PLANT PHYSIOLOGY

Minorsky, Peter V.

doi: 10.1104/pp.20.01131pmid: 33814632

A Novel Form of Crosstalk between GA and ABA The negative interaction between GA and the stress hormone abscisic acid (ABA) has been studied for many years in numerous plant species. These studies suggest that GA and ABA negatively affect each other’s biosynthesis and signaling. The nuclear DELLA proteins suppress almost all GA responses by interacting with various transcription factors. ABA plays a central role in the regulation of stomatal closure under water-deficit conditions. Previously, Shohat et al. (pp. 518–528) demonstrated that a gibberellin response inhibitor in tomato (Solanum lycopersicum), the DELLA protein PROCERA (PRO), promotes ABA-induced stomatal closure and gene transcription in guard cells. Their attention has now turned to the question of how PRO affects stomatal closure. PRO does not affect ABA accumulation in leaves, suggesting that it affects ABA signaling or uptake into guard cells via transcriptional regulation of unidentified ABA signaling components or transporter genes. To examine these possibilities, the authors performed RNA-sequencing analysis of isolated guard cells. They have identified ABA-IMPORTING TRANSPORTERs (AITs) as being upregulated by PRO. Tomato has four AIT1 genes, but only AIT1.1 and AIT1.2 were upregulated by PRO, and only AIT1.1 exhibited high expression in guard cells. The functional analysis of AIT1.1 in yeast (Saccharomyces cerevisiae) confirmed its activity as an ABA transporter. An ait1.1 mutant exhibited increased transpiration, larger stomatal apertures, and a reduced stomatal response to ABA. Moreover, ait1.1 suppressed the promoting effects of PRO on ABA-induced stomatal closure and gene expression in guard cells, suggesting that the effects of PRO on stomatal aperture and transpiration are AIT1.1-dependent. Although many previous studies have revealed negative crosstalk between gibberellin and ABA that is mediated by changes in hormone biosynthesis and signaling, the results of this study suggest that this crosstalk can also be mediated by changes in hormone transport. Villin and GLABRA2 Regulate Root Hair Growth The enhanced elongation of root hairs in response to mild water deficiency permits more effective water and nutrition uptake. The growth of root hairs is regulated in part by actin dynamics. Thick actin-filament bundles in the apical and subapical area of root hairs inhibit root hair growth. Actin-binding proteins, including villins (VLNs), are believed to be major organizers of the thick bundles in root hairs. Additionally, a series of key transcription factors have been identified as key regulatory factors that influence root hair growth. The transcription factor GLABRA2 (GL2) in particular plays an important role in the initiation and growth of root hairs in Arabidopsis (Arabidopsis thaliana). Several gl2 mutants, for example, have significantly longer root hairs than the wild type. GL2 directly suppresses the function of positive hair growth regulators, including several transcription factors, thus negatively regulating root hair cell growth. Wang et al. (pp. 165–175) now show that vln1 mutants display significantly longer hairs, with longer hair growing time and defects in the thick actin bundles and bundling activities in the subapical and apical regions. The authors show that VLN1 overexpression suppresses the gl2 mutant phenotypes with regard to hair growth and actin dynamics. Moreover, GL2 directly recognizes the promoter of VLN1 and positively regulates VLN1 expression in root hairs. The GL2-mediated VLN1 pathway is also shown to be involved in the root hair growth response to osmotic stress. These results demonstrate that the GL2-mediated VLN1 pathway plays an important role in the root hair growth response to osmotic stress and suggest a transcriptional mechanism that regulates actin dynamics and hence cell tip growth in response to environmental signals. Biosynthesis of Montbretin, an Antidiabetes Drug Diabetes and obesity are major health challenges. Diabetes alone affects over 422 million people worldwide and is among the top ten leading causes of death. Type-2 diabetes is characterized by the body’s inefficient use of insulin, which leads to elevated blood Glc levels with detrimental effects on different organs and increased risk of dying prematurely. The plant metabolite montbretin A (MbA) is being developed as an antidiabetes and antiobesity treatment due to its potent and specific inhibition of the human pancreatic α-amylase. MbA is a complex acylated flavonol glycoside formed in small amounts in the corms of montbretia (Crocosmia × crocosmiiflora), a member of the iris family, during the early summer. Unfortunately, the spatial and temporal patterns of MbA accumulation limit its supply for drug development and application. Irmisch et al. (pp. 97–109) are exploring MbA biosynthesis with the aim of enabling metabolic engineering of this rare and valuable compound. Genes and enzymes for the first four steps of MbA biosynthesis, starting from the flavonol precursor myricetin, have recently been identified. Now, the authors describe the gene discovery and functional characterization of the remaining two enzymes of MbA biosynthesis. The authors reveal that two UDP-glycosyltransferases, CcUGT4 and CcUGT5, catalyze consecutive reactions in the formation of the disaccharide moiety at the 4′-hydroxy position of the MbA flavonol core. Both enzymes are specific for flavonol glycosides and their respective sugar donors. This study completes the discovery of the MbA biosynthetic pathway and provides the complete set of genes to engineer MbA biosynthesis. Indeed, the authors announce their successful reconstruction of MbA biosynthesis in Nicotiana benthamiana. The Regulation of Cuticle Biosynthesis The outer surface of the aerial parts of land plants is covered by the cuticle, a