Plant Physiology

doi: 10.1104/pp.18.01538pmid: 30610129

Minorsky, Peter V.

doi: 10.1104/pp.18.01511pmid: N/A

Plant Reactive Oxygen Species Enhance Virus Spread by Aphids Hemipterans, a group of phloem-feeding insects that includes aphids, planthoppers, and whiteflies, are responsible for the spread of most plant viruses from plant to plant. Stylet positioning and feeding activities have important consequences for the acquisition and transmission of viruses by insect vectors. Persistently transmitted viruses typically benefit from sustained vector feeding from the phloem. In contrast, nonpersistently transmitted viruses (NPTVs) benefit when insect vectors frequently change the feeding location or even the host plant, because these changes increase the probability of virus acquisition and transmission. Aphids, which are the most well-studied vectors of plant viruses, transmit over 300 plant viruses, and most are NPTVs. Aphids generally probe more frequently when there are stronger plant defenses in the epidermis and mesophyll tissues (i.e. when they confront high levels of reactive oxygen species [ROS], activation of phytohormone-mediated resistance, cross-linking of the cell wall, and deposition of callose). These plant defenses and their associated molecular signaling can be modified by some virus-encoded proteins. For example, the 2b protein, which is encoded by the NPTV Cucumber mosaic virus (CMV), is a well-studied suppressor of host RNA interference (RNAi) that targets the host’s RNA-binding protein ARGONAUTE1 (AGO1). AGO1 is required for a number of pathogen-associated molecular pattern-triggered immunity responses, including callose deposition. Guo et al. (pp. 143–155) report that, compared with a CMVD2b viral strain that has a deletion of the viral suppressor of RNAi 2b protein, plants infected with wild-type CMV produce higher concentrations of the ROS H2O2 in plant tissues. Aphids on wild-type CMV-infected plants also engage in shorter probes and less phloem feeding relative to CMVD2b-infected plants. Therefore, the frequency of virus acquisition and the virus load per aphid were greater on CMV-infected plants than on CMVD2b-infected plants. Aphids also moved away from initial feeding sites more frequently on wild-type CMV-infected versus CMVD2b-infected plants. H2O2 levels were not elevated in CMV-infected tobacco (Nicotiana tabacum) plant strains that were deficient in the induction of ROS production, and aphid behavior was unchanged on these strains. These results suggest that CMV uses its viral suppressor of RNAi protein to increase plant ROS levels, thereby enhancing its acquisition and transmission by vector insects. Auxin Function in a Brown Alga Auxin controls body plan patterning in land plants, and it has been proposed to play a similar role in the development of brown algae (Phaeophyta) despite their distant evolutionary relationship with land plants. In flowering plants and many multicellular brown algae, the establishment of the apical-basal pattern is produced through an initial asymmetric cell division pattern. The apical cell grows into the shoot meristem or thallus, while the basal cell develops into the suspensor and root pole or rhizoids in land plants and brown algae, respectively. In land plants, the phytohormone auxin plays a crucial role in the establishment of this apical-basal axis and the subsequent embryo patterning. The mechanism of auxin action in brown algae remains controversial because of contradictory conclusions from pharmacological studies. These disparities may have arisen due to differences in the strains used, the time of their collection, and differences in experimental conditions such as pH and light. Bogaert et al. (pp. 280–299) have used Dictyota dichotoma as a model system to show that auxin plays a role during the apical-basal patterning of the embryo of D. dichotoma. Indole-3-acetic acid was detectable in D. dichotoma germlings and mature tissue. Although two-celled D. dichotoma zygotes