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International Symposium on Long-Distance Signaling in Plants

International Symposium on Long-Distance Signaling in Plants As sessile organisms, plants have developed elaborate means to optimize their metabolism and growth in response to environmental fluctuations. Although plants sense fluctuations only locally, their responses must be co-ordinated at the whole-plant level. Long-distance signaling between organs, via either xylem or phloem, is required for this co-ordination. Signaling molecules such as sugars, RNAs, polypeptides, phytohormones and peptide hormones have all been proposed to function as long-distance signals. Recently, great advances have been made in elucidating the molecular bases for long-distance signaling. Such advances were the focus of the Integrative Graduate Education and Research Program in Green Natural Sciences (IGER) International Symposium on Long-Distance Signaling in Plants, which was held on November 21, 2017 at Nagoya University, Japan. This report summarizes some of the new insights presented at this symposium by key researchers in the field. Long-Distance Signaling via RNAs All classes of RNA molecules, including small interfering RNAs (siRNAs), microRNAs (miRNAs), tRNAs and protein-encoding mRNAs, are detected in phloem exudates and are proposed to be mobile between tissues and organs (Kehr and Kragler 2018). Recent advances in analyzing the mobile transcriptome in heterografts indicate that a high number of mRNAs are transported via the phloem with tissue specificity and directionality (Notaguchi et al. 2015, Thieme et al. 2015); however, the molecular basis for mRNA mobility has been elusive. Friedrich Kragler (Max Planck Institute of Molecular Plant Physiology, Germany) and his colleagues studied how RNA motifs trigger mobility by conducting a bioinformatic analysis of mobile mRNAs. The team found that tRNA-like stem–bulge–stem–loop structures (TLSs) are enriched in mobile mRNAs (Guan et al. 2017). By assessing the long-distance mobility of reporter transcripts with or without the TLS motif, the team reported that TLS motifs are necessary and sufficient for long-distance transport of mRNAs (Zhang et al. 2016; see also Winter and Kragler 2018 in this Spotlight Issue). Plant miRNAs are 20–24 nucleotide-long non-coding RNAs that negatively regulate gene expression and have vital roles in many aspects of plant growth and developmental regulation (Zhang et al. 2006). Next-generation sequencing methods have identified an extensive number of miRNAs in phloem sap; however, the function of most of these miRNAs remains unknown. Tzyy-Jen Chiou (Academia Sinica, Taiwan) presented an excellent example of how a miRNA functions as a long-distance signal in the systemic regulation of phosphate (Pi) homeostasis. The Chiou group showed that, upon Pi starvation, miR399 is up-regulated first in the shoots and then moves via the phloem to the roots, where miR399 directs the cleavage of PHOSPHATE2 (PHO2) transcripts (Chien et al. 2017). PHO2 encodes ubiquitin-conjugating E2 enzyme 24 (UBC24) that modulates the activities of Pi acquisition and root to shoot Pi translocation by mediating the protein degradation of PHOSPHATE TRANSPORTER1 and the Pi efflux transporter PHOSPHATE1, respectively (Liu et al. 2012, Huang et al. 2013). These studies revealed how plants orchestrate the two activities, Pi acquisition at the root surface and Pi loading of xylem at the root stele, to maintain whole-plant Pi homeostasis by using an miRNA as a long-distance signal. In this issue, Chien et al. 2018 further discuss the potential cross-talk between various regulatory pathways underlying local and systemic responses to Pi deprivation. Long-Distance Signaling via Proteins Although many proteins are present in the phloem exudates of many plant species, we know very little about the signaling functions of these proteins. One of the best