waxy layer that provides a barrier against damage caused by environmental factors, as well as protection against nonstomatal water loss. Castorina et al. (pp. 266–282) now show that both cuticle deposition and cuticle-dependent leaf permeability during the juvenile phase of plant development are controlled in maize (Zea mays) by the transcription factor ZmFUSED LEAVES-1 (FDL1). Lack of ZmFDL1 activity in the fused leaves1-1 (fdl1-1) mutant specifically affects seedling development at early developmental stages and results in organ fusions due to the lack of cuticular material in the boundary between organs and irregular distribution of wax crystals on young leaf epidermal surfaces. To gain further insight into the role of ZmFDL1, the authors compared the cuticle composition of mutant and wild-type seedlings and analyzed the impact of the mutation on the transcriptome during early phases of seedling development. They also investigated ZmFDL1 involvement in controlling cuticular permeability and in mediating the drought stress response in maize seedlings. Their biochemical analyses reveal that among cutin compounds, ω-hydroxy fatty acids and polyhydroxy-fatty acids were specifically affected, while the reduction of epicuticular waxes was mainly observed in primary long chain alcohols and, to a minor extent, in long-chain wax esters. Transcriptome analysis allowed the identification of candidate genes involved in lipid metabolism and a hypothetical construct of a proposed pathway for cuticle biosynthesis in maize. Lack of ZmFDL1 affects the expression of genes located in different modules of the pathway. Overall, their results indicate that the response to water stress involves activation of wax biosynthesis and involvement of both ZmFDL1 and ABA regulatory pathways. The functional characterization of the ZmFDL1 regulatory gene presented here sheds light on the molecular mechanisms underlying cuticle-mediated drought stress tolerance in maize. Sphingolipids and Plasmodesmata Plasmodesmata are cytoplasmic channels that physically connect the cytoplasm and endoplasmic reticulum of adjoining plant cells. These intercellular channels play important roles during plant development by allowing the molecular exchange of signaling molecules such as transcription factors, RNAs, and growth regulators. Interestingly, the plasma membrane (PM) of plasmodesmata is distinct from the general cellular PM and is enriched in sterol and sphingolipid (SL) species. The domains enriched with these special lipids are referred to as lipid rafts. Perturbation of sterol biosynthesis affects plasmodesmatal connectivity by changing the subcellular localization of two glycosylphosphatidylinositol (GPI)-anchored plasmodesmata proteins, namely plasmodesmata callose binding-1 (PDCB1) and plasmodesmata-associated β-1,3-glucanase-2 (PdBG2); this, in turn, results in the accumulation of plasmodesmata-associated callose, with the consequence that the exclusion limit of plasmodesmata is lowered. Iswanto et al. (pp. 407–420) now turn their attention to the other class of lipids enriched in the PMs of plasmodesmata, the SLs. By way of SL pathway inhibitors and two distinct SL pathway mutants, the authors report that they were able to modulate callose deposition to control symplasmic connectivity through perturbations of SL metabolism. The alteration of glucosylhydroxyceramide levels in particular disturbed the secretory machinery for the GPI-anchored PdBG2 protein, resulting in an overaccumulation of callose. In summary, this study reveals that changes in the composition of SL species and related compounds are important for the regulation of plasmodesmatal transport via their effects on PdBG2 and callose. A Molecular Determinant of Rice Plant Architecture Plant architecture is a major determinant of rice (Oryza sativa) productivity. Rice plant architecture is mainly defined by plant height, the spatial pattern of leaves, and tiller and inflorescence branching patterns. Plant height and tiller branching determine the biomass and harvest index, while the spatial pattern of leaves, including leaf shape and angle, influences the photosynthesis rate and therefore the accumulation of carbohydrates. GROWTH-REGULATING FACTORs (GRFs), proteins specific to plants, participate in reproductive and vegetative development, senescence. and stress tolerance. In rice, there are 12 GRFs, but the role of the miR396-OsGRF7 regulatory module remains unknown. Chen et al. (pp. 393–406) now report that OsGRF7 shapes rice plant architecture via the regulation of auxin and GA metabolism. OsGRF7 is mainly expressed in lamina joints, nodes, internodes, axillary buds, and young inflorescences. The overexpression of OsGRF7 causes a semidwarf and compact plant architecture with an increased culm wall thickness and narrowed leaf angles mediated by shortened cell length, altered cell arrangement, and increased parenchymal cell layers in the culm and adaxial side of the lamina joints. Knockout and knockdown lines of OsGRF7 exhibit contrasting phenotypes with severe degradation of parenchymal cells in the culm and lamina joints at maturity. Further analysis indicated that OsGRF7 binds a specific motif in the promoters of a cytochrome P450 gene and AUXIN RESPONSE FACTOR12, which are involved in the GA synthesis and auxin signaling pathways, respectively. Correspondingly, OsGRF7 alters the contents of endogenous GAs and auxins and sensitivity to exogenous phytohormones. This study demonstrates that OsGRF7 is a key regulator of the shaping of plant architecture through its effects on GA and auxin signaling networks. Author notes www.plantphysiol.org/cgi/doi/10.1104/pp.20.01131 © 2020 American Society of Plant Biologists. All Rights Reserved. © The Author(s) 2020. Published by Oxford University Press on behalf of American Society of Plant Biologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