normally develop a rhizoid from one pole and a thallus meristem from the other, the addition of exogenous auxins to one-celled embryos affected polarization, and both poles of the spheroidal embryo developed into rhizoids instead. An in silico survey of auxin genes suggested a diverse range of auxin biosynthesis and transport genes in D. dichotoma, including PIN-LIKES and ATP-binding cassette subfamily (ABCB) transporters. An inhibitor of the ABCB/multidrug resistance/P58 glycoprotein subfamily of transporters in land plants affected rhizoid formation by increasing rhizoid branching and inducing ectopic rhizoids. Together with reports of auxin function in basal lineages of green algae, these results suggest that auxin function predates the divergence between the green and brown lineages and the transition toward land plants. New Insights into Carboxysomes Despite its essential role in photosynthetic carbon fixation, Rubisco is a relatively inefficient enzyme, due in part to its inability to discriminate between CO2 and oxygen as substrates. To suppress the oxygenase reaction and enhance the carboxylase activity of Rubisco, cyanobacteria have specialized bacterial microcompartments (BMCs) called carboxysomes that are central components of these organisms’ CO2-concentrating mechanisms (CCMs). Understanding the molecular mechanism underlying Rubisco assembly and carboxysome biogenesis may prove useful for engineering functional CO2-fixing complexes in other photosynthetic organisms, especially plants, with the aim of boosting photosynthesis and agricultural productivity. There are two types of carboxysomes, distinguished by the form of Rubisco they encapsulate: form IA in α-carboxysomes and form IB in β-carboxysomes. In β-carboxysomes, form IB Rubisco and carbonic anhydrase are densely packed into an ordered matrix with internal linker proteins to form the enzyme core, which is encapsulated by a proteinaceous shell. The shell acts as a selective barrier that is permeable to bicarbonate and ribulose-1,5-bisphosphate, the substrates of Rubisco. The shells of carboxysomes consist of three protein types, each named after the oligomer it forms: BMC-H (hexamer), BMC-P (pentamer), and BMC-T (trimer). These three protein types form cyclic homooligomers with pores at the center of symmetry that enable metabolite transport across the shell. Carboxysome shells contain multiple BMC-H paralogs, each with distinctly conserved residues surrounding the pore, which are assumed to be associated with specific metabolites. Sommer et al. (pp. 156–167) have examined the regulation of β-carboxysome shell composition by investigating the BMC-H-encoding genes ccmK3 and ccmK4. A recent comprehensive survey of carboxysome genes in β-cyanobacteria showed that ccmK3 and ccmK4 genes always co-occur; although functionally linked, the two proteins are not redundant. The current study provides evidence that CcmK3 does not form homohexamers but, rather, that CcmK3 and CcmK4 form a heterohexameric complex with a 1:2 stoichiometry that can further form dodecamers under certain conditions. The authors suggest that heterohexamer formation could provide a means of fine-tuning β-carboxysome shell permeability. Moreover, the observed formation of dodecamers in solution suggests that carboxysome shell permeability may be dynamically attenuated by capping hexamers with a second hexamer. Heterohexamer formation and capping could provide a rapid and reversible means to alter metabolite flux across the shell in response to environmental/growth conditions. A second contribution in this issue relating to carboxysomes concerns a chaperone protein, RbcX, that is essential for proper protein folding and Rubisco assembly. Huang et al. (pp. 184–194) have investigated the in vivo function of RbcX in Synechococcus using molecular, biochemical, and live-cell fluorescence imaging approaches. Their results show that genetic deletion of the rbcX gene affects Rubisco abundance as well as carboxysome formation