldroyd and Downie 2008 ). Isolation of into new avenues in the ‘post-genome era’. Obviously, the large genes by a forward genetics approach from symbiotic mutants number of symbiotic mutants and cloned genes that have generated by conventional mutagenesis methodology appears been accumulated during the past decade could be the most to be practically reaching saturation. One promising approach powerful basis for such avenues of research. 1392 Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. Legume genes involved in symbiosis Borisov , A.Y. , Madsen , L.H. , Tsyganov , V.E. , Umehara , Y. , Voroshilova , V.A. , Funding Batagov , A.O. , et al . ( 2003 ) The sym35 gene required for root nodule development in pea is an ortholog of nin from Lotus japonicus . The Ministry of Agriculture, Forestry, and Fisheries of Japan Plant Physiol. 131 : 1009 – 1017 . [Rice Genome Project Grant PMI-0001 to H.I.-A. and M.H.]; the Caetano-Anolles , G. and Gresshoff , P.M. 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Copyright: © The Author 2010. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.
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DOI: 10.1093/pcp/pcq107
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Abstract

Special Issue – Mini Review How Many Peas in a Pod? Legume Genes Responsible for Mutualistic Symbioses Underground 1, 1 1 1,4 Hiroshi Kouchi * , Haruko Imaizumi-Anraku , Makoto Hayashi , Tsuneo Hakoyama , 1 1 2 3 Tomomi Nakagawa , Yosuke Umehara , Norio Suganuma and Masayoshi Kawaguchi Department of Plant Sciences, National Institute of Agrobiological Sciences, Tsukuba, 305-8602 Japan Department of Life Science, Aichi University of Education, Kariya, 448-8542 Japan Department of Evolutionary Biology and Biodiversity, National Institute for Basic Biology, Okazaki, 444-8585 Japan Present address: Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, 113-8657 Japan * Corresponding author: E-mail, [email protected] ; Fax, + 81-29-838-8347 (Received May 28, 2010; Accepted July 17, 2010) The nitrogen-ﬁ xing symbiosis between legume plants and Rhizobium , in which endosymbiotic rhizobia ﬁ x atmospheric Rhizobium bacteria is the most prominent plant–microbe nitrogen. Our understanding of this agriculturally important endosymbiotic system and, together with mycorrhizal fungi, endosymbiosis has been greatly advanced during the last has critical importance in agriculture. The introduction of two decades. The discovery of rhizobial symbiotic signal two model legume species, Lotus japonicus and Medicago molecules [Nod factors (NFs)] in the early 1990s was a signiﬁ - truncatula , has enabled us to identify a number of host cant breakthrough which led to elucidation of the basic legume genes required for symbiosis. A total of 26 genes scheme of rhizobial nodulation ( Nod ) gene functions (for a have so far been cloned from various symbiotic mutants review, see Spaink 1995 ). NFs are chitin ( N -acetylglucosamine of these model legumes, which are involved in recognition oligomers) derivatives, of which the non-reducing end is of rhizobial nodulation signals, early symbiotic signaling N -acylated and the reducing end is modiﬁ ed by various cascades, infection and nodulation processes, and regulation molecules. These speciﬁ c NF structures determine the strict of nitrogen ﬁ xation. These accomplishments during the speciﬁ city between Rhizobium and host legume species, and past decade provide important clues to understanding not elicit both the rhizobial infection process and the initiation only the molecular mechanisms underlying plant–microbe of nodule primordia in the roots of the compatible host endosymbiotic associations but also the evolutionary aspects legumes. of nitrogen-ﬁ xing symbiosis between legume plants and Molecular identiﬁ cation of NFs and successive vast progress Rhizobium bacteria. In this review we survey recent progress in understanding the functions of bacterial Nod genes have in molecular genetic studies using these model legumes. promoted investigation into host legume genes essential for endosymbiosis, including mycorrhizal symbiosis, which is evo- Keywords: Lotus japonicus • Medicago truncatula • Model lutionarily related to the legume– Rhizobium symbiosis. To this legumes • Nitrogen ﬁ xation • Nodules • Plant–microbe aim, utilization of two model legume species, Lotus japonicus symbiosis . and Medicago truncatula , was proposed, because they are self- Abbreviations : AM , arbuscular mycorrhizal ; AON , fertile diploids with relatively small genome size and short autoregulation of nodulation ; CaM , calmodulin ; CCaMK , generation periods, and are capable of molecular transfection 2 + Ca - and calmodulin-dependent protein kinase ; CCD , ( Barker et al. 1990 , Handberg and Stougaard 1992 ). On the cortical cell division ; CSP , common symbiosis pathway ; HCS , basis of the resources established for genome research in homocitrate synthase ; IT , infection thread ; Lb , leghemoglobin ; these model legumes, a number of host legume genes LRR , leucine-rich repeat ; LysM-RK , LysM receptor-like kinase ; involved in NF perception and subsequent symbiotic signal NCR , nodule-speciﬁ c cysteine-rich ; NF , Nod factor ; PBM , transduction, bacterial infection and nodule organogenesis, peribacteroid membrane ; RN , root nodule. and regulation of nitrogen ﬁ xation have been identiﬁ ed in the past decade ( Table 1 ). In this review, we present a survey of the current status of our knowledge about host legume genes Introduction and mechanisms underlying the mutualistic endosymbiotic Legume plants are able to form root nodules (RNs) by associations with microbes, focusing mainly on nitrogen-ﬁ xing symbiotic association with soil bacteria collectively termed symbiosis between legume plants and rhizobia. For mycorrhizal Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107, available online at www.pcp.oxfordjournals.org © The Author 2010. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.5), which permits unrestricted non-commercial use distribution, and reproduction in any medium, provided the original work is properly cited. Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. 1381 H. Kouchi et al. Table 1 Cloned genes involved in legume– Rhizobium symbiosis Genes in model Mutant phenotypes Gene product Possible function Legume orthologs References legumes b c d Inf Nod EC LjNFR1 , MtLYK3 − − − LysM receptor kinase NF receptor PsSYM37 1, 2, 3 LjNFR5 , MtNFP − − − LysM receptor kinase NF receptor GmNFR5 , PsSYM10 1, 4, 5 LjSYMRK , MtDMI2 − − − LRR receptor kinase CSP MsNORK , PsSYM19 6, 7 2 + LjCASTOR − − − Ca -gated ion channel CSP 8 2 + LjPOLLUX , MtDMI1 CSP PsSYM8 8,9 − − − Ca -gated ion channel LjNUP133 − − − Nucleoporin CSP 10 LjNUP85 Nucleoporin CSP 11 − − − 2 + 2 + LjCCaMK , MtDMI3 − − − Ca /CaM-dependent CSP (putative Ca signal PsSYM9 12, 13 kinase decoder) LjCYCLOPS , MtIPD3 ± ± − Nuclear protein CSP (CCaMK interactor) 14, 15 IT growth LjNIN , MtNIN − − − Putative transcription Infection, CCD PsSYM35 16, 17, 18 factor LjNSP1 , MtNSP1 GRAS family transcription Infection, CCD 19, 20 − − − regulator LjNSP2 , MtNSP2 − − − GRAS family transcription Infection, CCD PsSYM7 19, 20, 21 regulator LjLHK1 , ( MtCRE1 ) + ± − Cytokinin receptor kinase Nodule organogenesis 22, 23, 24 LjNAP1 ± ± − Component of F-actin IT growth 25 condensing complex LjPIR1 ± ± − Component of F-actin IT growth 25 condensing complex LjHAR1 , MtSUNN LRR receptor kinase AON GmNARK, PsSYM29 26, 27, 28 + + + + + MtSICKLE + + + + + + EIN2 (ethylene-insensitive) Regulation of IT growth 29 LjASTRAY + + + + bZIP transcription factor Regulation of nodulation 30 LjCERBERUS , MtLIN ± ± − Putative E3 ubiquitin ligase IT growth 31, 32 MtERN1 ± ± − ERF transcription factor IT growth 33 MtRPG Novel coiled-coil protein IT growth 34 ± ± − MtNIP/LATD + ± ± NTR1 transporter IT growth 35 LjFEN1 + + + Homocitrate synthase Nitrogenase biosynthesis GmN56 36, 37 LjIGN1 + + + Ankyrin repeat membrane Bacteroid maintenance 38 protein LjSST1 + + + Sulfate transporter Transport SO to bacteroids 39 MtDNF1 + + + Signal peptidase subunit Symbiosome and/or 40 bacteroid differentiation Only the genes identiﬁ ed by forward genetics are listed in this table. Many other genes have been demonstrated or suggested to be involved in symbiosis by the reverse genetics approach and/or expression proﬁ les (see details in the text). Lj and Mt at the beginning of the gene