Minorsky, Peter V.

doi: 10.1104/pp.20.01131pmid: 33814632

Blatt, Mike; Williams, Mary

doi: 10.1104/pp.20.01067pmid: 33814633

This past January, Plant Physiology welcomed 24 new Assistant Features Editors to the editorial board. Together with Assistant Features Editors recruited in 2018, these young scientists have brought their passion for science to the journal, communicating to our readers some of the most exciting developments at the forefront of global research in plants today. The Assistant Features Editors have helped shape and expand our content through commentaries, blog posts, and related material highlighting the “here and now” of Plant Physiology and bringing awareness of matters of special interest to the community. They have gained professionally, too, and will build on their experience going forward, just as, for us, working with the Assistant Features Editors has proven immensely satisfying. We are now recruiting a new cohort of Assistant Features Editors to join the Plant Physiology editorial board, replacing some of the current members who will step down from their roles with the journal. This new cohort will work with the journal for 24 months beginning in January 2021. If you are interested in becoming an Assistant Features Editor, we are welcoming applications through Monday, October 5, 2020. Further details of the activities of the Assistant Features Editors and how to apply are available online at https://plantae.org/plant-physiology-is-recruiting-assistant-features-editors-for-2021/. We are interested in hearing about your current position and future goals and why you are interested in the position. We will need your Curriculum Vitae and the contact details of two individuals familiar with your work as a researcher. We will also expect two samples of your writing, one a first authored paper, and the other a sample News & Views commentary you write on your selection of one of the Plant Physiology articles listed online. We hope to have selected the new Assistant Features Editors late in November. Author notes www.plantphysiol.org/cgi/doi/10.1104/pp.20.01067 © 2020 American Society of Plant Biologists. All Rights Reserved. © The Author(s) 2020. Published by Oxford University Press on behalf of American Society of Plant Biologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

