PLANT PHYSIOLOGY

Burgess, Alexandra J; Majda, Mateusz

doi: 10.1093/plphys/kiac190pmid: 35478044

Accepted manuscripts Accepted manuscripts are PDF versions of the author’s final manuscript, as accepted for publication by the journal but prior to copyediting or typesetting. They can be cited using the author(s), article title, journal title, year of online publication, and DOI. They will be replaced by the final typeset articles, which may therefore contain changes. The DOI will remain the same throughout. Article PDF first page preview Close This content is only available as a PDF. © The Author(s) 2022. 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.

Ahmed, Sulaiman; Chen, Jian

doi: 10.1093/plphys/kiac185pmid: 35460247

Accepted manuscripts Accepted manuscripts are PDF versions of the author’s final manuscript, as accepted for publication by the journal but prior to copyediting or typesetting. They can be cited using the author(s), article title, journal title, year of online publication, and DOI. They will be replaced by the final typeset articles, which may therefore contain changes. The DOI will remain the same throughout. Article PDF first page preview Close This content is only available as a PDF. Author notes Jian Chen. Senior author © The Author(s) 2022. Published by Oxford University Press on behalf of American Society of Plant Biologists. All rights reserved. For permissions, please email: [email protected] 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)

Ugalde, José Manuel

doi: 10.1093/plphys/kiac191pmid: 35478035

Accepted manuscripts Accepted manuscripts are PDF versions of the author’s final manuscript, as accepted for publication by the journal but prior to copyediting or typesetting. They can be cited using the author(s), article title, journal title, year of online publication, and DOI. They will be replaced by the final typeset articles, which may therefore contain changes. The DOI will remain the same throughout. Article PDF first page preview Close This content is only available as a PDF. © The Author(s) 2022. 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.

Mishra, Divya

doi: 10.1093/plphys/kiac183pmid: 35471662

Accepted manuscripts Accepted manuscripts are PDF versions of the author’s final manuscript, as accepted for publication by the journal but prior to copyediting or typesetting. They can be cited using the author(s), article title, journal title, year of online publication, and DOI. They will be replaced by the final typeset articles, which may therefore contain changes. The DOI will remain the same throughout. Article PDF first page preview Close This content is only available as a PDF. © The Author(s) 2022. Published by Oxford University Press on behalf of American Society of Plant Biologists. All rights reserved. For permissions, please email: [email protected] 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)

Kazachkova, Yana

doi: 10.1093/plphys/kiac186pmid: 35460251

Accepted manuscripts Accepted manuscripts are PDF versions of the author’s final manuscript, as accepted for publication by the journal but prior to copyediting or typesetting. They can be cited using the author(s), article title, journal title, year of online publication, and DOI. They will be replaced by the final typeset articles, which may therefore contain changes. The DOI will remain the same throughout. Article PDF first page preview Close This content is only available as a PDF. © The Author(s) 2022. 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.

Oses-Ruiz, Miriam

doi: 10.1093/plphys/kiac140pmid: 35325231

Article PDF first page preview Close This content is only available as a PDF. © The Author(s) 2022. 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.

Zhou, Lijuan; Ye, Yajin

doi: 10.1093/plphys/kiac168pmid: 35417022

Accepted manuscripts Accepted manuscripts are PDF versions of the author’s final manuscript, as accepted for publication by the journal but prior to copyediting or typesetting. They can be cited using the author(s), article title, journal title, year of online publication, and DOI. They will be replaced by the final typeset articles, which may therefore contain changes. The DOI will remain the same throughout. Article PDF first page preview Close This content is only available as a PDF. © The Author(s) 2022. 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.