names indicate Lotus japonicus and Medicago truncatula , respectively. Inf = formation of infection threads (ITs) penetrating into the cortex. ± indicates occasional IT formation within root hair cells. Nod = nodule formation. ± indicates the formation of bumps (arrest of nodule development). EC = endocytosis of rhizobia inside nodules. ± indicates development of nodule-infected cells at low frequency compared with the wild type nodules. Ps, Pisum sativum ; Gm, Glycine max ; Ms, Medicago sativa . Common symbiosis pathway. Cortical cell division. Autoregulation of nodulation References: 1, Radutoiu et al. (2003) ; 2, Limpens et al. (2003) ; 3, Smit et al. (2007) ; 4, Madsen et al. (2003) ; 5, Arrighi et al. (2006) ; 6, Stracke et al. (2002) ; 7, Endre et al. (2002) ; 8, Imaizumi-Anraku et al. (2005) ; 9, Anè et al. (2004) ; 10, Kanamori et al. (2006) ; 11, Saito et al. (2007) ; 12, Tirichine et al. (2006) ; 13, Levy et al. (2004) ; 14, Yano et al. (2008) ; 15, Messinese et al. (2007) ; 16, Schauser et al. (1999) ; 17, Marsh et al. (2007) ; 18, Borisov et al. (2003) ; 19, Heckmann et al. (2006) ; 20, Kalo et al. (2005) ; 21, Murakami et al. (2006) ; 22, Murray et al. (2007) ; 23, Tirichine et al. (2007) ; 24, Gonzalez-Rizzo et al. (2006) ; 25, Yokota et al. (2009) ; 26, Nishimura et al. (2002a) ; 27, Krusell et al. (2002) ; 28, Schnabel et al. (2005) ; 29, Penmetsa et al. (2008) ; 30, Nishimura et al. (2002b) ; 31, Yano et al. (2009) ; 32, Kiss et al. (2009) ; 33, Middleton et al. (2007) ; 34, Arrighi et al. (2008) ; 35, Yendrek et al. (2010) ; 36, Hakoyama et al. (2009) ; 37, Kouchi and Hata (1995) ; 38, Kumagai et al. (2007) ; 39, Krusell et al. (2005) ; 40, Wang et al. (2010) . 1382 Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. Legume genes involved in symbiosis symbiosis, the most up to date knowledge was presented in detail in a recent review by Hata et al. (2010) . Perception of microbial signals Putative NF receptors have been identiﬁ ed in various legume species: NFR1 and NFR5 from L. japonicus ( Madsen et al. 2003 , Radutoiu et al. 2003 ) and from Glycine max ( Indrasumunar et al. 2010 ); LYK3 and NFP from M. truncatula ( Limpens et al. 2003 , Arrighi et al. 2006 ); and SYM37 and SYM10 from Pisum sativum ( Zhukov et al. 2008 ). These putative NF receptors have a common structure composed of a single-pass trans- membrane domain anchored to an extracellular lysin motif (LysM) receptor domain and an intracellular kinase domain, and are thus termed LysM receptor-like kinases (LysM-RKs). Most of their loss-of-function mutants lack any of the responses to rhizobial inoculation as well as to puriﬁ ed NFs. The LysM domain is known to be involved in binding peptidoglycan and/or structurally related molecules, such as chitin oligosac- charides. At present, however, no structural study has been carried out on the interactions of LysM domains with speciﬁ c NF structures. In L. japonicus , NFR1 and NFR5 are thought to form a recep- tor complex (most possibly a heterodimer) responsible for speciﬁ c recognition of NFs secreted from Mesorhizobium loti , a Rhizobium species compatible with L. japonicus ( Fig. 1 ), because their co-transformation has been shown to be able to extend the host range of M. loti to the heterologous plant Fig. 1 Recognition of Nod factors by NFR1 and NFR5 in L. japonicus . species ( Radutoiu et al. 2007 ). Since the intracellular domain of Extracellular LysM domains are thought to be responsible for binding LjNFR5 has been shown to lack the kinase activity ( Madsen Nod factors, and then transduce the symbiotic signals through the et al. 2003 ), LjNFR1 could be crucial for transmitting the intracellular kinase of NFR1 to downstream signaling cascades, leading intracellular signal to downstream symbiotic signaling path- to rhizobial infection and nodulation. PM, plasma membrane. ways. Indeed, the kinase activity of NFR1 was demonstrated to be essential for activating downstream symbiotic signaling pathways in L. japonicus (T. Nakagawa, unpublished result). however, it should be noted that legume plants have a large In M. truncatula , NFP is thought to be an ortholog of NFR5 number of LysM-RKs compared with non-legumes. For exam- ( Arrighi et al. 2006 ) and its mutant shows no response to ple, the L. japonicus genome contains at least 17 LysM-RKs and NFs puriﬁ ed from Sinorhizobium meliloti , a Rhizobium species they are all expressed, while Arabidopsis and rice have ﬁ ve and compatible with Medicago plants ( Amor et al. 2003 ). However, six LysM-RK genes in their genome, respectively ( Lohmann et al. the M. truncatula hcl mutant of LYK3 , which is proposed 2010 ). Analysis of the whole-genome sequences suggested that to be an ortholog of NFR1 , retains the earliest responses upon the LysM-RK gene family has further diversiﬁ ed by tandem and 2 + inoculation with S. meliloti , such as Ca spiking and root hair segmental duplication in legumes (Zhang et al. 2007, Lohmann deformation ( Wais et al. 2000 , Catoira et al. 2001 , Smit et al. et al. 2010 ). These ﬁ ndings raise the possibility that NF percep- 2007 ). Therefore, the positions of NFR1 and LYK3 in symbiotic tion and subsequent intracellular signaling are mediated by signaling appear not to be identical. In Medicago plants, complex combinations of multiple LysM-RKs including those a model composed of two distinct NF receptors, i.e. signaling other than NFR1 and NFR5 ( Oldroyd and Downie, 2008 ). and entry receptors, has been proposed ( Ardourel et al. 1994 , Thus the exact mechanisms of the host recognition of NFs are Smit et al. 2007 ). These two receptors (or receptor complexes) still elusive. are postulated to have different levels of requirements with It is intriguing that a chitin receptor, CERK1, in Arabidopsis regard to NF structures, and to be responsible differentially has been demonstrated to be essential to induce plant innate for infection thread (IT) formation and nodule organogenesis. immunity against fungal pathogens ( Miya et al. 2007 ), because In L. japonicus , a single receptor complex composed of NFR1 CERK1 is a LysM-RK which belongs in the same phylogenic and NFR5 appears to be responsible for the activation of clade as NF receptors such as NFR1 and LYK3. In particular, both infection and nodulation processes ( Hayashi et al. 2010 , its intracellular kinase domain shows high similarity (approxi- Madsen et al. 2010 ; see details in the next section). In this regard, mately 67 % identity) to that of NFR1. Based on the structural Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. 1383 H. Kouchi et al. similarity together with the microsynteny in the Arabidopsis organogenesis ( Kevei et al. 2007 ). SIP is a novel DNA-binding and Lotus genome around CERK1 and NFR1, it has been pro- protein with an AT-rich domain (ARID), which speciﬁ cally posed that these LysM-RKs are the descendants of a common binds to the promoter of NIN ( Zhu et al. 2008 ). These results ancestor ( Zhu et al. 2006 ). Indeed, NFR1 has been shown to suggest that SYMRK also participates directly or indirectly in retain the ability to activate transiently defense-related genes nodulation-speciﬁ c pathways that follow the CSP. 2 + in response to puriﬁ ed NFs (T. Nakagawa, unpublished results). CASTOR and POLLUX , both of which encode Ca -gated It is of great interest to elucidate how these structurally related cation (most probably potassium) channel proteins, have been LysM-RKs induce apparently opposite biological responses in identiﬁ ed as members of the CSP in L. japonicus ( Imaizumi- their host plants; one induces endosymbiotic association and Anraku et al. 2005 , Charpentier et al. 2008 ). Despite their high the other induces defense reactions. Addressing this question structural similarity, a single mutation of CASTOR or POLLUX in more detail would provide new direction in the analysis of caused symbiosis-defective phenotypes, indicating that they the evolutionary process of the legume– Rhizobium symbiosis. fulﬁ ll a symbiotic function(s) in combination. In contrast, only DMI1 , an ortholog of POLLUX , has been identiﬁ ed from symbi- osis-defective mutants of M. truncatula ( Anè et al. 2004 ). It is Early symbiotic signaling noteworthy that in rice, a monocotyledonous mycorrhizal About half of the non-nodulating legume mutants isolated so plant, the requirement for both OsCASTOR and OsPOLLUX far are also defective in arbuscular mycorrhizal (AM) symbiosis, in