Blatt, Mike; Williams, Mary

doi: 10.1104/pp.20.01067pmid: 33814633

Gelderen, Kasper van

doi: 10.1104/pp.20.01013pmid: 33890089

van Gelderen, Kasper

doi: 10.1104/pp.20.01013pmid: 32900970

The study of plant movement toward light, also called phototropism, has a venerable history, with giants such as Charles Darwin and Frits Went involved in its study, which led to the discovery of the plant hormone auxin (Went, 1928). We now have a deep understanding of its mechanistic underpinnings (Christie and Murphy, 2013). Therefore, it is all the more surprising that fundamentals of phototropic responses can still be uncovered. Among these discoveries, Ballaré et al. (1992) observed that phototropism is enhanced when plants are growing within a canopy. Plants sense the crowding under a canopy by a lowering of the ratio of far-red (FR) to red (R) light (low R:FR; LRFR). This effect arises from the enhanced reflection of FR light from neighboring leaves. The surrounding leaves also filter and reduce the available blue light (low blue light; LBL). LRFR and LBL promote the stem elongation of plants, and this competitive response is seen as an adaptive change to accelerate plant growth out of the canopy and reach sunlight, the main resource of plant life. So, which of these light cues is important and which photoreceptors are involved? In the previous issue of Plant Physiology, Boccaccini et al. (2020) showed that in Arabidopsis (Arabidopsis thaliana), a combination of LBL and LRFR promotes phototropism and that LBL alone is sufficient. In addition, they demonstrate that the blue light receptor cryptochrome 1 (cry1) is active in this response. Previous work had shown that LRFR can promote phototropism in artificial lighting conditions (Goyal et al., 2016), where etiolated seedlings are exposed to a unidirectional source of blue light. However, with a more natural lighting regime, Boccaccini et al. (2020) found that LRFR was not sufficient. Only a combination of LBL and LRFR resulted in increased phototropism toward a blue light source within the white growth light (WL; Fig. 1A). A pretreatment of LBL combined with LBL during the phototropic response led to the same result as the combined LBL and LRFR treatment. Thus, the authors proceeded to further investigate this LBL-mediated mechanism by comparing the LBL condition with an LBL pretreatment (LBL/LBL) and without (WL/LBL; Fig. 1B). Figure 1. Open in new tabDownload slide LBL enhances phototropism by releasing cry1-mediated inhibition of PIF4 expression. A, Seedlings growing in WL do not show a strong phototropic response to unidirectional blue light (BL). However, they do bend toward blue light when the light environment is changed by filter to achieve LBL and the addition of extra FR lighting to get LRFR. B, The same effect can also be achieved by LBL alone, when an LBL pretreatment is applied. C, cry1 shows a phototropic response without LBL pretreatment, and this effect is dependent upon pif4 pif5 pif7. wt, Wild type. Figure based on figures 1 and 4 from Boccaccini et al., (2020). Figure 1. Open in new tabDownload slide LBL enhances phototropism by releasing cry1-mediated inhibition of PIF4 expression. A, Seedlings growing in WL do not show a strong phototropic response to unidirectional blue light (BL). However, they do bend toward blue light when the light environment is changed by filter to achieve LBL and the addition of extra FR lighting to get LRFR. B, The same effect can also be achieved by LBL alone, when an LBL pretreatment is applied. C, cry1 shows a phototropic response without LBL pretreatment, and this effect is dependent upon pif4 pif5 pif7. wt, Wild type. Figure based on figures 1 and 4 from Boccaccini et al., (2020). The main photoreceptors regulating phototropism are the phototropins (phot), and in a phot1 phot2 double knockout no phototropism is observed. However, plants have another set of blue light photoreceptors, the cryptochromes. Boccaccini et al. (2020) discovered that the cry1 mutant has an increased phototropism response in WL/LBL, without a further increase in bending in the LBL/LBL condition, compared with the wild type, which only had a strong