characterized examples is FLOWERING LOCUS T (FT) protein. FT protein moves from leaves to the shoot apex via phloem to act as a potent activator of flowering in many plants (Notaguchi et al. 2008, Putterill and Varkonyi-Gasic 2016). Xiangdong Fu (Chinese Academy of Sciences, China) and colleagues identified another example, ELONGATED HYPOCOTYL5 (HY5) (Chen et al. 2016). HY5 is a bZIP transcription factor that functions as a positive regulator of photomorphogenesis. Fu presented evidence that HY5 moves from shoots to roots via phloem to activate the high-affinity nitrate transporter gene NITRATE TRANSPORTER2.1 (NRT2.1) and represses the auxin signaling repressor gene SHORT HYPOCOTYL2, thereby promoting nitrate uptake and root growth. This example illustrates that long-distance movement of HY5 from shoots to roots co-ordinates carbon and nitrogen metabolism, thus enabling plants to orchestrate shoot and root growth at the whole-plant level in response to changes in the light environment. Long-Distance Signaling via Cytokinins Because vascular sap contains several phytohormones and their derivatives, it has long been proposed that phytohormones are involved in long-distance signaling (Hoad 1995, Kudo et al. 2010, Lacombe and Achard 2016); however, little is known about exactly how and why phytohormones are translocated long distances. Hitoshi Sakakibara (Nagoya University, Japan) reviewed his group’s recent progress in deciphering the molecular mechanism and the physiological role of cytokinin (CK) translocation. Previously, this team identified ABCG14, a member of the ABC transporter family, as a key factor for root to shoot translocation of CKs (Ko et al. 2014). Recently, Sakakibara’s group showed that plants have a dual root to shoot long-distance CK signaling system, in which two CK molecular species, trans-zeatin (tZ) and trans-zeatin riboside (tZR), convey different messages (Osugi et al. 2017). The root-borne tZ plays a role in controlling leaf size, whereas tZR is involved in regulating meristem activity-related traits. This dual long-distance cytokinin signaling system enables plants to fine-tune shoot growth in a manner responsive to environmental fluctuations. Sandrine Ruffel [French National Institute for Agricultural Research (INRA), France] has been focusing on the role of CKs in systemic nitrogen demand signaling. Since nitrogen is often distributed unevenly in the soil, plants utilize the systemic nitrogen demand signaling system, by which nitrogen starvation on one side of the root induces a compensatory up-regulation of nitrate uptake on the other side in a nitrogen-rich environment. Ruffel presented her group’s latest finding that tZ-type CKs in the shoot have an essential role in systemic nitrogen demand signaling (Poitout et al. 2018). The long-distance signaling of CKs and other nutrients is further reviewed by Ruffel (2018), in this issue. Long-Distance Signaling via Peptide Hormones At present, the importance of signaling peptides, now often referred to as ‘peptide hormones’, in diverse growth and developmental processes is well established (Matsubayashi 2014, Okamoto et al. 2016). Although most of the peptide hormones characterized so far mediate local signaling, Takuya Suzaki (University of Tsukuba, Japan) and Yoshikatsu Matsubayashi (Nagoya University, Japan) presented their evidence for mobile peptides. Suzaki summarized his lab’s studies of how legume plants control symbiosis using a peptide hormone as a long-distance signal. Leguminous plants engage in symbiosis with nitrogen-fixing soil rhizobia and form nodules. Because nodulation is an energy-consuming process, host plants control the number of nodules via long-distance signaling to balance the nitrogen demand and the energy cost. Previously, Suzaki’s colleagues identified Lotus japonicus CLAVATA3/ESR-RELATED ROOT SIGNAL2 (CLE-RS2) peptide as a root to shoot long-distance signal that inhibits nodulation (Okamoto et