AM symbiosis has been proven ( Banba et al. 2008 , Gutjahr implying that the genes responsible for those mutants are et al. 2008 , Chen et al. 2009 ). Similarly to L. japonicus , a single required for both RN and AM symbioses. Thus, the signal trans- mutation of either OsCASTOR or OsPOLLUX results in the duction pathway mediated by those genes is termed the abortion of AM infection, indicating that functional collabora- ‘common symbiosis pathway’ (CSP). In L. japonicus , seven genes tion between these ‘twin’ genes is also the case in rice. Thus, so far have been positioned in the CSP ( Table 1 ). The range of considering the requirement for CASTOR and POLLUX, which symbiosis-defective phenotypes of the CSP genes indicates are very closely structurally related to each other, in Lotus , rice that they are grouped into two categories; one is positioned and probably in the ancestral lineage of mycorrhizal plants, it upstream (upstream genes) and the other is downstream of appears intriguing that in Medicago , DMI1 probably has been 2 + Ca spiking, which is a central physiological reaction in the endowed during evolution with a function which integrates CSP ( Ehrhardt et al. 1996 , Miwa et al. 2006 ). these ‘twin’ channel proteins. It is still an open question how Following the perception of NFs through LysM-RKs (see CASTOR and POLLUX share their functions in symbiotic signal- 2 + 2 + above), biphasic Ca signaling is induced in root hair cells, i.e. ing processes leading to generation of Ca spiking. The cellular 2 + a rapid inﬂ ux of Ca into the root hair cells and then periodical localization of these components is something of a mystery 2 + oscillation of cytosolic Ca concentrations at the perinuclear at present. They have been reported to be localized in the 2 + 2 + region (Ca spiking). Ca spiking is also induced in response nuclear envelope ( Riely et al. 2007 , Charpentier et al. 2008 ), to AM infection, and is critical for AM symbiosis as well as RN while L. japonicus CASTOR and POLLUX have a signal peptide symbiosis ( Kosuta et al. 2008 ). In L. japonicus , ﬁ ve out of seven which is predicted to be a plastid targeting signal, and have CSP genes, SYMRK , CASTOR , POLLUX , NUP85 and NUP133 , are been shown to be in plastids when expressed under the 2 + required for the induction of Ca spiking ( Stracke et al. 2002 , control of the cauliﬂ ower mosaic virus (CaMV) 35S promoter Imaizumi-Anraku et al. 2005 , Kanamori et al. 2007, Saito et al. ( Imaizumi-Anraku et al. 2005 , Charpentier et al. 2008 ). Further 2007 ), whereas CCaMK and CYCLOPS are positioned down- evaluation of the spatio-temporal gene expression and cellular 2 + stream of Ca spiking ( Tirichine et al. 2006 , Yano et al. 2008 ), localization of CASTOR and POLLUX is required. and thus they have been thought to play important roles in Both nup85 and nup133 mutants show temperature-sensitive 2 + transmitting symbiotic signals mediated by Ca signals to the symbiosis-defective phenotypes. Rhizobial and AM infections downstream RN- and AM-speciﬁ c pathways. are aborted in the epidermis at high temperature, while normal SYMRK and DMI2 , which encode LRR (leucine-rich repeat)- invasion of the microsymbionts occurs on the roots of both receptor kinases, have been isolated from L. japonicus and mutants under the normal temperature regime ( Kanamori M. truncatula , respectively ( Endre et al. 2002 , Stracke et al. 2002 ). et al. 2006 , Saito et al. 2007 ). Based on the sequence similarity Because of their cellular localization in the plasma membrane to mammalian nucleoporins, both NUP85 and NUP133 are ( Limpens et al. 2005 ), SYMRK/DMI2 are believed to be the predicted to be the components of the NUP107–NUP160 sub- starting point of the CSP, although the ligand(s) of their complex, which is located on both sides of the nuclear pore extracellular receptor domains are still unknown. Screening ( Meier and Brkljacic 2009 ). Because symbiotic NF-responsive 2 + of interacting factors with SYMRK/DMI2 kinase domains Ca spiking is associated with the root hair cell nucleus, NUP85/ resulted in isolation of HMGR1 from M. truncatula and SIP NUP133 are postulated to be involved in transport or localiza- 2 + from L. japonicus . HMGR1 encodes a putative mevalonate tion of the factor(s) needed for the induction of Ca spiking. 2 + synthase which is involved in the synthesis of isoprenoid Ca - and calmodulin (CaM)-dependent protein kinase, compounds. Knock-down analysis of HMGR1 suggested its CCaMK, consists of three functional domains, i.e. a serine/ involvement in the rhizobial infection process and nodule threonine-kinase domain, a CaM-binding (autoinhibitory) 1384 Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. Legume genes involved in symbiosis T265D domain (CaMBD) and a domain of three EF hands which inter- CCaMK or kinase-only CCaMK mimic the activated status 2 + 2 + act with Ca ions. As its name and domain organization sug- of CCaMK in response to Ca spiking in vivo, these data sug- 2 + gest, CCaMK is a putative decoder of Ca signals. CCaMK was gest a possible function for CCaMK as the connecting point of ﬁ rst isolated from lily ( Lilium longiﬂ orum ), and biochemical two signaling pathways which are split from the NF receptors. analyses have shown that its kinase activity is dependent on An intriguing subject for the future will be to address the 2 + 2 + 2 + interactions with Ca and CaM ( Patil et al. 1995 ). However, hypothesis that two different Ca signals, i.e. Ca inﬂ ux and 2 + CCaMK function during plant growth has remained elusive Ca spiking, are prerequisite in order to exceed the threshold for a long time. Isolation and characterization of dmi3/ of CCaMK activity required for intracellular infection of snf1/ccamk mutants produced an answer to the question. rhizobia. M. truncatula dmi3 and L. japonicus ccamk mutants are defec- Recently, Lefebvre et al. (2010) isolated a symbiotic remorin, 2 + tive in both RN and AM symbioses, though Ca spiking is MtSYMREM1 from M. truncatula , which is exclusively expressed induced in response to rhizobial inoculation and to NF applica- in the nodulation process. Remorins are the ﬁ lamentous pro- tion in these mutants ( Levy et al. 2004 , Tirichine et al. 2006 ). teins that have been implicated to have scaffolding functions Furthermore, spontaneous nodulation in the absence of rhizo- generally in the cell membrane, and some members of this bia was induced by gain-of-function mutation of CCaMK, in multigene family have been described to be involved in biotic which Thr265 at the autophosphorylation site of the kinase interactions in plants ( Lefebvre et al. 2010 ). The most promi- domain is substituted by isoleucine ( snf1 , Tirichine et al. 2006 ) nent feature of MtSYMREM1 is that it interacts with LYK3, NFP or aspartate ( Gleason et al. 2006 ), indicating a pivotal role for and DMI2, which are the orthologs of NFR1, NFR5 and SYMRK CCaMK in nodule organogenesis. in L. japonicus , respectively. In nodulated roots of Medicago , Recent studies showed that introduction of the snf1 genetic MtSYMREM1 was localized in the plasma membrane enclosing T265D background or CCaMK into L. japonicus mutants of the ITs as well as in the symbiosome membrane. These ﬁ ndings CSP genes ( SYMRK , CASTOR , POLLUX , NUP85 and NUP133 ), suggest that SYMREM1 plays a role in retaining LysM-RKs and 2 + which are positioned upstream of Ca spiking, suppressed loss- SYMRK in the plasma membrane at the growing IT tips, thus 2 + of-function mutation of these mutants, not only rhizobial but enabling continuous operation of Ca signaling mediated by also AM infection ( Hayashi et al. 2010 , Madsen et al. 2010 ). LysM-RKs and CSP components. Such continuation of the 2 + This indicates that these upstream genes are solely required Ca signaling at the interface with rhizobia allows the host 2 + for the generation of Ca spiking. In contrast, expression of cells to support the IT elongation and penetration into cortical T265D CCaMK in either nfr1 or nfr5 did not alter their infection cells ( Fig. 2B ). defects, although it could induce nodule organogenesis in The RN symbiosis is presumed to have its evolutionary origin these mutants irrespective of the presence or absence of in the more ancient AM symbiosis and to have evolved by M. loti ( Hayashi et al. 2010 ). The snf1/nfr1/nfr5 triple mutants recruiting the pre-existing CSP genes ( Markmann and Parniske