and spatial distribution. Moreover, RbcX appears to be a component of the carboxysome and shows a dynamic interaction with Rubisco enzymes. Dark-Induced Nuclear Positioning in Leaf Cells The appropriate spatial arrangement of nuclei is essential for various cellular activities during cell division, growth, migration, and differentiation in eukaryotes. In plants, nuclear positioning also is required for proper responses to environmental stimuli, including pathogen infection, touch, temperature, and light. The nuclei of Arabidopsis (Arabidopsis thaliana) leaf cells move to the anticlinal walls of cells in response to strong ultraviolet-A light. This response mitigates the DNA damage and cell death caused by ultraviolet irradiation. Light-induced nuclear positioning depends on chloroplast movement. Nuclei cannot move by themselves; instead, nucleus-attached chloroplasts carry the nuclei to anticlinal walls of cells. Light-induced chloroplast movement is a well-known process that is regulated by the blue light receptor phototropins, actin filaments, and several regulatory proteins. Hence, in mutants lacking these proteins, this type of nuclear positioning does not occur. Unlike light-induced nuclear positioning, the mechanism underlying dark-induced nuclear positioning is not fully understood. Iwabuchi et al. (pp. 233–247) show that ANGUSTIFOLIA (AN) and ACTIN7 regulate centripetal nuclear positioning in Arabidopsis leaves. Two mutants defective in the positioning of nuclei in the dark were isolated and designated as unusual nuclear positioning1 (unp1) and unp2. In the dark, nuclei of unp1 were positioned at the anticlinal walls of adaxial and abaxial mesophyll cells and abaxial pavement cells, whereas the nuclei of unp2 were positioned at the anticlinal walls of mesophyll and pavement cells on both the adaxial and abaxial sides. unp1 was caused by a dominant-negative mutation in ACTIN7, and unp2 resulted from a recessive mutation in AN. Actin filaments in unp1 were fragmented and reduced in number, which led to pleiotropic defects in nuclear morphology, cytoplasmic streaming, and plant growth. The mutation in AN caused aberrant positioning of nuclei-associated actin filaments at the anticlinal walls. AN also interacts physically with plant-specific dual-specificity Tyr phosphorylation-regulated kinases (DYRKPs). The results presented suggest that the AN-DYRKP complex regulates the alignment of actin filaments during centripetal nuclear positioning in leaf cells. Hydrogen Cyanide Regulation by S-Cyanylation Despite its toxicity, cyanide has been proposed to act as a regulator of several biological processes such as seed dormancy and germination and resistance to fungal and viral infection. Arabidopsis null mutants of the mitochondrial enzyme β-CYANOALANINE SYNTHASE (CAS-C1) accumulate cyanide to apparently nontoxic levels, as the plants are completely viable, but show a root hairless phenotype suggesting a signaling role in root development. Garcia et al. (pp. 107–123) have performed a quantitative proteomic analysis of mitochondrially enriched samples isolated from cas-c1 mutants and wild-type plants. Their analysis reveals significant changes in protein content: 451 proteins were absent or less abundant in cas-c1 and 353 proteins were only present or more abundant in cas-c1. Gene Ontology classification of these proteins identified proteomic changes that explain the root hairless phenotype and the altered immune response observed in the cas-c1 mutant. The authors analyzed the molecular mechanism by which cyanide can act as a signaling molecule. Gene Ontology classification and protein-protein interaction cluster analysis showed that S-cyanylation is involved in the regulation of primary metabolic pathways, such as glycolysis, and the Calvin and S-adenosyl-Met cycles. Author notes www.plantphysiol.org/cgi/doi/10.1104/pp.18.01511 © 2019 American Society of Plant Biologists. All Rights Reserved. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)