al. 2009, Okamoto et al. 2013). CLE-RS2 is highly up-regulated in roots by rhizobial inoculation and nitrate supplementation, and is perceived by the HYPERNODULATION ABERRANT ROOT FORMATION (HAR1) receptor in shoots. Suzaki’s group recently identified a key factor in the nitrate-responsive systemic inhibition of nodulation, NITRATE UNRESPONSIVE SYMBIOSIS1 (NRSYM1) (Nishida et al. 2018). In response to nitrate, NRSYM1, a NIN-LIKE PROTEIN transcription factor, accumulates in nuclei and directly activates CLE-RS2 expression, leading to the abolishment of nodulation. These studies revealed how leguminous plants respond to the nitrogen environment and control symbiosis by integrating environmental and symbiotic signals. This topic is the focus of the review by Nishida and Suzaki (2018), also featured in this Spotlight Issue. Matsubayashi’s group has thus far identified two classes of mobile peptides involved in systemic nitrogen demand signaling. One class is C-TERMINALLY ENCODED PEPTIDEs (CEPs) that are up-regulated in nitrogen-starved roots, transported to shoots and perceived by CEP RECEPTORs (CEPRs) (Tabata et al. 2014). The other class is CEP DOWNSTREAMs (CEPDs) that are induced in shoot phloem in a CEP/CEPR-dependent manner, transported to roots and activate nitrate uptake through up-regulation of NRT2.1 (Ohkubo et al. 2017). An important future challenge will be to elucidate the relationship between tZ-type CK-mediated and CEP–CEPD-mediated systemic nitrogen demand signaling systems. During the poster session, Fuminori Takahashi (RIKEN CSRS, Japan) presented his team’s recent discovery that CLE25 peptide functions as a root to shoot water deficiency signal (Takahashi et al. 2018). Many uncharacterized peptides have been identified by xylem sap peptidomics (Okamoto et al. 2015), suggesting that peptide hormones have a much broader role in long-distance signaling. Yoshikatsu Matsubayashi closed the symposium by emphasizing that plant long-distance signaling research is still an emerging field that requires networking and collaboration to establish and expand this field further. Indeed, this symposium not only provided a fantastic opportunity to kick-start networking and collaboration within the field, but also proved to be a huge success with exciting prospects ahead in terms of the quality of science presented. On behalf of the organizing committee, I thank the presenters and sponsors for their great contributions to the symposium. Disclosures The author has no conflicts of interest to declare. References Chen X. , Yao Q. , Gao X. , Jiang C. , Harberd N.P. , Fu X. ( 2016 ) Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition . Curr. Biol . 26 : 640 – 646 . Google Scholar Crossref Search ADS PubMed Chien P.-S. , Chiang C.-P. , Leong S.J. , Chiou T.-J. ( 2018 ) Sensing and signaling of phosphate starvation—from local to long distance . Plant Cell Physiol . 59 : 1714 – 1722 . Chien P.S. , Chiang C.B. , Wang Z.R. , Chiou T.J. ( 2017 ) MicroRNA-mediated signaling and regulation of nutrient transport and utilization . Curr. Opin. Plant Biol. 39 : 73 – 79 . Google Scholar Crossref Search ADS PubMed Guan D. , Yan B. , Thieme C. , Hua J. , Zhu H. , Boheler K.R. , et al. ( 2017 ) PlaMoM: a comprehensive database compiles plant mobile macromolecules . Nucleic Acids Res. 45 : D1021 – D1028 . Google Scholar Crossref Search ADS PubMed Hoad G.V. ( 1995 ) Transport of hormones in the phloem of higher-plants . Plant Growth Regul. 16 : 173 – 182 . Google Scholar Crossref Search ADS Huang T.K. , Han C.L. , Lin S.I. , Chen Y.J. , Tsai Y.C. , Chen Y.R. , et al. ( 2013 ) Identification of downstream components of ubiquitin-conjugating enzyme PHOSPHATE2 by quantitative membrane proteomics in Arabidopsis roots . Plant Cell 25 : 4044 – 4060 . Google Scholar Crossref Search ADS PubMed Kehr J. , Kragler F. ( 2018 ) Long distance RNA movement . New Phytol. 