allowed rhizobia to invade through an ‘intercellular’ route 2009 ). Given the fact that CSP regulates two different symbiosis (so-called ‘crack entry’) at a very low frequency, but in that case systems in legumes, it is plausible that the CSP has retained its 2 + rhizobial infection was not accompanied by the formation of functions, i.e. a generator and transmitter of Ca spiking for ITs within root hairs ( Madsen et al. 2010 ). Thus the gain-of- the establishment of AM symbiosis, during acquisition of RN function form of CCaMK alone is sufﬁ cient to induce nodule symbiosis in legume plants. Indeed, rice orthologs of CASTOR, organogenesis, while intracellular accommodation of rhizobia POLLUX, CCaMK and CYCLOPS, which all have conserved through root hair ITs requires an additional signaling pathway domain structures between Lotus and rice, could restore the derived from NFR1 and NFR5, which is distinct from that defects in rhizobial infection of the corresponding Lotus mutant 2 + involving Ca spiking mediated by the CSP upstream genes lines, indicating the functional conservation of these CSP genes 2 + ( Fig. 2A ; Hayashi et al. 2010 ). In this regard, Ca inﬂ ux is a pos- in legumes and non-legumes ( Banba et al, 2008 , Yano et al. sible candidate for involvement in this additional signaling 2008 ). One exception is SYMRK; a monocot SYMRK from rice 2 + pathway, because generation of Ca inﬂ ux is dependent on has only one LRR and a non-legume dicot SYMRK from tomato NFR1/NFR5, but not on the CSP genes ( Miwa et al. 2006 ). As has two LRRs, while legume SYMRKs and those of actinorhizal shown in Fig. 2A , the integration point of the two pathways is plants which are involved in nitrogen-ﬁ xing symbiosis with postulated to be at or around CCaMK. The essentiality of the the actinomycetes Frankia have three LRRs. In addition, rice 2 + Ca binding capacity of CCaMK for rhizobial infection has SYMRK lacks an extended N-terminal domain of unknown also been shown by kinase-only CCaMK which lacks both the function. Cross-species complementation tests demonstrated CaMBD and EF hands. Introduction of the kinase-only CCaMK that the shorter version of SYMRK could restore the defect in into M. truncatula dmi3 mutants resulted in induction of spon- AM symbiosis but not RN symbiosis in Lotus symrk mutants, taneous nodulation, while rhizobial infection did not occur while a ‘full-length’ version from the nodulating clade could upon inoculation with S. meliloti ( Gleason et al. 2006 ), suggest- restore both AM and RN symbioses ( Markmann et al. 2008 ). 2 + ing that binding of Ca ions to CCaMK per se, or the activated Therefore, there are divergent evolutionary pathways among 2 + status of CCaMK through Ca signaling, is prerequisite for the CSP genes, and SYMRK has a distinctive position as an rhizobial infection. Although it remains unclear to what extent adaptive factor for the evolution of RN symbiosis in legumes. Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. 1385 H. Kouchi et al. Fig. 2 A current model of early symbiotic signaling pathways. (A) The gene cascades in early symbiotic signaling (modiﬁ ed from Hayashi et al. 2010 ). In response to Nod factors, the signal generated by NFR1/NFR5 splits into two pathways; one ﬂ ows into the common symbiosis pathway (CSP, blue line) and the other (pink line) is prerequisite for successful infection of rhizobia. The genes of CSP components are indicated by green 2 + letters. (B) The proposed roles of Ca signaling and CCaMK activation in infection thread formation and growth. The exact localization and composition of the NF receptor complex(es) have not yet been determined. 2 + Since it has been shown that Ca spiking has different signa- to internal and external cues. An important internal cue is tures dependent on RN or AM symbiotic interactions ( Kosuta a systemic feedback regulatory system involving long-distance et al. 2008 ), such diversiﬁ cation of SYMRK as the entrance to root–shoot signaling, termed autoregulation of nodulation the CSP may lead to the transmission of RN- and AM-speciﬁ c (AON), which is shown to be closely linked with early symbiotic signals to the downstream pathways through the activation signaling triggered by NFs ( Caetano-Anollés and Gresshoff 1991 , 2 + status of CCaMK mediated by different Ca signatures. Con- Oka-kira and Kawaguchi 2006 ). AON is believed to consist of versely, CSP genes other than SYMRK have basically kept their two presumptive long-distance signals, i.e. root-derived and functions throughout the evolution of the RN symbiosis in shoot-derived signals. The root-derived signal is generated in legumes, and thus constituted the foundation of the CSP in roots in response to rhizobial NFs and then translocated to the the course of evolution ( Banba et al. 2008 ). shoot, while the shoot-derived signal is generated in shoots and then translocated to the root to restrict further nodulation ( Fig. 3 ; Magori and Kawaguchi 2009 ). Mutants defective in AON, such as G. max nts / nark , L. japonicus har1 , M. truncatula Systemic regulation of symbiosis sunn and P. sativum sym29 , display a so-called ‘hypernodula- Although symbiotic nitrogen ﬁ xation is highly beneﬁ cial to tion’ phenotype ( Carroll et al. 1985 , Sagan and Duc 1996 , Wop- legume hosts, excessive nodulation interferes with plant ereis et al. 2000 , Penmetsa et al. 2003 ). Grafting experiments growth because nodulation and nitrogen ﬁ xation require a high indicated that these mutants are defective in the production of energy cost. To balance the symbiosis, legume plants develop shoot-derived signals. The responsive genes have been shown speciﬁ c mechanisms to control the nodule number in response to encode an LRR receptor-like kinase ( Krusell et al. 2002 , 1386 Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. Legume genes involved in symbiosis HAR1 (H. Miyazawa et al. unpublished data). Thus, KLV and HAR1 are likely to function coordinately to receive the root- derived signal in the shoot. The shoot-regulated hypernodula- tion and fasciated stem phenotypes of klv are shared with P. sativum sym28 and nod4 ( Sagan and Duc 1996 , Sidorova and Shumnyi 2003 ). Molecular identiﬁ cation of these genes might shed light on a common mechanism to connect RN- and legume-speciﬁ c shoot apical meristem regulation. The next important question is the molecular nature of the root-derived signal(s). There is evidence that receptor-like kinases such as HAR1 show a high similarity to Arabidopsis CLV1 . It has been shown recently that an extracellular domain of CLV1 directly binds to a modiﬁ ed CLE peptide processed from CLAVATA3 (CLV3) ( Ogawa et al. 2008 ). The CLE gene encodes a small secreted peptide composed of 12–13 amino acids. In Arabidopsis, the CLE genes constitute a family of at least 31 peptide ligand genes including CLV3 ( Sawa et al. 2006 ). In L. japonicus , at least 39 potential CLE genes have been identi- ﬁ ed in its genome. Among them, small peptides derived from two CLE genes (LjCLE-RS1 and LjCLE-RS2) have been proposed as strong candidates for the root-derived signal ( Okamoto et al. 2009 ), based on the following observations: (i) CLE-RS1/2 are rapidly and signiﬁ cantly up-regulated in response to rhizo- Fig. 3 A model for LRR receptor-like kinase-mediated autoregulation bial inoculation; (ii) perception of NFs and successive compo- of nodulation (AON). (1) Perception of the rhzobial Nod factor nents of the symbiotic signaling pathway such as CASTOR and initiates nodulation but also the production of a long-distance CCaMK are essential for CRE-RS1/2 up-regulation; (iii) overex- inhibitor called the root-derived signal. (2) L. japonicus CLE-RS1 and pression of CLE-RS1/2 in a hairy root system strongly suppresses -RS2 peptides as strong candidates of the root-derived signal may be nodulation; (iv) this inhibitory effect travels systemically from transported to the shoot, and (3) elicit the production of the transformed roots to untransformed roots; and (v) HAR1 is shoot-derived signal. Legume CLV1-like receptor-like kinases such as required for CLE-RS1/2 -mediated suppression of nodulation. HAR1/NARK/SUNN/SYM29 and KLAVIER mediate this process. The entire similarity of CLE-RS1/2 genes is not obvious, but (4) The shoot-derived signal(s) is translocated to the root and the 12 amino acids (PLSPGGPDPQHN) constituting the CLE negatively regulates nodulation via TML/RDH1. Pisum sativum NOD3 domain