Minorsky, Peter V.

doi: 10.1104/pp.18.01511pmid: N/A

Mhamdi, Amna; Gommers, Charlotte M.M.

doi: 10.1104/pp.18.01421pmid: 30610130

The nuclear genome encodes the majority of chloroplast-localized proteins and, in return, chloroplasts exert some control over nuclear gene expression via so-called retrograde signals. These signals derive from developing chloroplasts (referred to as biogenic signals) or from mature chloroplasts in response to environmental constraints such as excessive light, drought, or heat (referred to as operational signals; Crawford et al., 2018; Dubreuil et al., 2018; Hernández-Verdeja and Strand, 2018). The major nuclear targets of plastid signals are photosynthesis-associated nuclear genes (PhANGs); retrograde signals also target developmental processes such as seedling photomorphogenesis (Martín et al., 2016). Despite the plethora of research focusing on chloroplast signaling, retrograde signals remain poorly understood and probably consist of several signals including reactive oxygen species and metabolites (Fig. 1). In most studies, biogenic retrograde signaling is induced by the inhibition of carotenoid biosynthesis using norflurazon or by the inhibition of plastid translation using lincomycin, which inhibit PhANG expression. Six Arabidopsis (Arabidopsis thaliana) genomes uncoupled (gun) mutants have been isolated that maintain PhANG expression under these treatments (Susek et al., 1993). All six original GUN proteins are localized in the chloroplast; GUN2 to GUN6 act in the tetrapyrrole synthesis pathway, and GUN1 is a pentatricopeptide repeat protein, responding to disruptions in plastid gene expression. Figure 1. Open in new tabDownload slide Updated model of biogenic retrograde signals. The current model omits ABI4 and PTM and highlights different GUN proteins and intermediates derived from the tetrapyrrole biosynthesis pathway. GUN1 is believed to be a signal integrator. GUN6 (FERROCHELATASE1), GUN2 (HEME OXYGENASE1), and GUN3 (PHYTOCHROMOBILIN SYNTHASE) are involved in the heme branch of tetrapyrrole biosynthesis. GUN5 (SUBUNIT OF MG-CHELATASE) and GUN4 (a porphyrin-binding protein that enhances the activity of MG-CHELATASE) are involved in the biosynthesis of Mg-protoporphyrin IX. Tetrapyrrole intermediates such as Mg-protoporphyrin IX and heme are suggested to be exported from plastids to the nucleus and to act as regulators of PhANGs. The transport mechanism involved in signaling remains unknown, and nuclear targets of retrograde signals, although via unknown mechanisms, are the transcription factors GOLDEN-LIKE1 (GLK1), GLK2, ELONGATED HYPOCOTYL5 (HY5), and the blue-light receptor CRYPTOCHROME1 (CRY1). Figure 1. Open in new tabDownload slide Updated model of biogenic retrograde signals. The current model omits ABI4 and PTM and highlights different GUN proteins and intermediates derived from the tetrapyrrole biosynthesis pathway. GUN1 is believed to be a signal integrator. GUN6 (FERROCHELATASE1), GUN2 (HEME OXYGENASE1), and GUN3 (PHYTOCHROMOBILIN SYNTHASE) are involved in the heme branch of tetrapyrrole biosynthesis. GUN5 (SUBUNIT OF MG-CHELATASE) and GUN4 (a porphyrin-binding protein that enhances the activity of MG-CHELATASE) are involved in the biosynthesis of Mg-protoporphyrin IX. Tetrapyrrole intermediates such as Mg-protoporphyrin IX and heme are suggested to be exported from plastids to the nucleus and to act as regulators of PhANGs. The transport mechanism involved in signaling remains unknown, and nuclear targets of retrograde signals, although via unknown mechanisms, are the transcription factors GOLDEN-LIKE1 (GLK1), GLK2, ELONGATED HYPOCOTYL5 (HY5), and the blue-light receptor CRYPTOCHROME1 (CRY1). How the retrograde signaling is perceived by the nucleus is still enigmatic, and in this context, the transcription factor ABSCISIC ACID INSENSITIVE4 (ABI4) was proposed to act as a nuclear target of the GUN1-mediated retrograde signals (Nott et al., 2006; Koussevitzky et al., 2007; Sun et al., 2011). Several reports showed that abi4 mutants have a weak gun phenotype exhibiting elevated PhANG expression following norflurazon treatment. In addition, many photosynthesis-related nuclear genes controlled by plastid signals contain abscisic acid-responsive elements in their promoters (Koussevitzky et al., 2007). Surprisingly, several research groups were unable to reproduce the gun phenotype described for abi4 mutants. In this issue of Plant Physiology, Kacprzak et al. (2019) address this by analyzing the gun phenotypes in multiple abi4 alleles in different laboratories. The authors show that abi4 mutants, unlike gun1, failed to restore the expression of a set of PhANGs in the presence of norflurazon and lincomycin. Thus, Kacprzak et al. (2019) convincingly demonstrate that ABI4 is not a target of retrograde signaling and should be omitted from future models of biogenic retrograde signaling. Interestingly, the same researchers last year dismantled another gun-like