218 : 29 – 40 . Google Scholar Crossref Search ADS PubMed Ko D. , Kang J. , Kiba T. , Park J. , Kojima M. , Do J. , et al. ( 2014 ) Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin . Proc. Natl. Acad. Sci. USA 111 : 7150 – 7155 . Google Scholar Crossref Search ADS Kudo T. , Kiba T. , Sakakibara H. ( 2010 ) Metabolism and long-distance translocation of cytokinins . J. Integr. Plant Biol. 52 : 53 – 60 . Google Scholar Crossref Search ADS PubMed Lacombe B. , Achard P. ( 2016 ) Long-distance transport of phytohormones through the plant vascular system . Curr. Opin. Plant Biol. 34 : 1 – 8 . Google Scholar Crossref Search ADS PubMed Liu T.Y. , Huang T.K. , Tseng C.Y. , Lai Y.S. , Lin S.I. , Lin W.Y. , et al. ( 2012 ) PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis . Plant Cell 24 : 2168 – 2183 . Google Scholar Crossref Search ADS PubMed Matsubayashi Y. ( 2014 ) Posttranslationally modified small-peptide signals in plants . Annu. Rev. Plant Biol. 65 : 385 – 413 . Google Scholar Crossref Search ADS PubMed Nishida H. , Suzaki T. ( 2018 ) Two negative regulatory systems of root nodule symbiosis—how are symbiotic benefits and costs balanced? Plant Cell Physiol . 59 : 1733 – 1738 . Nishida H. , Tanaka S. , Handa Y. , Ito M. , Sakamoto Y. , Matsunaga S. , et al. ( 2018 ) A NIN-LIKE PROTEIN mediates nitrate-induced control of root nodule symbiosis in Lotus japonicus . Nat. Commun. 9 : 499. Google Scholar Crossref Search ADS PubMed Notaguchi M. , Abe M. , Kimura T. , Daimon Y. , Kobayashi T. , Yamaguchi A. , et al. ( 2008 ) Long-distance, graft-transmissible action of Arabidopsis FLOWERING LOCUS T protein to promote flowering . Plant Cell Physiol . 49 : 1645 – 1658 . Google Scholar Crossref Search ADS PubMed Notaguchi M. , Higashiyama T. , Suzuki T. ( 2015 ) Identification of mRNAs that move over long distances using an RNA-Seq analysis of Arabidopsis/Nicotiana benthamiana heterografts . Plant Cell Physiol . 56 : 311 – 321 . Google Scholar Crossref Search ADS PubMed Ohkubo Y. , Tanaka M. , Tabata R. , Ogawa-Ohnishi M. , Matsubayashi Y. ( 2017 ) Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition . Nat. Plants 3 : 17029. Google Scholar Crossref Search ADS PubMed Okamoto S. , Ohnishi E. , Sato S. , Takahashi H. , Nakazono M. , Tabata S. , et al. ( 2009 ) Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation . Plant Cell Physiol. 50 : 67 – 77 . Google Scholar Crossref Search ADS PubMed Okamoto S. , Shinohara H. , Mori T. , Matsubayashi Y. , Kawaguchi M. ( 2013 ) Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase . Nat. Commun. 4 : 2191. Google Scholar Crossref Search ADS PubMed Okamoto S. , Suzuki T. , Kawaguchi M. , Higashiyama T. , Matsubayashi Y. ( 2015 ) A comprehensive strategy for identifying long-distance mobile peptides in xylem sap . Plant J. 84 : 611 – 620 . Google Scholar Crossref Search ADS PubMed Okamoto S. , Tabata R. , Matsubayashi Y. ( 2016 ) Long-distance peptide signaling essential for nutrient homeostasis in plants . Curr. Opin. Plant Biol. 34 : 35 – 40 . Google Scholar Crossref Search ADS PubMed Osugi A. , Kojima M. , Takebayashi Y. , Ueda N. , Kiba T. , Sakakibara H. ( 2017 ) Systemic transport of trans-zeatin and its precursor have differing roles in Arabidopsis shoots . Nat. Plants 3 : 17112. Google Scholar Crossref Search ADS PubMed Poitout A. , Crabos A. , Petřík I. , Novák O. , Krouk G. , Lacombe B. , et al. ( 2018 ) Root responses to heterogeneous nitrate availability are mediated by trans-zeatin in arabidopsis shoots . Plant Cell 30 : 1243 – 1257 . Google Scholar Crossref Search ADS PubMed Putterill J. , Varkonyi-Gasic E. ( 2016 ) FT and florigen long-distance flowering control in plants . Curr. Opin. Plant Biol. 33 : 77 – 82 . Google Scholar Crossref Search ADS PubMed Ruffel S. ( 2018 ) Nutrient-related long-distance signals: common players and possible crosstalk . Plant Cell Physiol . 