response with the LBL pretreatment (LBL/LBL; Fig. 1C). This result indicates that cry1 normally inhibits the phototropism response in an LBL environment. However, an increase in blue light from one side can deactivate cry1 and therefore allow phototropism to occur. The most important downstream actors of the cry and phytochrome photoreceptors are the PHYTOCHROME INTERACTING FACTORS (PIFs). The triple mutant pif4 pif5 pif7 is lacking in phototropic bending. This pif4 pif5 pif7 mutant, when crossed with cry1, still does not have the phototropic response, showing that these PIFs are necessary for cry1 to inhibit phototropism (Fig. 1C). During a typical day, PIF4 and PIF5 levels gradually decrease; however, the authors found that the LBL/LBL treatment causes PIF levels to remain higher for longer. This accumulation of PIF4 depends upon a functional cry1. Overexpressing lines of PIF4 and PIF5 had enhanced phototropism responses, showing that increases in PIF4/5 levels are connected to phototropism. In conclusion, the authors convincingly show that cry1 inhibits PIF4/5 and that the unidirectional blue light allows a buildup of PIFs. Of course, one asks: how does a buildup of PIFs lead to a directional response? From previous research, we know that PIFs activate auxin biosynthesis and transport during phototropism (Goyal et al., 2016). Therefore, the authors also show that in their setup an auxin gradient builds up away from the blue light source and that this is dependent upon the PIN-FORMED auxin efflux carriers PIN3, PIN4, and PIN7, which, during phototropism, pump auxin out from the vasculature tissue, toward the cortex and epidermis (Ding et al., 2011). In short, this article bridges a long-standing gap between traditional phototropism studies that often use highly artificial lighting regimes and etiolated seedlings exposed to unidirectional monochromatic light. Boccaccini et al. (2020) combine these studies with work using green seedlings and growth under regimes with blue light enrichment (Fig. 1A), and they relate these studies to the real world in which a growing plant often experiences canopy shading. In the latter case, the authors even grow Arabidopsis in a field, next to a grass covering, to show that both cry1 and cry1 pif457 mutants behave the same as in the lab. Altogether, the findings in this article neatly show how plants use competition and shading cues to grow toward the sun and enhance their future success. LITERATURE CITED Ballaré CL , Scopel AL, Radosevich SR, Kendrick RE( 1992 ) Phytochrome-mediated phototropism in de-etiolated seedlings: Occurrence and ecological significance . Plant Physiol 100 : 170 – 177 Google Scholar Crossref Search ADS PubMed WorldCat Boccaccini A , Legris M, Krahmer J, Allenbach Petrolati L, Goyal A, Ampudia CG, Vernoux T, Karayekov E, Casal JJ, Fankhauser C( 2020 ) Low blue light enhances phototropism by releasing cryptochrome 1-mediated inhibition of PIF4 expression . Plant Physiol 183 : 1780 – 1793 Google Scholar Crossref Search ADS PubMed WorldCat Christie JM , Murphy AS( 2013 ) Shoot phototropism in higher plants: New light through old concepts . Am J Bot 100 : 35 – 46 Google Scholar Crossref Search ADS PubMed WorldCat Ding Z , Galván-Ampudia CS, Demarsy E, Łangowski Ł, Kleine-Vehn J, Fan Y, Morita MT, Tasaka M, Fankhauser C, Offringa R , et al. ( 2011 ) Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis . Nat Cell Biol 13 : 447 – 452 Google Scholar Crossref Search ADS PubMed WorldCat Goyal A , Karayekov E, Galvão VCC, Ren H, Casal JJJ, Fankhauser C( 2016 ) Shade promotes phototropism through phytochrome B-controlled auxin production . Curr Biol 26 : 3280 – 3287 Google Scholar Crossref Search ADS PubMed WorldCat Went FW ( 1928 ) Wuchsstoff und Wachstum . Recl Trav Bot Neerl 25 : 1 – 116 Google Scholar OpenURL Placeholder Text WorldCat Author notes 1 Author for contact: [email protected]. 2 Senior author. www.plantphysiol.org/cgi/doi/10.1104/pp.20.01013 © 2020 American Society of Plant Biologists. All Rights Reserved. © The Author(s) 2020. Published by Oxford University Press on behalf of American Society of Plant Biologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