mutant. The plastid transmembrane-localized transcription factor PTM was once described as being activated by GUN1. After this activation, the cleaved PTM moved to the nucleus, where it promoted ABI4 expression and repressed PhANG expression. However, with an approach similar to that presented here, Page et al. (2017) concluded that PTM should be excluded as a major player in retrograde signaling. Based on these results, it would be interesting to further investigate the factors that might explain discrepancies with the original studies, especially in the case of abi4, since several groups previously reported a gun-like phenotype for abi4. Together, these studies finally resolved uncertainties surrounding the roles of ABI4 and PTM in retrograde signaling. They point to the need to have several lines of evidence supporting our conclusions and to carefully question the biological relevance of data. The work of Kacprzak and colleagues proves that much work remains to be done to understand the complex organellar signaling events during development and stress responses. An important starting point would be to unravel the function of GUN1, the main mediator of retrograde signaling. Recent work has shown that GUN1 is involved in chloroplast biogenesis as well as retrograde signaling. Rapid protein turnover in green tissues helps to specify GUN1 accumulation during plastid development and stress (Song et al., 2018; Wu et al., 2018; Zhao et al., 2018). Nevertheless, it remains unknown how GUN1 degradation is prevented in the absence of functioning chloroplasts and what type of signal this releases. Future endeavors will help bridge our understanding of chloroplast damage, GUN1 accumulation, nuclear gene expression, and ultimately plant performance. To achieve this, we need a multidisciplinary approach and possibly many more guns to be dismantled. LITERATURE CITED Crawford T , Lehotai N, Strand Å ( 2018 ) The role of retrograde signals during plant stress responses . J Exp Bot 69 : 2783 – 2795 Google Scholar Crossref Search ADS PubMed WorldCat Dubreuil C , Jin X, Barajas-López JD, Hewitt TH, Tanz S, Dobrenel T, Schröder W, Hanson J, Pesquet E, Grönlund A, et al. ( 2018 ) Establishment of photosynthesis through chloroplast development is controlled by two distinct regulatory phases . Plant Physiol 176 : 1199 – 1214 Google Scholar Crossref Search ADS PubMed WorldCat Hernández-Verdeja T , Strand Å ( 2018 ) Retrograde signals navigate the path to chloroplast development . Plant Physiol 176 : 967 – 976 Google Scholar Crossref Search ADS PubMed WorldCat Kacprzak SM , Mochizuki N, Naranjo B, Xu D, Leister D, Kleine T, Okamoto H, Terry MJ ( 2019 ) Plastid-to-nucleus retrograde signalling during chloroplast biogenesis does not require ABI4 . Plant Physiol Google Scholar OpenURL Placeholder Text WorldCat Koussevitzky S , Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J ( 2007 ) Signals from chloroplasts converge to regulate nuclear gene expression . Science 316 : 715 – 719 Google Scholar Crossref Search ADS PubMed WorldCat Martín G , Leivar P, Ludevid D, Tepperman JM, Quail PH, Monte E ( 2016 ) Phytochrome and retrograde signalling pathways converge to antagonistically regulate a light-induced transcriptional network . Nat Commun 7 : 11431 Google Scholar Crossref Search ADS PubMed WorldCat Nott A , Jung HS, Koussevitzky S, Chory J ( 2006 ) Plastid-to-nucleus retrograde signaling . Annu Rev Plant Biol 57 : 739 – 759 Google Scholar Crossref Search ADS PubMed WorldCat Page MT , Kacprzak SM, Mochizuki N, Okamoto H, Smith AG, Terry MJ ( 2017 ) Seedlings lacking the PTM protein do not show a genomes uncoupled (gun) mutant phenotype . Plant Physiol 174 : 21 – 26 Google Scholar Crossref Search ADS PubMed WorldCat Song L , Chen Z, Larkin RM ( 2018 ) The genomes uncoupled mutants are more sensitive to norflurazon than wild type . Plant Physiol 178 : 965 – 971 Google Scholar Crossref Search ADS PubMed WorldCat Sun X , Feng P, Xu X, Guo H, Ma J, Chi W, Lin R, Lu C, Zhang L ( 2011 ) A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus . Nat Commun 2 : 477 Google Scholar Crossref Search ADS PubMed WorldCat Susek RE , Ausubel FM, Chory J ( 1993 ) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development . Cell 74 : 787 – 799 Google Scholar Crossref Search ADS PubMed WorldCat Wu GZ , Chalvin C, Hoelscher M, Meyer EH, Wu XN, Bock R ( 2018 ) Control of retrograde signaling by rapid turnover of GENOMES UNCOUPLED1 . Plant Physiol 176 : 2472 – 2495 Google Scholar Crossref Search ADS PubMed WorldCat Zhao X , Huang J, Chory J ( 2018 ) genome uncoupled1 mutants are hypersensitive to norflurazon and lincomycin . Plant Physiol 178 : 960 – 964 Google Scholar Crossref Search ADS PubMed WorldCat Author notes 1 Author for contact: [email protected]. 2 Senior author. www.plantphysiol.org/cgi/doi/10.1104/pp.18.01421 © 2019 American Society of Plant Biologists. All Rights Reserved. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)