59 : 1723 – 1732 . Tabata R. , Sumida K. , Yoshii T. , Ohyama K. , Shinohara H. , Matsubayashi Y. ( 2014 ) Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling . Science 346 : 343 – 346 . Google Scholar Crossref Search ADS PubMed Takahashi F. , Suzuki T. , Osakabe Y. , Betsuyaku S. , Kondo Y. , Dohmae N. , et al. ( 2018 ) A small peptide modulates stomatal control via abscisic acid in long-distance signalling . Nature 556 : 235 – 238 . Google Scholar Crossref Search ADS PubMed Thieme C.J. , Rojas-Triana M. , Stecyk E. , Schudoma C. , Zhang W. , Yang L. , et al. ( 2015 ) Endogenous Arabidopsis messenger RNAs transported to distant tissues . Nat. Plants 1 : 15025. Google Scholar Crossref Search ADS PubMed Winter N. , Kragler F. ( 2018 ) Conceptual and methodological considerations on mRNA and proteins as intercellular and long-distance signals . Plant Cell Physiol . 59 : 1700 – 1713 . Zhang B. , Pan X. , Cobb G.P. , Anderson T.A. ( 2006 ) Plant microRNA: a small regulatory molecule with big impact . Dev. Biol. 289 : 3 – 16 . Google Scholar Crossref Search ADS PubMed Zhang W. , Thieme C.J. , Kollwig G. , Apelt F. , Yang L. , Winter N. , et al. ( 2016 ) tRNA-related sequences trigger systemic mRNA transport in plants . Plant Cell 28 : 1237 – 1249 . Google Scholar Crossref Search ADS PubMed © The Author(s) 2018. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Plant and Cell Physiology Oxford University Press

International Symposium on Long-Distance Signaling in Plants

Takatoshi, Kiba,
Plant and Cell Physiology , Volume 59 (9) – Sep 1, 2018
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Publisher
Oxford University Press
Copyright
© The Author(s) 2018. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oup.com
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0032-0781
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1471-9053
DOI
10.1093/pcp/pcy151
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Abstract

As sessile organisms, plants have developed elaborate means to optimize their metabolism and growth in response to environmental fluctuations. Although plants sense fluctuations only locally, their responses must be co-ordinated at the whole-plant level. Long-distance signaling between organs, via either xylem or phloem, is required for this co-ordination. Signaling molecules such as sugars, RNAs, polypeptides, phytohormones and peptide hormones have all been proposed to function as long-distance signals. Recently, great advances have been made in elucidating the molecular bases for long-distance signaling. Such advances were the focus of the Integrative Graduate Education and Research Program in Green Natural Sciences (IGER) International Symposium on Long-Distance Signaling in Plants, which was held on November 21, 2017 at Nagoya University, Japan. This report summarizes some of the new insights presented at this symposium by key researchers in the field. Long-Distance Signaling via RNAs All classes of RNA molecules, including small interfering RNAs (siRNAs), microRNAs (miRNAs), tRNAs and protein-encoding mRNAs, are detected in phloem exudates and are proposed to be mobile between tissues and organs (Kehr and Kragler 2018). Recent advances in analyzing the mobile transcriptome in heterografts indicate that a high number of mRNAs are transported via the phloem with tissue specificity and directionality (Notaguchi et al. 2015, Thieme et al. 2015); however, the molecular basis for mRNA mobility has been elusive. Friedrich Kragler (Max Planck Institute of Molecular Plant Physiology, Germany) and his colleagues studied how RNA motifs trigger mobility by conducting a bioinformatic analysis of mobile mRNAs. The team found that tRNA-like stem–bulge–stem–loop structures (TLSs) are enriched in mobile mRNAs (Guan et al. 2017). By assessing the long-distance mobility of reporter transcripts with or without the TLS motif, the team reported that TLS motifs are necessary and sufficient for long-distance transport of mRNAs (Zhang et al. 2016; see also Winter and Kragler 2018 in this Spotlight Issue). Plant