Gommers, Charlotte

doi: 10.1104/pp.20.00993pmid: 33890102

Gommers, Charlotte

doi: 10.1104/pp.20.00993pmid: 32900971

For a long time, the study of light fueled two independent fields of plant science. On the one hand, light energy is absorbed in the chloroplasts to drive sugar production via photosynthesis. On the other hand, light is an environmental signal that steers plant development. Even though most light-driven growth and development aims to secure light capture for photosynthesis, the bridge between understanding light as a source of energy and light as a signal has hardly ever been made. Until now. Plants gather information about their light environment via a collection of specialized photoreceptors, particularly phytochromes (phys) and cryptochromes (crys). Many of the pathways mediated by these photoreceptors, such as the shade avoidance syndrome to outgrow (future) neighboring plants (Fraser et al., 2016) and phototropism to move leaves toward the light (Goyal et al., 2013), optimize light harvesting. When etiolated seedlings first see the light, photoreceptor activation induces a transition that prepares the seedling for a photoautotrophic life. This transition is referred to as photomorphogenesis: cotyledons separate, etioplasts develop into mature chloroplasts, and the hypocotyl stops elongating (Gommers and Monte, 2018). Upon exposure to light, phys and crys inactivate repressors of photomorphogenesis, among which is the E3 ubiquitin ligase CONSTITUTIVELY PHOTOMORPHOGENIC1 (COP1). The inactivation of COP1 releases an important promotor of photomorphogenesis, the bZIP transcription factor ELONGATED HYPOCOTYL5 (HY5). HY5 is named for its role in repressing hypocotyl elongation but turns out to be one of the major regulators of many light-driven processes above- and belowground. In addition to its role in photomorphogenesis, HY5 promotes the transcription of nuclear genes with a role in photosynthesis, such as those encoding enzymes involved in the biosynthesis of chlorophyll and carotenoids (Toledo-Ortiz et al., 2014). An indirect role for HY5 in photoprotection was described previously, when it was shown to be responsible for the transcription of enzymes of the anthocyanin biosynthesis pathway (Richter et al., 2020). These red pigments protect plants against high light by absorbing excess photons. Recently in Plant Physiology, Li et al. (2020) built another strong connection between the HY5-mediated light signaling pathway and photosynthesis. They show that among the direct targets of HY5 is HIGH CHLOROPHYLL FLUORESCENCE173 (HCF173), encoding a chloroplast-localized protein involved in the translation of the chloroplast gene photosystem II reaction center protein A (psbA). psbA encodes the PSII reaction center protein D1, which is quickly turned over in light and needs to be constantly synthesized to maintain PSII light harvesting. Accordingly, Li et al. (2020) have discovered that the hy5 loss of function mutant reduces PSII activity under white, blue, red, and far-red light. This work by Li et al. (2020) provides a direct link between HY5 activity and the assembly of PSII in the chloroplast, and the authors additionally found that HY5 is important for PSII maintenance, as it transcribes a set of PSII repair genes. As a consequence, hy5 seedlings suffer significantly more from high light-induced photodamage than do the wild-type controls. The direct involvement of HY5 in the assembly and repair of