Ponnu, Jathish

doi: 10.1093/plphys/kiac139pmid: 35325226

Timely germination ensures proper seedling establishment and therefore has vital importance in the dispersal, adaptation, and survival of plant species. After ripening, seeds enter into dormancy, a physiological state that suppresses germination, caused partly by the interplay of internal hormone signaling with external factors such as light, temperature, and the availability of moisture. Under favorable environmental conditions, the spatio-temporal dynamics of the antagonistic plant hormones gibberellins (GA) and abscisic acid (ABA) determine the timing of dormancy-breaking and seed germination. While a high GA-to-ABA ratio favors germination of imbibed seeds, a low ratio promotes dormancy (Carrera-Castaño et al., 2020). In line with the major role of GA in seed germination, Arabidopsis (Arabidopsis thaliana) mutants with impaired GA-biosynthesis fail to germinate without exogenous GA (Holdsworth et al., 2008). Central to GA signaling is the DELLA domain-containing transcriptional regulators (DELLAs) that repress GA-responsive genes. The GA-receptor GA INSENSITIVE DWARF1 (GID1) perceives bioactive GA and undergoes conformational changes that enable the interaction between GID1 and DELLAs. The F-box proteins SLEEPY1 and SNEEZY, as components of the Skp1–Cul1–F-box-protein (SCF) ubiquitin ligase, target the GA-GID1-DELLA complex for ubiquitin-mediated proteolysis, thereby alleviating the repression of GA-responsive genes and initiating the GA signaling cascade (Bao et al., 2020). Among the five Arabidopsis DELLA proteins (GA INSENSITIVE [GAI], REPRESSOR OF ga1-3 [RGA], RGA-LIKE 1 [RGL1], RGL2, and RGL3), RGL2 functions as the major repressor of GA-mediated seed germination (Carrera-Castaño et al., 2020). Recent work demonstrates that the DELLA proteins GAI and RGA can also be degraded (Blanco-Touriñán et al., 2020) via the CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1)/SUPPRESSOR OF PHYA-105 (SPA) complex, an evolutionarily conserved E3 ligase that acts as a master regulator of photomorphogenesis (Ponnu and Hoecker, 2021). The COP1/SPA complex directly interacts with and facilitates the degradation of GAI and RGA to regulate plant growth under warm temperature and shade conditions (Blanco-Touriñán et al., 2020). In this issue of Plant Physiology, Lee and co-workers (Lee et al., 2022) show that the COP1/SPA complex promotes seed germination by targeting yet another DELLA protein, RGL2, for ubiquitination and subsequent degradation. The authors observed that exogenous GA restored the slight but significant delay in the germination of cop1-4 (a weak cop1 allele), suggesting a positive role of COP1 in seed germination. However, the presence of the GA-biosynthesis inhibitor paclobutrazol (PAC) impaired the germination of cop1-4 more severely than the wild-type Col-0, implying an enhanced effect of COP1 under GA-deficient conditions. In contrast, the Arabidopsis rgl2 mutant showed PAC insensitivity and the rgl2 mutation completely rescued the PAC-hypersensitive phenotype of cop1-4, indicating the epistatic effect of RGL2 over COP1. Furthermore, the authors showed that RGL2 and COP1 physically interact (Lee et al., 2022). Similar to COP1-RGA/GAI interactions (Blanco-Touriñán et al., 2020), the presence of SPA1 as a bridge protein is essential for the in vivo association of COP1 with RGL2 (Lee et al., 2022), reinforcing the important role of SPA proteins (Hoecker, 2017) in the COP1/SPA E3 ligase complex. Consistent with the idea that COP1 destabilizes RGL2, the recombinant MBP-RGL2 degraded faster when incubated with soluble protein extracts of a COP1-overexpressing line, but slower with extracts of cop1-4 mutant, compared to Col-0 in a cell-free degradation assay. In addition, COP1 could directly ubiquitinate RGL2 in vitro, confirming RGL2 as a direct target of COP1. Furthermore, germination-promoting genes suppressed by RGL2, such as GA-STIMULATED ARABIDOPSIS 6, expansins, and xyloglucan endotransglucosylases/endohydrolases, were downregulated in the cop1-4 mutant. Collectively, Lee and co-workers (Lee et al., 2022) demonstrate that Arabidopsis COP1 destabilizes the downstream ubiquitination target RGL2 and thereby relieves the expression of germination-promoting genes (Figure 1). Whether COP1 targets the other RGLs (RGL1 and RGL3) is presently unknown. Figure 1 Open in new tabDownload slide COP1 destabilizes RGL2 to promote seed germination. The arrows and dashed arrows denote direct and indirect effects, respectively. The lines with blunt ends show negative regulation. The question mark (?) represents unknown mechanisms. Modified from Lee et al. (2022). Figure 1 Open in new tabDownload slide COP1 destabilizes RGL2 to promote seed germination. The arrows and dashed arrows denote direct and indirect effects, respectively. The lines with blunt ends show negative regulation. The question mark (?) represents unknown mechanisms. Modified from Lee et al. (2022). The components that regulate seed germination via determining the spatiotemporal balance of GA and ABA are often interconnected. For example, PHYTOCHROME INTERACTING FACTOR 1 (PIF1), which enhances COP1 activity during photomorphogenesis, negatively regulates seed germination by promoting the expression of DELLA proteins. Similarly, ELONGATED HYPOCOTYL 5 (HY5), an important target of COP1, may suppress seed germination by promoting ABA signaling (Carrera-Castaño et al., 2020). However, germination assays using the respective mutants suggested a PIF1- and HY5-independent role of COP1 in GA-mediated seed germination (Lee et al., 2022). Also, the purple coloration phenotype (fusca) observed in many light signaling mutants, including cop1-4, cannot generally be associated with GA-related germination defects (Lee et al., 2022). The effect of COP1 on GA and ABA signaling seems to be antagonistic in seeds, but not in seedlings. COP1 enhances GA-mediated seed germination via destabilizing RGL2 (Lee et al., 2022), but suppresses post-germination seedling establishment by participating in the ABA signaling pathway (Yadukrishnan et al., 2020). Reciprocally, both GA and ABA may influence COP1 activity. In line with this, GA application enhanced COP1 protein accumulation in the imbibed seeds via unknown mechanisms (Lee et al., 2022; Figure 1). Similarly, a recent preprint reported the ABA-induced translocation of COP1 into the cytoplasm in seeds (Chen et al., 2021). However, the ABA-induced nucleo-cytoplasmic repartitioning of COP1 negatively regulates ABA-mediated seed germination inhibition. Hence, COP1 may promote seed germination via enhancing downstream signaling of GA and repressing the activities of ABA. Elucidation of the complex interplay between COP1 and the two antagonistic plant hormones GA and ABA requires further research. References Bao S , Hua C, Shen L, Yu H ( 2020 ) New insights into gibberellin signaling in regulating flowering in Arabidopsis . J Integr Plant Biol 62 : 118 – 131 Google Scholar Crossref Search ADS PubMed WorldCat Blanco-Touriñán N , Legris M, Minguet EG, Costigliolo-Rojas C, Nohales MA, Iniesto E, García-León M, Pacín M, Heucken N, Blomeier T, et al. ( 2020 ) COP1 destabilizes DELLA proteins in Arabidopsis . Proc Natl Acad Sci USA 117 : 13792 – 13799 Google Scholar Crossref Search ADS PubMed WorldCat Carrera-Castaño G , Calleja-Cabrera J, Pernas M, Gómez L, Oñate-Sánchez L ( 2020 ) An updated overview on the regulation of seed germination . Plants (Basel) 9 : 703 Google Scholar Crossref Search ADS WorldCat Chen Q-B , Wang W-J, Zhang Y, Zhan Q-D, Liu K, Botella JR, Bai L, Song C-P ( 2022 ) Abscisic acid-induced cytoplasmic translocation of constitutive photomorphogenic 1 enhances reactive oxygen species accumulation through the HY5-ABI5 pathway to modulate seed germination . Plant Cell Environ doi: 10.1111/pce.14298 Google Scholar OpenURL Placeholder Text WorldCat Crossref Hoecker U ( 2017 ) The activities of the E3 ubiquitin ligase COP1/SPA, a key repressor in light signaling . Curr Opin Plant Biol 37 : 63 – 69 Google Scholar Crossref Search ADS PubMed WorldCat Holdsworth MJ , Bentsink L, Soppe WJJ ( 2008 ) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination . New Phytol 179 : 33 – 54 Google Scholar Crossref Search ADS PubMed WorldCat Lee B-D , Yim Y, Cañibano E, Kim S-H, García-León M, Rubio V, Fonseca S, Paek N-C ( 2022 ) CONSTITUTIVE PHOTOMORPHOGENIC 1 promotes seed germination by destabilizing RGA-LIKE 2 in Arabidopsis . Plant Physiol https://doi.org/10.1093/plphys/kiac060 Google Scholar OpenURL Placeholder Text WorldCat Ponnu J , Hoecker U ( 2021 ) Illuminating the COP1/SPA ubiquitin ligase: fresh insights into its structure and functions during plant photomorphogenesis . Front Plant Sci 12 : 486 Google Scholar Crossref Search ADS WorldCat Yadukrishnan P , Rahul PV, Ravindran N, Bursch K, Johansson H, Datta S ( 2020 ) CONSTITUTIVELY PHOTOMORPHOGENIC1 promotes ABA-mediated inhibition of post-germination seedling establishment . Plant J 103 : 481 – 496 Google Scholar Crossref Search ADS PubMed WorldCat © American Society of Plant Biologists 2022. All rights reserved. For permissions, please email: [email protected] 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)