miRNAs are 20–24 nucleotide-long non-coding RNAs that negatively regulate gene expression and have vital roles in many aspects of plant growth and developmental regulation (Zhang et al. 2006). Next-generation sequencing methods have identified an extensive number of miRNAs in phloem sap; however, the function of most of these miRNAs remains unknown. Tzyy-Jen Chiou (Academia Sinica, Taiwan) presented an excellent example of how a miRNA functions as a long-distance signal in the systemic regulation of phosphate (Pi) homeostasis. The Chiou group showed that, upon Pi starvation, miR399 is up-regulated first in the shoots and then moves via the phloem to the roots, where miR399 directs the cleavage of PHOSPHATE2 (PHO2) transcripts (Chien et al. 2017). PHO2 encodes ubiquitin-conjugating E2 enzyme 24 (UBC24) that modulates the activities of Pi acquisition and root to shoot Pi translocation by mediating the protein degradation of PHOSPHATE TRANSPORTER1 and the Pi efflux transporter PHOSPHATE1, respectively (Liu et al. 2012, Huang et al. 2013). These studies revealed how plants orchestrate the two activities, Pi acquisition at the root surface and Pi loading of xylem at the root stele, to maintain whole-plant Pi homeostasis by using an miRNA as a long-distance signal. In this issue, Chien et al. 2018 further discuss the potential cross-talk between various regulatory pathways underlying local and systemic responses to Pi deprivation. Long-Distance Signaling via Proteins Although many proteins are present in the phloem exudates of many plant species, we know very little about the signaling functions of these proteins. One of the best characterized examples is FLOWERING LOCUS T (FT) protein. FT protein moves from leaves to the shoot apex via phloem to act as a potent activator of flowering in many plants (Notaguchi et al. 2008, Putterill and Varkonyi-Gasic 2016). Xiangdong Fu (Chinese Academy of Sciences, China) and colleagues identified another example, ELONGATED HYPOCOTYL5 (HY5) (Chen et al. 2016). HY5 is a bZIP transcription factor that functions as a positive regulator of photomorphogenesis. Fu presented evidence that HY5 moves from shoots to roots via phloem to activate the high-affinity nitrate transporter gene NITRATE TRANSPORTER2.1 (NRT2.1) and represses the auxin signaling repressor gene SHORT HYPOCOTYL2, thereby promoting nitrate uptake and root growth. This example illustrates that long-distance movement of HY5 from shoots to roots co-ordinates carbon and nitrogen metabolism, thus enabling plants to orchestrate shoot and root growth at the whole-plant level in response to changes in the light environment. Long-Distance Signaling via Cytokinins Because vascular sap contains several phytohormones and their derivatives, it has long been proposed that phytohormones are involved in long-distance signaling (Hoad 1995, Kudo et al. 2010, Lacombe and Achard 2016); however, little is known about exactly how and why phytohormones are translocated long distances. Hitoshi Sakakibara (Nagoya University, Japan) reviewed his group’s recent progress in deciphering the molecular mechanism and the physiological role of cytokinin (CK) translocation. Previously, this team identified ABCG14, a member of the ABC transporter family, as a key factor for root to shoot translocation of CKs (Ko et al. 2014). Recently, Sakakibara’s group showed that plants have a dual root to shoot long-distance CK signaling system, in which two CK molecular species, trans-zeatin (tZ) and trans-zeatin riboside (tZR), convey different messages (Osugi et al. 2017). The root-borne tZ plays a role in controlling leaf size, whereas tZR is involved in regulating meristem activity-related traits. This dual long-distance cytokinin signaling system enables plants to fine-tune shoot growth in a manner responsive to environmental fluctuations. Sandrine Ruffel [French National Institute for Agricultural Research (INRA), France] has been