both nuclear and plastid-encoded photosynthesis proteins is novel. It builds a bridge between the photobiologists studying photoreceptor signaling on one side and those studying photosynthesis on the other. Given the wealth of functions already assigned to HY5, most readers will not be surprised that this transcription factor is one of the bridge’s pillars. An outstanding question is whether the role of HY5 in PSII repair is triggered by excess light. Besides the photoreceptor-mediated stabilization of HY5, a photoreceptor-independent pathway exists that might play an important role. Damage done to chloroplasts can trigger the release of retrograde signals from the organelle toward the nucleus (de Souza et al., 2017). Retrograde signals induced by chloroplast-inhibiting chemicals or high light inhibit photomorphogenesis and anthocyanin synthesis with interplay of HY5 (Ruckle and Larkin, 2009; Martín et al., 2016; Richter et al., 2020). If light stress in the chloroplast triggers a regulatory feedback loop toward HY5 in the nucleus, it means that the newly built bridge can be walked both ways: Photoreceptors drive photosynthesis, and chloroplast-derived signals in turn affect the downstream targets of photoreceptors. The photobiology paradox is starting to disappear, but more work is needed to define the key role of HY5 and identify the other pillars. LITERATURE CITED de Souza A , Wang J-Z, Dehesh K( 2017 ) Retrograde signals: Integrators of interorganellar communication and orchestrators of plant development . Annu Rev Plant Biol 68 : 85 – 108 Google Scholar Crossref Search ADS PubMed WorldCat Fraser DP , Hayes S, Franklin KA( 2016 ) Photoreceptor crosstalk in shade avoidance . Curr Opin Plant Biol 33 : 1 – 7 Google Scholar Crossref Search ADS PubMed WorldCat Gommers CMM , Monte E( 2018 ) Seedling establishment: A dimmer switch-regulated process between dark and light signaling . Plant Physiol 176 : 1061 – 1074 Google Scholar Crossref Search ADS PubMed WorldCat Goyal A , Szarzynska B, Fankhauser C( 2013 ) Phototropism: At the crossroads of light-signaling pathways . Trends Plant Sci 18 : 393 – 401 Google Scholar Crossref Search ADS PubMed WorldCat Li X , Wang H-B, Jin H-L ( 2020 ) Light signaling-dependent regulation of PSII biogenesis and functional maintenance . Plant Physiol 184 : 1885 – 1868 Google Scholar OpenURL Placeholder Text 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 Richter AS , Tohge T, Fernie AR, Grimm B( 2020 ) The genomes uncoupled-dependent signalling pathway coordinates plastid biogenesis with the synthesis of anthocyanins . Philos Trans R Soc Lond B Biol Sci 375 : 20190403 Google Scholar Crossref Search ADS PubMed WorldCat Ruckle ME , Larkin RM( 2009 ) Plastid signals that affect photomorphogenesis in Arabidopsis thaliana are dependent on GENOMES UNCOUPLED 1 and cryptochrome 1 . New Phytol 182 : 367 – 379 Google Scholar Crossref Search ADS PubMed WorldCat Toledo-Ortiz G , Johansson H, Lee KP, Bou-Torrent J, Stewart K, Steel G, Rodríguez-Concepción M, Halliday KJ( 2014 ) The HY5-PIF regulatory module coordinates light and temperature control of photosynthetic gene transcription . PLoS Genet 10 : e1004416 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.20.00993 © 2020 American Society of Plant Biologists. All Rights Reserved. © The Author(s) 2020. Published by Oxford University Press on behalf of American Society of Plant Biologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