are identical ( Okamoto et al. 2009 ). Thus, HAR1 may and M. truncatula RDN that function in the root have a role in either the transmission of the root-derived signal or the perception of the perceive one modiﬁ ed CLE peptide derived from two CLE genes shoot-derived signal. in the shoot. In M. truncatula , two CLE genes ( MtCLE12 and MtCLE13 ), which suppress local and systemic nodulation, have been reported ( Mortier et al. 2010 ). Differently from Lotus , the Nishimura et al. 2002a , Schnabel et al. 2005 ), and have high MtCLE12/13 genes are not required for SUNN receptor-like similarity to CLAVATA1 ( CLV1 ) of Arabidopsis ( Clark et al. kinase, suggesting that the other receptor(s) is responsible for 1997 ) and FON1 of rice ( Suzaki et al. 2004 ). CLV1 and FON1 AON-mediated CLE signaling in M. truncatula . are speciﬁ cally expressed in shoot and ﬂ oral meristems, and The perception of the root-derived signal by legume CLV1- restrict their sizes by receiving a CLE peptide derived from the like receptor kinase is then presumed to initiate the production stem cell region ( Miwa et al. 2009 ). In contrast, the legume of the shoot-derived signal(s). Although the chemical nature of genes represented by L. japonicus HAR1 are widely expressed the shoot-derived signal is unknown, foliar application of plant in various organs but not in the shoot apex, suggesting that hormones has produced results indicating that brassinolide these genes uniquely evolved in legumes to produce the and methyl jasmonate may function as the shoot-derived shoot-derived inhibitor of nodulation by receiving the root- signal ( Nakagawa and Kawaguchi 2006 , Terakado et al. 2006 ). derived signal. Alternatively, polar auxin transport has been postulated to Together with HAR1 receptor-like kinase, KLAVIER ( KLV ) is play an important role in long-distance control of nodulation also indispensable for AON signaling in L. japonicus ( Oka-kira ( van Noorden et al. 2006 ). However, the involvement of these et al. 2005 ). The mutation exhibits stem fasciation as well as plant hormones in AON remains elusive, because of the lack of a hypernodulation phenotype. A double mutation analysis a uniﬁ ed explanation. The most reliable strategy to deﬁ ne the indicated that KLV functions in the same genetic pathway as shoot-derived signal would be to ﬁ nd the regulatory factors HAR1 . KLV encodes an LRR receptor-like kinase and is speciﬁ - from leaf extracts using a bioassay system. To characterize the cally expressed in the leaf vascular tissues, as with the case of signal, two research groups have developed novel bioassay Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. 1387 H. Kouchi et al. systems by feeding aqueous leaf extracts directly into the nodulation, and hypernodulation mutants such as nts , har1 , petiole of wild-type and supernodulation nark / NOD1-3 mutant klv and nod3 exhibit more or less nitrate-tolerant phenotypes plants of G. max ( Lin et al. 2010 , Yamaya and Arima 2010 ). Both ( Carroll et al. 1985 , Postma et al. 1988 , Wopereis et al. 2000 , groups succeeded in detecting nodulation suppression activity, Oka-Kira et al. 2005 ). Very recently it has been shown that but their results partly differ. Yamaya and Arima (2010) showed L. japonicus CLE-RS2 is strongly up-regulated in roots in that the suppressive activity of nodulation is constantly response to nitrate ( Okamoto et al. 2009 ). As CLE-RS2 -mediated detected irrespective of Bradyrhizobium japonicum inocula- suppression of nodulation is not observed in the har1 mutants, tion, whereas Lin et al. (2010) showed that the activity is promi- the nitrate-induced CLE-RS2 peptide is likely to suppress nently observed in a B. japonicum -secreted NF-dependent nodulation through HAR1. According to this model, nitrate manner. Further studies using the petiole feeding assay will be tolerance of the hypernodulation mutants can be explained needed to identify the signal molecule(s). because the mutations in NTS and HAR1 lead to defective CLE Root-speciﬁ c hypernodulation mutants have been isolated peptide perception in the presence of nitrate. Thus, CLE-RS2 in P. sativum nod3 ( Postma et al. 1988 ), L. japonicus rdh1 and is most probably a key regulator in nitrogen signaling and tml ( Ishikawa et al. 2008 , Magori et al. 2009 ) and M. truncatula develop mental plasticity that adapts to environmental nitro- rdn (J.A. Frugoli et al. unpublished data). These mutants are gen conditions. thought to be impaired in the translocation of the root- derived signal or in the perception of the shoot-derived signal Infection process and nodule organogenesis if they participate in long-distance root–shoot communication. Among them, L. japonicus TML has been shown by double Infection of rhizobia initially takes place at the root epidermis mutation and grafting analyses to function in the same genetic (root hair cells). The response of root hairs to NFs is restricted pathway as HAR1 . Furthermore, inverted-Y grafting experi- to a particular axial region of roots, the infection zone, where ments revealed that the suppressive effect of TML on nodula- root hairs develop. In order to incorporate rhizobia efﬁ ciently, tion cannot be transmitted systemically from wild-type roots many legumes have evolved a structural pathway for invasion, to the tml roots. These results suggest that TML is likely to func- i.e. ITs ( Sprent 2007 ). The IT is a tubular structure ﬁ rst initiated tion downstream of HAR1, possibly as a receptor or a mediator in the root hair, where it elongates by cell wall deposition and of the as yet unidentiﬁ ed shoot-derived signals ( Magori and ramiﬁ es the root cortex towards the nodule primordium that Kawaguchi 2009 , Magori et al. 2009 ). developed from the pericycle ( Gage and Margolin 2000 ). Independentoly of AON, the role of ethylene is well charac- Initiation of ITs requires several sequential steps; attachment terized as a negative regulator of nodulation. In M. truncatula , of bacteria on the root hairs, root hair curling and bacterial the numbers of successful bacterial infections and nodules colonization at the tip of distorted (curled) root hairs. Puriﬁ ed are substantially increased in the ethylene-insensitive mutant, NFs alone can induce a nodule meristem, but no root hair curl- sickle ( Penmetsa and Cook 1997 ). The SICKLE gene has been ing, indicating that the latter requires the presence of bacteria demonstrated to encode an M. truncatula ortholog of the at the surface of a root hair tip. However, not all root hairs Arabidopsis ethylene signaling protein, EIN2 ( Penmetsa et al. with attached bacteria in the infection zone exhibit root hair 2008 ). Inhibition of ABA biosynthesis and signaling through curling, suggesting the presence of a cell-speciﬁ c determinant(s) the use of a speciﬁ c inhibitor or a dominant-negative allele for susceptibility to rhizobial infection. Root hair curling is of ABSCISIC ACID INSENSITIVE1 leads to a hypernodulation characteristic of root nodule symbiosis: the normal polar tip phenotype, indicating that endogenous ABA is also involved growth of root hair development is disrupted, resulting in the in the negative regulation of nodulation ( Suzuki et al. 2004 , enclosure of attached bacteria inside a curl, where bacteria Ding et al. 2008 ). proliferate, colonize and express cell wall-degrading enzymes In addition to internal signaling represented by AON, host to penetrate to the root hair plasma membrane. The root hair legumes also control nodulation by sensing external signals. tip growth system is diverted to the focus of degradation to Light irradiation on roots strongly inhibits nodulation, but deposit the IT wall. This growth and direction of the IT is con- the roots of L. japonicus astray mutants can nodulate even in trolled by the presence of the nucleus and the rearrangement the light. The nodulation zone of astray is wider than that of microtubules and the actin cytoskeleton. The pathway of of the wild type, although the overall nodule density is com- IT development is paved by formation of pre-infection threads parable with that of the wild type. ASTRAY is closely related or cytoplasmic bridges ( van Brussel et al. 1992 ), which is analo- to Arabidopsis HY5 , a bZIP transcription factor. Interestingly it gous to the cytoplasmic strand formed during cell division. has a RING-ﬁ nger motif and an acidic region in its N-terminal Concomitantly with IT formation