focusing on the role of CKs in systemic nitrogen demand signaling. Since nitrogen is often distributed unevenly in the soil, plants utilize the systemic nitrogen demand signaling system, by which nitrogen starvation on one side of the root induces a compensatory up-regulation of nitrate uptake on the other side in a nitrogen-rich environment. Ruffel presented her group’s latest finding that tZ-type CKs in the shoot have an essential role in systemic nitrogen demand signaling (Poitout et al. 2018). The long-distance signaling of CKs and other nutrients is further reviewed by Ruffel (2018), in this issue. Long-Distance Signaling via Peptide Hormones At present, the importance of signaling peptides, now often referred to as ‘peptide hormones’, in diverse growth and developmental processes is well established (Matsubayashi 2014, Okamoto et al. 2016). Although most of the peptide hormones characterized so far mediate local signaling, Takuya Suzaki (University of Tsukuba, Japan) and Yoshikatsu Matsubayashi (Nagoya University, Japan) presented their evidence for mobile peptides. Suzaki summarized his lab’s studies of how legume plants control symbiosis using a peptide hormone as a long-distance signal. Leguminous plants engage in symbiosis with nitrogen-fixing soil rhizobia and form nodules. Because nodulation is an energy-consuming process, host plants control the number of nodules via long-distance signaling to balance the nitrogen demand and the energy cost. Previously, Suzaki’s colleagues identified Lotus japonicus CLAVATA3/ESR-RELATED ROOT SIGNAL2 (CLE-RS2) peptide as a root to shoot long-distance signal that inhibits nodulation (Okamoto et al. 2009, Okamoto et al. 2013). CLE-RS2 is highly up-regulated in roots by rhizobial inoculation and nitrate supplementation, and is perceived by the HYPERNODULATION ABERRANT ROOT FORMATION (HAR1) receptor in shoots. Suzaki’s group recently identified a key factor in the nitrate-responsive systemic inhibition of nodulation, NITRATE UNRESPONSIVE SYMBIOSIS1 (NRSYM1) (Nishida et al. 2018). In response to nitrate, NRSYM1, a NIN-LIKE PROTEIN transcription factor, accumulates in nuclei and directly activates CLE-RS2 expression, leading to the abolishment of nodulation. These studies revealed how leguminous plants respond to the nitrogen environment and control symbiosis by integrating environmental and symbiotic signals. This topic is the focus of the review by Nishida and Suzaki (2018), also featured in this Spotlight Issue. Matsubayashi’s group has thus far identified two classes of mobile peptides involved in systemic nitrogen demand signaling. One class is C-TERMINALLY ENCODED PEPTIDEs (CEPs) that are up-regulated in nitrogen-starved roots, transported to shoots and perceived by CEP RECEPTORs (CEPRs) (Tabata et al. 2014). The other class is CEP DOWNSTREAMs (CEPDs) that are induced in shoot phloem in a CEP/CEPR-dependent manner, transported to roots and activate nitrate uptake through up-regulation of NRT2.1 (Ohkubo et al. 2017). An important future challenge will be to elucidate the relationship between tZ-type CK-mediated and CEP–CEPD-mediated systemic nitrogen demand signaling systems. During the poster session, Fuminori Takahashi (RIKEN CSRS, Japan) presented his team’s recent discovery that CLE25 peptide functions as a root to shoot water deficiency signal (Takahashi et al. 2018). Many uncharacterized peptides have been identified by xylem sap peptidomics (Okamoto et al. 2015), suggesting that peptide hormones have a much broader role in long-distance signaling. Yoshikatsu Matsubayashi closed the symposium by emphasizing that plant long-distance signaling research is still an emerging field that requires networking and collaboration to establish and expand this field further. Indeed, this symposium not only provided a fantastic opportunity to kick-start networking and collaboration within the field, but also proved to be a huge success with exciting prospects ahead in terms of the quality of science presented. On behalf of the organizing committee, I thank the presenters and sponsors for their great contributions to the symposium. Disclosures The author has no conflicts of interest to declare. References Chen X. , Yao Q. , Gao X. , Jiang C. , Harberd N.P. , Fu X. ( 2016 ) Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition . Curr. Biol . 