Roell, Marc-Sven

doi: 10.1104/pp.20.00919pmid: 32900972

Cannabis sativa (cannabis) is the cornerstone of the multibillion-dollar legal marijuana industry. Cannabis plants are industrially used for fiber and oilseed production, but are primarily known for their resin, which is produced from glandular trichomes covering the surface of female flowers and is rich in cannabinoids and terpenes. The medicinal and psychoactive properties of cannabis depend on the total cannabinoid amount and the ratio of tetrahydrocannabinolic acid to cannabidiolic acid. However, fragrance and flavor are affected by terpene composition (Booth et al., 2017). To predict and design cannabis smell and taste to meet consumer demands, two milestones have to be reached. First, a comprehensive understanding of terpene composition is required, which can be achieved by using quantitative terpene profiling in existing cultivars. Second, the underlying molecular and biochemical mechanisms leading to these distinct profiles need to be understood. In this issue of Plant Physiology, Booth et al. (2020) provide the framework for future breeding efforts to produce cannabis fragrance and flavor features demanded by consumers. Specifically, they analyzed terpene profiles of eight cannabis cultivars and characterized 13 new cannabis terpene synthases. In plants, terpenes form a diverse group of hydrocarbon-based metabolites estimated to encompass thousands of different molecules (Pichersky and Raguso, 2018). Terpenes have diverse roles. They function as primary cellular components, e.g. as hormones or antioxidants, and they are indispensable for ecological interactions, e.g. signaling and defense against herbivores (Pichersky and Raguso, 2018). In cannabis, more than 100 different terpenes have been identified that define odor and flavor of different cultivars (Rothschild et al., 2005; Andre et al., 2016). Terpene- and cannabinoid-biosynthesis depend on the five carbon building block isopentenyl pyrophosphate (IPP; Fig. 1). IPP is produced by the plastidial methylerythritol phosphate pathway and the cytosolic mevalonate pathway. Metabolic fluxes within both pathways contribute to the substrate pools available for terpene synthases (TPSs). TPSs produce the diversity of cyclic and acyclic terpene core structures, using geranyl diphosphate or farnesyl diphosphate for monoterpene or sesquiterpene synthesis, respectively (Fig. 1). Figure 1. Open in new tabDownload slide Simplified scheme of terpene biosynthesis. IPP is produced either by the methylerythritol phosphate (MEP) pathway or the mevalonate (MEV) pathway. TPSs catalyze the last step of terpene biosynthesis. G3P, Glyceraldehyde 3-phosphate; CBGA, cannabigerolic acid. Adapted from figure 1 of Booth et al. (2020). Figure 1. Open in new tabDownload slide Simplified scheme of terpene biosynthesis. IPP is produced either by the methylerythritol phosphate (MEP) pathway or the mevalonate (MEV) pathway. TPSs catalyze the last step of terpene biosynthesis. G3P, Glyceraldehyde 3-phosphate; CBGA, cannabigerolic acid. Adapted from figure 1 of Booth et al. (2020). The accurate predicting and design of cannabis terpene profiles requires understanding of TPS, the key enzyme in terpene biosynthesis (Fig. 1). Booth et al. (2020) identified 19 TPS gene models in the ‘Purple Kush’ cannabis reference genome. TPS genes show multicopy gene clustering, a common phenomenon previously observed for genes of the IPP and cannabinoid biosynthetic pathways (Taura et al., 2009). Foliar terpene profiling of eight cannabis cultivars revealed a total of 48 different terpenes with three monoterpenes (myrcene, α‐pinene, and limonene) and two sesquiterpenes (β‐caryophyllene and α‐humulene) present in all cultivars. In six selected cultivars, monoterpenes accumulated during the life cycle, in tissues including leaves, juvenile flowers, and adult flowers. Using trichome transcriptome profiling, Booth et al. (2020) identified 33 TPS genes among the selected six cultivars. Further, 13 new TPSs were biochemically characterized regarding product formation using both geranyl diphosphate and farnesyl diphosphate as substrates. Overall TPS specificity varied between the production of a single mono- or sesquiterpene to as many as 13 different sesquiterpenes produced by a single TPS enzyme. With these results, simple assumptions regarding TPS transcript abundance and terpene profiles can be made. However, spatiotemporal profiling of TPS transcript levels and terpene quantities will be necessary for more accurate predictions. Integrating the 13 TPSs characterized in this study with previously characterized TPS brings the total number to 30 known TPSs across 14 different cannabis cultivars (Booth et al., 2017; Zager et al., 2019; Livingston et al., 2020). 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Plant Physiol 180 : 1877 – 1897 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.20.00919 © 2020 American Society of Plant Biologists. All Rights Reserved. © The Author(s) 2020. Published by Oxford University Press on behalf of American Society of Plant Biologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

Roell, Marc-Sven

doi: 10.1104/pp.20.00919pmid: 33890098