Mhamdi, Amna; Gommers, Charlotte M.M.

doi: 10.1104/pp.18.01421pmid: 30610130

Nagel, Raimund

doi: 10.1104/pp.18.01403pmid: 30610131

Nagel, Raimund

doi: 10.1104/pp.18.01403pmid: 30610131

We think of enzymes as highly specific catalysts that carry out one reaction and show nearly absolute substrate specificity. However, absolute specificity is the exception, not the rule, as most enzymes accept several structurally similar substrates. Moreover, many enzymes catalyze alternative reactions and, in some cases, even perform functions that are best described as nonenzymatic (Moore, 2004; Huberts and van der Klei, 2010). These alternative functions are sometimes referred to as moonlighting activity. A recent example of such an enzyme with a nonenzymatic function was published in this issue of Plant Physiology (Schmid et al., 2018). The authors showed that the nuclear-encoded plastid UMP kinase from Arabidopsis (Arabidopsis thaliana), PUMPKIN, catalyzes the phosphorylation of UMP to UDP with the cosubstrate ATP. While the kinetic parameters are similar to the characterized homolog from E. coli, the loss of enzymatic function alone in transfer DNA insertion and RNAi lines could not explain the phenotype of severe growth retardation, photobleaching, and an increase in generation time (∼21 weeks versus ∼ 8 weeks for the wild type). Through quantitation of major plastid proteins and analysis of de novo protein synthesis rates, the authors showed that the loss of PUMPKIN affects protein translation in plastids. They followed this up with experiments that show that PUMPKIN is a compound of several large protein complexes in the plastid, of which some are sensitive to RNase treatment. RNA-immunoprecipitation combined with deep sequencing and additional experiments convincingly showed that PUMPKIN associates with group II introns of five genes of the chloroplast genome. PUMPKIN stabilizes its target RNAs but does not seem to be involved in splicing of these introns. Interestingly, a small number of group II introns are catalytically active ribozymes that self-excise from their mRNA in vitro; however, in vivo proteins are usually required for splicing of group II introns (Bonen and Vogel, 2001). The mechanism by which PUMPKIN stabilizes its RNA targets is unknown, and no known RNA-binding motifs were found in PUMPKIN. Therefore, the identity of the RNA sequence and/or 3D structure that is bound remains a target of future research. The authors speculate that multimerization of PUMPKIN could explain RNA binding, given that its enzymatic function already involves binding of one RNA monophosphate nucleotide. Thus, individual subunits of a multimeric enzyme could bind an RNA sequence with high enough affinity. In light of this research, we have to ask ourselves: how often are we overlooking moonlighting activities? And does moonlighting activity explain why in vitro biochemical characterizations cannot always be linked to mutant phenotypes? LITERATURE CITED Bonen L , Vogel J ( 2001 ) The ins and outs of group II introns . Trends Genet 17 : 322 – 331 Google Scholar Crossref Search ADS PubMed WorldCat Huberts DH , van der Klei IJ ( 2010 ) Moonlighting proteins: an intriguing mode of multitasking . Biochim Biophys Acta 1803 : 520 – 525 Google Scholar Crossref Search ADS PubMed WorldCat Moore Bd ( 2004 ) Bifunctional and moonlighting enzymes: lighting the way to regulatory control . Trends Plant Sci 9 : 221 – 228 Google Scholar Crossref Search ADS PubMed WorldCat Schmid L-M , Ohler L, Möhlmann T, Brachmann A, Muiño J, Leister D, Meurer J, Manavski N ( 2018 ) PUMPKIN, the sole plastid UMP Kinase associates with Group II Introns and impacts their metabolism . Plant Physiology 179 : 248 – 264 Google Scholar Crossref Search ADS PubMed WorldCat Author notes 1 Author for contact: [email protected]. 2 Senior author. www.plantphysiol.org/cgi/doi/10.1104/pp.18.01403 © 2019 American Society of Plant Biologists. All Rights Reserved. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)