in the root hair, differen- half ( Nishimura et al. 2002b ). This type of transcription factor tiated cells at the root cortex (and then pericycle) start to is found in G. max and Vicia faba , but not in non-legumes, divide to develop a nodule meristem [cortical cell division indicating that this combination of motifs appears to be char- (CCD)]. This coordinated development between the infection acteristic of legumes. process and nodule organogenesis is believed to be crucial Another major external signal is soil nitrogen. High con- for successful nitrogen-ﬁ xing nodule formation ( Oldroyd and centrations of nitrogen such as nitrate or ammonia abolish Downie 2008 ). In L. japonicus , as well as in soybean and bean, 1388 Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. Legume genes involved in symbiosis the activity of the nodule meristem is restricted at the early drastically induced in the epidermis soon after NF perception, stages of nodule development. The developed nodule does not and is conﬁ ned to the infection zone ( Radutoiu et al. 2003 ). have a persistent meristem and is a spherical shape (determi- This induction requires NSP2 (Murakami et al. 2007), CYCLOPS nate nodules). In contrast, M. truncatula , as well as pea and ( Yano et al. 2008 ) and CERBERUS ( Yano et al. 2009 ). The cis - clover, has a persistent meristem at the tip of elongated nodule motifs for NIN binding have not yet been reported. structures even after full maturation (indeterminate nodules). CERBERUS and its Medicago ortholog, LIN , encode a U-box In this case, ITs remained in the nodule and continuously release protein with WD-40 repeats which is postulated to be an E3 bacteria for endosymbiosis. ubiquitin ligase ( Kiss et al. 2009 , Yano et al. 2009 ). CERBERUS is So far 11 genes have been cloned and reported to be necessary for IT initiation in addition to CYCLOPS and ERN1 . essential for coordinative progression of IT growth and nodule ERN1 encodes an ERF transcription factor, which contains an organogenesis ( Table 1 ). Intracellular signal transduction AP2 DNA-binding domain ( Middleton et al. 2007 ). In contrast through so-called common symbiosis genes following NF per- to CYCLOPS and CERBERUS , ERN1 is essential for spontaneous ception (see above sections) is a prerequisite to triggering nodulation by a gain-of-function CCaMK ( Middleton et al. this stage of symbiosis development. The only exception is 2007 ). Due to the facts that both CYCLOPS and CERBERUS are CYCLOPS , which is also required for symbiosis with arbuscular not required for spontaneous nodule formation but are neces- mycorrhiza, and thus is a member of the CSP genes, but its loss- sary for NIN induction in epidermis, and that NIN is essential for of-function mutant forms nodule primordia (which appear as CCD but CYCLOPS and CERBERUS are not ( Yano et al. 2008 , small bumps) upon inoculation of M. loti without any success- Yano et al. 2009 ), regulation of NIN expression in the epidermis ful infection events ( Yano et al. 2008 ). CYCLOPS is a nuclear- and cortex may differ in terms of their signaling cascades. localized protein and has been shown to be phosphorylated by Rearrangement of the cytoskeleton is important in biotic CCaMK in vitro ( Yano et al. 2008 ), and its Medicago ortholog, interaction in plants ( Takemoto and Hardham 2004 ). NAP1 and IPD3, has been shown to interact with DMI3 (CCaMK) in planta PIR1 have been shown to play such a role in rhizobial infection, by ( Messinese et al. 2007 ). Since the loss-of-function mutants of their involvement in actin polymerization, but are not involved CCaMK display neither root hair curling nor CCD, CYCLOPS is in CCD ( Yokota et al. 2009 ). They are also essential for trichome thought to be important for the function of CCaMK in the development like CRINKLE , which has been identiﬁ ed as a locus rhizobial infection process (see above section). required for both IT growth and normal trichome development Plant hormones are involved in various aspects of plant through actin cytoskeleton rearrangement ( Tansengco et al. development. In RN symbiosis, several hormones are reported 2003 , Tansengco et al. 2004 ). Microtubules have been shown to to be important. Among them, cytokinin has been shown play an important role in IT development ( Timmers et al. 1999 , genetically to be essential for nodule organogenesis. LHK1 in Vassileva et al. 2005 ), but their function in IT formation has not L. japonicus , which encodes a cytokinin receptor kinase, is yet been deﬁ ned genetically. only involved in nodule organogenesis in the cortex, not in IT RPG encodes a putative coiled-coil protein, which is local- formation. The loss-of-function mutant hit1 forms excessive ized in the nucleus ( Arrighi et al. 2008 ). In the loss-of-function ITs penetrating into the root cortex without inducing timely mutant, development of ITs is abnormal and is arrested mostly CCD after rhizobial inoculation ( Murray et al. 2007 ). In accor- in the root epidermis. LATD/NIP encodes a putative transporter dance with this ﬁ nding, a Lotus snf2 , which is a gain-of-function of the NRT1 (nitrate transporter) family ( Yendrek et al. 2010 ). mutant of LHK1 , exhibits spontaneous nodulation in the Mutation in LATD/NIP shows developed but abnormal ITs, and absence of rhizobia, indicating the crucial role of LHK1 in nodule bacterial release from ITs is aborted. The mutation also affects organogenesis ( Tirichine et al. 2007 ). Spontaneous nodule for- primary and lateral root development by meristem arrest. mation in snf2 requires NSP2 and NIN , but not CYCLOPS , so that The genes described above are mostly essential for IT initia- LHK1 functions in nodule organogenesis upstream of NSP2 tion and/or its growth, but not for induction of CCD per se, and NIN , but it is positioned downstream of or in a separate except for LHK1 . However, they are also involved in the pathway from CYCLOPS ( Tirichine et al. 2007 ), consistent with nodule organogenesis program, directly or indirectly. At least the observation that in the cyclops mutants nodule organo- in L. japonicus mutants, the infection process and nodule genesis is initiated ( Yano et al. 2008 ). organogenesis seem to be developmentally coupled ( Fig. 4 ; NSP2 encodes a GRAS family transcription regulator, and is in the case of pea, see Tsyganov et al. 2002 ). The mutants, required for CCD and root hair curling. NSP2 is localized in the which show no or aberrant root hair curling, fail to induce any nucleus and interacts with another GRAS family transcription CCD ( nsp1 , nsp2 and nin ). Abortion of IT initiation after regulator, NSP1 ( Hirsch et al. 2009 ). This interaction is neces- root hair curling and bacterial colonization coincides with sary for nodule organogenesis, and NSP1 associates with the formation of small bumps which are impaired in their develop- promoters of early nodulin genes, such as ENOD11 , NIN and ment into mature nodule structures ( cyclops and cerberus ). ERN1 ( Hirsch et al. 2009 ). NIN is a putative transcription regula- When ITs are developed in the root epidermis ( crinkle , alb1 tor that is also required for CCD and controlling root hair curl- and pir1-3 ), the arrest of nodule development is at a much ing ( Schauser et al. 1999 ). Its loss of unction results in unusually later stage, resulting in occasional abnormal bacterial release extensive root hair curling but no IT initiation. NIN expression is from developed ITs into infected cells in aberrant nodules Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. 