26 : 640 – 646 . Google Scholar Crossref Search ADS PubMed Chien P.-S. , Chiang C.-P. , Leong S.J. , Chiou T.-J. ( 2018 ) Sensing and signaling of phosphate starvation—from local to long distance . Plant Cell Physiol . 59 : 1714 – 1722 . Chien P.S. , Chiang C.B. , Wang Z.R. , Chiou T.J. ( 2017 ) MicroRNA-mediated signaling and regulation of nutrient transport and utilization . Curr. Opin. Plant Biol. 39 : 73 – 79 . Google Scholar Crossref Search ADS PubMed Guan D. , Yan B. , Thieme C. , Hua J. , Zhu H. , Boheler K.R. , et al. ( 2017 ) PlaMoM: a comprehensive database compiles plant mobile macromolecules . Nucleic Acids Res. 45 : D1021 – D1028 . Google Scholar Crossref Search ADS PubMed Hoad G.V. ( 1995 ) Transport of hormones in the phloem of higher-plants . Plant Growth Regul. 16 : 173 – 182 . Google Scholar Crossref Search ADS Huang T.K. , Han C.L. , Lin S.I. , Chen Y.J. , Tsai Y.C. , Chen Y.R. , et al. ( 2013 ) Identification of downstream components of ubiquitin-conjugating enzyme PHOSPHATE2 by quantitative membrane proteomics in Arabidopsis roots . Plant Cell 25 : 4044 – 4060 . Google Scholar Crossref Search ADS PubMed Kehr J. , Kragler F. ( 2018 ) Long distance RNA movement . New Phytol. 218 : 29 – 40 . Google Scholar Crossref Search ADS PubMed Ko D. , Kang J. , Kiba T. , Park J. , Kojima M. , Do J. , et al. ( 2014 ) Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin . Proc. Natl. Acad. Sci. USA 111 : 7150 – 7155 . Google Scholar Crossref Search ADS Kudo T. , Kiba T. , Sakakibara H. ( 2010 ) Metabolism and long-distance translocation of cytokinins . J. Integr. Plant Biol. 52 : 53 – 60 . Google Scholar Crossref Search ADS PubMed Lacombe B. , Achard P. ( 2016 ) Long-distance transport of phytohormones through the plant vascular system . Curr. Opin. Plant Biol. 34 : 1 – 8 . Google Scholar Crossref Search ADS PubMed Liu T.Y. , Huang T.K. , Tseng C.Y. , Lai Y.S. , Lin S.I. , Lin W.Y. , et al. ( 2012 ) PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis . Plant Cell 24 : 2168 – 2183 . Google Scholar Crossref Search ADS PubMed Matsubayashi Y. ( 2014 ) Posttranslationally modified small-peptide signals in plants . Annu. Rev. Plant Biol. 65 : 385 – 413 . Google Scholar Crossref Search ADS PubMed Nishida H. , Suzaki T. ( 2018 ) Two negative regulatory systems of root nodule symbiosis—how are symbiotic benefits and costs balanced? Plant Cell Physiol . 59 : 1733 – 1738 . Nishida H. , Tanaka S. , Handa Y. , Ito M. , Sakamoto Y. , Matsunaga S. , et al. ( 2018 ) A NIN-LIKE PROTEIN mediates nitrate-induced control of root nodule symbiosis in Lotus japonicus . Nat. Commun. 9 : 499. Google Scholar Crossref Search ADS PubMed Notaguchi M. , Abe M. , Kimura T. , Daimon Y. , Kobayashi T. , Yamaguchi A. , et al. ( 2008 ) Long-distance, graft-transmissible action of Arabidopsis FLOWERING LOCUS T protein to promote flowering . Plant Cell Physiol . 49 : 1645 – 1658 . Google Scholar Crossref Search ADS PubMed Notaguchi M. , Higashiyama T. , Suzuki T. ( 2015 ) Identification of mRNAs that move over long distances using an RNA-Seq analysis of Arabidopsis/Nicotiana benthamiana heterografts . Plant Cell Physiol . 56 : 311 – 321 . Google Scholar Crossref Search ADS PubMed Ohkubo Y. , Tanaka M. , Tabata R. , Ogawa-Ohnishi M. , Matsubayashi Y. ( 2017 ) Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition . Nat. Plants 3 : 17029. 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Journal

Plant and Cell Physiology – Oxford University Press

Published: Sep 1, 2018

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