Boavida, Leonor C.

doi: 10.1104/pp.18.01455pmid: 30610132

Most of the carbon dioxide sequestered by plants during photosynthesis is converted into sugars and stored into polysaccharide-enriched cells walls that constitute the majority of the plant biomass. While plants have long been considered a valuable resource of biomaterials for the chemical and textile industries, recent efforts have been directed toward the use of lignocellulosic materials as a feedstock for the sustainable production of second-generation biofuels (Carpita and McCann, 2008). These efforts have prioritized the search for plants with enhanced biomass yields and higher conversion efficiency of lignocellulose into sugars (saccharification; Himmel et al., 2007). However, the genetic manipulation of cell wall composition often has been challenging, resulting in severe alterations in plant growth and development (Kumar et al., 2016). New genetic strategies targeting cellulose synthase activity or key regulatory factors in lignin biosynthesis have proven to be more effective in modifying the composition of secondary cell walls, achieving superior saccharification efficiencies without compromising plant growth (Li et al., 2018; Xie et al., 2018). Hybrids and polyploids often are associated with plant growth vigor, higher yields, and enhanced fitness (Comai, 2005). These characteristics have been widely used by plant breeders to improve biomass production in economically interesting species (Sattler et al., 2016). But do plants with higher ploidy levels always perform better? In particular, it is not well understood how increased ploidy levels affect the composition of the plant biomass. In this issue of Plant Physiology, Corneillie et al. (2018) conducted a series of kinematic, morphometric, and chemical analyses to assess how growth rates, biomass yield, and cell wall composition are affected in plants with increased ploidy levels (2n, 4n, 6n, and 8n) in Arabidopsis (Arabidopsis thaliana; Fig. 1). The authors show that plants with higher ploidy display a general increase in cell size, flowers, and seeds, a phenomenon that has been described as the Gigas effect (Knight and Beaulieu, 2008). However, increased ploidy in Arabidopsis comes with a fitness cost. Polyploids show an overall reduction in growth rates and delayed flowering. The increase in cell size is accompanied by a proportional reduction in cell proliferation, which significantly affects the vigor of hexaploid and octaploid plants. These detrimental effects are thought to result from a tradeoff between DNA nuclear volume/content and the cost of the cell cycle, usually referred to as the high-ploidy syndrome (Tsukaya, 2008). As a result, only tetraploids exhibit a significant increase in biomass yield, which was noticeably reverted in hexaploids and octaploids (Fig. 1). To further investigate the effects of plant growth, the authors analyzed cell wall structure and composition. Higher ploidy levels were associated with a proportional reduction in secondary cell wall deposition, lignin and cellulose content, which occurs with a compensatory increase in hemicelluloses, pectin, extensins, and arabinogalactan proteins. The observed reduction in lignin content and the parallel increase of other cell wall polysaccharides were associated with an increase in saccharification yield in higher polyploids. Figure 1. Open in new tabDownload slide Arabidopsis rosettes with increased ploidy levels. Variations in somatic ploidy levels are associated with increase in cell size and delayed development with an impact in biomass content (figure 1C in