1389 H. Kouchi et al. Host regulation of nitrogen ﬁ xation activity Almost concurrently with the emergence of nodules, rhizobia are released from ITs into the nodule cells, and they are then present in the host cell cytoplasm enclosed by the peribacte- roid membrane (PBM) which is derived from the host plasma membrane. They differentiate into a symbiosis-speciﬁ c form, the bacteroid, and then develop nitrogen-ﬁ xing activity. Bacte- roids at full maturation cease cell division, and PBM-enclosed bacteroids are essentially a nitrogen-ﬁ xing intracellular organ- elle, termed the ‘symbiosome’. Most Rhizobium species are unable to ﬁ x nitrogen in the free-living state. Housing within the nodule cells and differentiation into bacteroids is essential for rhizobial nitrogen ﬁ xation. Therefore, bacteroid differentia- tion and their nitrogen ﬁ xation are under strict control with complex interactions between the host legume cells and the intracellular bacteria; however, the mechanisms underlying differentiation of endosymbiotic rhizobia in symbiosomes to the bacteroid form are still largely unknown. In the indetermi- Fig. 4 Developmental regulation of the infection process and nodule organogenesis. The infection process and nodule organogenesis are nate nodules formed on legumes of the galegoid clade such sequentially (from left to right) drawn schematically. Genes essential as M. truncatula , recent evidence indicates that rhizobial for each step are indicated below the picture. (1) Attachment of a proli feration is terminated by DNA endoreduplication trig- bacterium on the surface of a root hair. (2). Root hair curling and the gered by host plant factors, which have been suggested to be following colonization of bacteria in the tight curl. (3) Infection thread nodule-infected cell-speciﬁ c cysteine-rich peptides ( Mergaert development in a root hair. A nodule primordium is initiated. (4) et al. 2006 ; see below), and BacA protein in rhizobia is shown Infection thread development into the nodule primordium. The to be involved in the uptake of the host-derived peptides nodule primordium is developed. The lower panel shows the ( Marlow et al. 2009 ). In the determinate nodules formed microphotographs of L. japonicus roots after inoculation with LacZ - on non-galegoid clade legumes, such as L. japonicus , however, labeled M. loti corresponding to steps 2, 3 and 4 from left to right. NP, the host mechanisms controlling rhizobial proliferation are nodule primordium. Bars = 100 µm. totally unknown. The bacteroids become slightly larger than the free-living (so-called ‘type II’ nodules; Yano et al. 2006 ). Because NFs from rhizobia in determinate nodules, whereas in indeterminate rhizobia are supposed to be initially recognized at the surface nodules they undergo much more remarkable morphological of the epidermis, there can be infection signal(s) transmitted changes such as cell elongation and/or Y-shaped transforma- from the epidermis downward to the cortex in order to tion. In addition, terminally differentiated bacteroids in inde- activate and regulate nodule organogenesis. This is consistent terminate nodules are functional but not viable, while the with the fact that only a small portion of ITs formed correlate bacteroids in determinate nodules have been shown to survive with CCD, and competence for CCD seems to be regulated in a reversed fashion, i.e. reverting to the free-living state by another signal(s) such as AON (see above section). As the when released in the soil from senesced and collapsed nodules. stages of nodule developmental arrest differ among the Therefore, the mechanisms of bacteroid differentiation and the different mutants, as described above, the regulation seems to situation of bacteroids inside nodule cells may be considerably involve multiple steps, so that there are probably several kinds different between indeterminate and determinate nodules. of signals from epidermis to cortex. One such transmitted A number of host legume genes (nodulin genes) speciﬁ cally signal may be cytokinin ( Oldroyd 2007 ). There may also be expressed during the nodulation process have been identiﬁ ed signals from cortex to epidermis to regulate the infection pro- from various legume species by differential or subtractive cess, because ITs that do not accompany CCD are aborted hybridization techniques ( Legocki and Verma 1980 , Kouchi and in the epidermis. Since the study of tissue-speciﬁ c expression Hata 1993 ). More recently, comprehensive analyses by means (epidermis or cortex) of the genes above described is quite of cDNA or oligo arrays and proteomics have revealed that limited, it is largely unknown whether those symbiosis genes more than a thousand genes are speciﬁ cally induced or highly are functional in epidermis or cortex, or in both. Analysis such enhanced in nodules ( Weinkoop and Saalbach 2003 , Colebatch as spatio-temporal expression of symbiosis genes in various et al. 2004 , Kouchi et al. 2004 , Tesfaye et al. 2006 , Larrainzar mutant backgrounds and gain-of-function studies with symbi- et al. 2007 , Benedito et al. 2008 , H ø gslund et al. 2009 ). Among osis genes including genes other than CCaMK and LHK1 is these genes, late nodulin genes, which are induced just before necessary to dissect the ﬁ ne-tuning of coordination of infection the onset of nitrogen ﬁ xation, have been implicated as being and nodule organogenesis programs. involved in the host regulation of nitrogen ﬁ xation. However, the 1390 Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. Legume genes involved in symbiosis experimental evidence regarding the exact functions of those genes is very limited. One example is leghemoglobin (Lb). Lb is nodule-speciﬁ c oxygen-binding protein, and has been thought to play the role both of keeping a low oxygen concentration in the nodule-infected cells and of facilitating O supply to the bacteroids for their aerobic respiration. RNA interference (RNAi) knock-down of Lb in L. japonicus was shown to result in almost complete loss of nitrogen-ﬁ xing activity, indicating an indispensable role for Lb to support rhizobial nitrogen ﬁ xation ( Ott et al. 2005 ). In regard to carbon metabolism, nodule-enhanced sucrose synthase, which is the ﬁ rst enzyme to break down photosynthate translocated to nodules from shoots, has been demonstrated to be crucial for nitrogen ﬁ xa- tion by means of the antisense technique ( Baier et al. 2007 ). In a similar way, a nodule-enhanced isoform of phosphoe- nolpyruvate carboxylase has been proven to be involved in the carbon and nitrogen ﬂ ux in nodules, and thus is essential for symbiotic nitrogen ﬁ xation ( Nomura et al. 2006 ). Although Fig. 5 A schematic representation showing the functions of SST1, FEN1 a number of nodule-speciﬁ c putative transporters such as and IGN1 for nitrogen-ﬁ xing symbiosis in L. japonicus nodules. SST1 is aquaporin (nodulin 26) have been identiﬁ ed in the PBM of a sulfate transporter localized in the peribacteroid membrane (PBM) L. japonicus nodules ( Wienkoop and Saalbach 2003 ), their 2 − and transfers SO from plant cytosol to bacteroids (B). FEN1 is exact functions in symbiosis have not yet been resolved. homocitrate synthetase which supplies homocitrate to bacteroids to Studies using various rhizobial mutants have demonstrated support synthesis of the nitrogenase complex. IGN1 is localized in the that transport of dicarboxylates and some amino acids to plasma membrane (PM) and is thought to function in symbiosome (S) bacteroids from the host plant cells is essential for nitrogen and/or bacteroid differentiation and maintenance. ﬁ xation and/or nodule persistence ( Ronson et al. 1981 , Prell et al. 2009 ). Nevertheless, the transporters responsible for those compounds across the PBM remain to be clariﬁ ed. Fix mutants are host plant mutants that form morphologi- The fen1 mutant was isolated and characterized by a system- cally normal nodules with endosymbiotic rhizobia, but exhibit atic effort to screen symbiotic mutants of L. japonicus , and it very low or no nitrogen-ﬁ xing activity, and thus are unable to forms pale pink, small nodules with very low nitrogen-ﬁ xing grow solely dependent on atmospheric nitrogen. Identiﬁ cation activity ( Imaizumi-Anraku et al. 1997 ). The causal gene, FEN1 , of the causal genes of Fix mutants provides important clues was cloned and demonstrated to encode homocitrate synthase for unraveling the host regulation mechanisms of symbiotic (HCS) which is expressed speciﬁ cally in nodule-infected cells nitrogen ﬁ xation. Three L. japonicus genes, SST1 , FEN1 and IGN1 , ( Hakoyama et al. 2009 ). Homocitrate is a quite unusual com- and one M. truncatula gene, DNF1 , have been identiﬁ ed by pound in the higher plant kingdom, and indeed it was found analyses of Fix mutants ( Table 1 ). abundantly only in legume nodules, whereas it is barely detect- A symbiotic sulfate transporter ( SST1 ) gene was found by able in nodules formed on the fen1 mutants. Homocitrate is map-based cloning from an L. japonicus Fix mutant sst1 known to be a component of iron–molybdenum cofactor ( Krusell et al. 2005 ). Expression of the SST1 gene is speciﬁ c to (FeMo-co) in the nitrogenase complex, on which nitrogen ﬁ xa- nodule-infected cells and its product is found to function as tion is thought to occur ( Hoover