Corneillie et al., 2018). Figure 1. Open in new tabDownload slide Arabidopsis rosettes with increased ploidy levels. Variations in somatic ploidy levels are associated with increase in cell size and delayed development with an impact in biomass content (figure 1C in Corneillie et al., 2018). Taken together, the results of Corneillie et al. (2018) show that Arabidopsis polyploids display substantial phenotypic variation with respect to growth characteristics and biomass accumulation. These results are consistent with an optimum balance for chromosome number, beyond which polyploid individuals become less vigorous. The findings of Corneillie et al. (2018) further indicate that the composition of cell walls in plants with higher ploidy levels present alterations that are seen as critical quality criteria for the production of biofuels. While Arabidopsis has been a powerful model system for plant cell wall research, finding mutants that affect cell wall features in polyploid species is certainly a challenge. Given that most of our current crops are natural or domesticated hybrids and polyploids, it is expected that the manipulation of ploidy levels can be explored further as a viable route to fulfill our needs for novel cultivars with improved biomass quality for renewable bioenergy production. LITERATURE CITED Carpita NC , McCann MC ( 2008 ) Maize and sorghum: Genetic resources for bioenergy grasses . Trends Plant Sci 13 : 415 – 420 Google Scholar Crossref Search ADS PubMed WorldCat Comai L ( 2005 ) The advantages and disadvantages of being polyploid . Nat Rev Genet 6 : 836 – 846 Google Scholar Crossref Search ADS PubMed WorldCat Corneillie S , De Storme N, Van Acker R, Fangel JU, De Bruyne M, De Rycke RM, Geelen DNV, Willats WGT, Vanholme B, Boerjan WA ( 2018 ) Polyploidy affects plant growth and alters cell wall composition . Plant Physiol pp.00967.2018 Google Scholar OpenURL Placeholder Text WorldCat Himmel ME , Ding SY, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD ( 2007 ) Biomass recalcitrance: Engineering plants and enzymes for biofuels production . Science 315 : 804 – 807 Google Scholar Crossref Search ADS PubMed WorldCat Knight CA , Beaulieu JM ( 2008 ) Genome size scaling through phenotype space . Ann Bot 101 : 759 – 766 Google Scholar Crossref Search ADS PubMed WorldCat Kumar M , Campbell L, Turner S ( 2016 ) Secondary cell walls: Biosynthesis and manipulation . J Exp Bot 67 : 515 – 531 Google Scholar Crossref Search ADS PubMed WorldCat Li F , Liu S, Xu H, Xu Q ( 2018 ) A novel FC17/CESA4 mutation causes increased biomass saccharification and lodging resistance by remodeling cell wall in rice . Biotechnol Biofuels 11 : 298 Google Scholar Crossref Search ADS PubMed WorldCat Sattler MC , Carvalho CR, Clarindo WR ( 2016 ) The polyploidy and its key role in plant breeding . Planta 243 : 281 – 296 Google Scholar Crossref Search ADS PubMed WorldCat Tsukaya H ( 2008 ) Controlling size in multicellular organs: Focus on the leaf . PLoS Biol 6 : e174 Google Scholar Crossref Search ADS PubMed WorldCat Xie M , Zhang J, Tschaplinski TJ, Tuskan GA, Chen JG, Muchero W ( 2018 ) Regulation of lignin biosynthesis and its role in growth-defense tradeoffs . Front Plant Sci 9 : 1427 Google Scholar Crossref Search ADS PubMed WorldCat Author notes 1 This work was supported by Purdue University. 2 Author for contact: [email protected] 3 Senior author. www.plantphysiol.org/cgi/doi/10.1104/pp.18.01455 © 2019 American Society of Plant Biologists. All Rights Reserved. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)

Boavida, Leonor C.

doi: 10.1104/pp.18.01455pmid: 30610132