et al. 1987 ). NIFV , which a high afﬁ nity sulfate transporter by its ability to complement encodes HCS, has been identiﬁ ed from many diazotrophs and a Saccharomyces cerevisiae sulfate transporter mutant. SST1 shown to be essential for their nitrogenase activity ( Hoover has been shown to be localized in the PBM ( Wienkoop and et al. 1987 , Zheng et al. 1997 ). However, the NIFV orthologs are Saalbach 2003 ). Sulfur has special importance in bacteroids as not found in most of the Rhizobium species which exert highly a component of metal–sulfur clusters within the nitrogenase efﬁ cient nitrogen ﬁ xation only in symbiotic association with complex and the related electron transfer proteins. Thus SST1 compatible host legumes. Therefore, it is very likely that nodule- could meet the high demand for sulfur by bacteroids inside speciﬁ c HCS encoded in the host legume genome could com- symbiosomes to support nitrogen ﬁ xation ( Fig. 5 ). Other sulfate pensate for the lack of NIFV in endosymbiotic rhizobia by transporter genes are also expressed in nodules of L. japonicus , supplying homocitrate to bacteroids from the host cell cyto- but none of them can compensate for the defect in SST1 plasm ( Fig. 5 ). This hypothesis was conﬁ rmed by the fact that function in the sst1 mutants. This indicates that acquisition of M. loti carrying the FEN1 gene or an authentic NIFV from a specialized form of symbiotic sulfate transporter by legumes Azotobacter vinelandii perfectly rescued the defect in nitrogen during evolution allowed legumes to fulﬁ ll efﬁ cient nitrogen ﬁ xation of the fen1 mutants. These ﬁ ndings highlighted the ﬁ xation activity by symbiotic rhizobia. complementary and indispensable partnership between legumes Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. 1391 H. Kouchi et al. and rhizobia in symbiotic nitrogen ﬁ xation. Furthermore, this provides impetus for exploring the co-evolution of legume plants and Rhizobium bacteria ( Hakoyama et al. 2009 ). In general, nodules formed on Fix mutants show more or less premature senescence, such as highly vacuolated infected cells and irregularly enlarged symbiosomes. The nodules formed on an L. japonicus Fix mutant ign1 are characterized by very rapid and severe premature senescence, followed by disruption of the integrity of the whole infected cell. The causal gene, IGN1 , encodes a novel ankyrin-repeat membrane protein, and is shown to be present in the plasma membrane ( Kumagai Fig. 6 A model for a nodule-specific secretory pathway of NCR et al. 2007 ). IGN1 expression is not speciﬁ c to nodules, but is peptides to direct symbiosome development and terminal also detected in all organs of L. japonicus plants at low levels. differentiation of bacteroids in indeterminate nodules. A signal Nevertheless, the mutant phenotype appears only with the peptidase complex (SPC), a component of which has been identiﬁ ed symbiotic defect, suggesting a role for IGN1 in surveillance or as DNF1, is required for targeting the nodule-speciﬁ c cysteine-rich control of responses to biotic infection. Based on these results, (NCR) peptides to the symbiosome. NCR peptides are thought to be it has been hypothesized that IGN1 is required for preventing incorporated into bacteroids, leading to terminal differentiation of the host plant cells from inappropriately invoking a defense bacteroids. CW, cell wall; PM, plasma membrane; ER, endoplasmic system against compatible microsymbionts, thus being essen- reticulum; IT, infection thread. tial for differentiation and/or persistence of bacteroids and symbiosomes, although the exact biochemical function of IGN1 is still to be elucidated. In M. truncatula , nodule-speciﬁ c cysteine-rich (NCR) pep- in the near future is the establishment of an efﬁ cient gene tagging tides were shown to be the host plant factors which direct system using endogenous retrotransposons represented by symbiotic rhizobia into terminal bacteroid differentiation LORE1 in L. japonicus ( Fukai et al. 2010 ), which could be ( Van de Velde et al. 2010 ). The NCR peptides are most similar applicable for both forward and reverse genetics. to defensin-type antimicrobial proteins, and have a signal pep- There has been remarkable progress in our understanding of tide which targets them into the secretory pathway. DNF1 , the host regulation of endosymbiosis with microbes in recent which encode a component of the signal peptidase complex, years. However, our current knowledge still remains, as a whole, was identiﬁ ed as the causal gene of an M. truncatula Fix mutant at the stage of the identiﬁ cation of individual components dnf1 and was shown to be highly expressed in nodules ( Wang involved in symbiotic signaling and/or functions. Deﬁ nition of et al. 2010 ). In the dnf1 mutants, differentiation of rhizobia to the exact biochemical functions of the gene products identiﬁ ed bacteroids and symbiosome organogenesis are both blocked and analyses of their spatio-temporal regulation, their epistatic/ at early stages of nodule development. Interestingly, in the hypostatic relationships and of their interactions, including dnf1 mutants, an NCR peptide was not properly targeted to the search for novel interactors, are required to clarify the basic the bacteroids ( Van de Velde, 2010 ). These results indicate scheme of gene networks that govern the symbiotic process that the host plants control the differentiation of rhizobia from mutual recognition, rhizobial infection, nodule formation into bacteroids by targeting NCR peptides through the and establishment of a functional (nitrogen-ﬁ xing) symbiosis. nodule-speciﬁ c protein secretory system in indeterminate To investigate these aspects in greater detail, cytological nodules ( Fig. 6 ). In contrast, no NCR genes have been found (including bio-imaging analyses), biochemical (protein–protein in the genomes of legumes that form determinate nodules, interactions) and physiological (metabolism and transport implying that alternative host plant mechanism(s) may be in nodules) approaches will have even greater importance in responsible for regulating bacteroid differentiation in these future studies. In addition, phylogenetic and comparative legume species. genomics approaches promise better understanding of how legumes have elaborated such a sophisticated association with soil bacteria. Now that the basic infrastructures for whole- genome sequencing, and the innovative tools for transcrip- Concluding remarks and prospects tome, proteome and metabolome analyses and their databases, Based on the establishment of genetic resources of the model are being established very rapidly, not only for the model legumes, > 40 host legume genes or loci essential for microbial legumes but also for the most important legume crop, soybean, endosymbiosis have been identiﬁ ed so far (this review; see also research on plant–microbe symbiotic interactions will move Sandal et al. 2006 , Oldroyd and Downie 2008 ). Isolation of into new avenues in the ‘post-genome era’. Obviously, the large genes by a forward genetics approach from symbiotic mutants number of symbiotic mutants and cloned genes that have generated by conventional mutagenesis methodology appears been accumulated during the past decade could be the most to be practically reaching saturation. One promising approach powerful basis for such avenues of research. 1392 Plant Cell Physiol. 51(9): 1381–1397 (2010) doi:10.1093/pcp/pcq107 © The Author 2010. Legume genes involved in symbiosis Borisov , A.Y. , Madsen , L.H. , Tsyganov , V.E. , Umehara , Y. , Voroshilova , V.A. , Funding Batagov , A.O. , et al . ( 2003 ) The sym35 gene required for root nodule development in pea is an ortholog of nin from Lotus japonicus . The Ministry of Agriculture, Forestry, and Fisheries of Japan Plant Physiol. 131 : 1009 – 1017 . [Rice Genome Project Grant PMI-0001 to H.I.-A. and M.H.]; the Caetano-Anolles , G. and Gresshoff , P.M. 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How Many Peas in a Pod? Legume Genes Responsible for Mutualistic Symbioses Underground

How Many Peas in a Pod? Legume Genes Responsible for Mutualistic Symbioses Underground

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How Many Peas in a Pod? Legume Genes Responsible for Mutualistic Symbioses Underground

How Many Peas in a Pod? Legume Genes Responsible for Mutualistic Symbioses Underground

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