Mason, Grace Alex

doi: 10.1093/plphys/kiac182pmid: 35485196

Accepted manuscripts Accepted manuscripts are PDF versions of the author’s final manuscript, as accepted for publication by the journal but prior to copyediting or typesetting. They can be cited using the author(s), article title, journal title, year of online publication, and DOI. They will be replaced by the final typeset articles, which may therefore contain changes. The DOI will remain the same throughout. Article PDF first page preview Close This content is only available as a PDF. © The Author(s) 2022. Published by Oxford University Press on behalf of American Society of Plant Biologists. All rights reserved. For permissions, please email: [email protected] 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)

Dubois, Marieke

doi: 10.1093/plphys/kiac187pmid: 35511161

Rice (Oryza sativa) is an important cereal crop that provides up to 60% of the calories taken up by half of the population worldwide (Slewinski, 2012). To feed the growing population, it is crucial for biologists and plant breeders to understand the mechanisms that control rice yield, which is not only determined by the number of grains per panicle, but also by the biomass of each grain. Grain biomass increases during reproductive development by importing sugars into the seeds, a process called grain filling. Plants accumulate sugars in photosynthetic organs during vegetative growth and store them as nonstructural carbohydrates (NSC), of which starch is the best-known example. Long-term NSC storage occurs in the stem of most grass species, including rice, maize (Zea mays), sugarcane (Saccharum Officinarum), and sorghum (Sorghum bicolor; Slewinski, 2012). In some rice varieties, NSC are also stored in the sheath, the lower region of the leaf enrobing the stem (Okamura et al., 2018). NSC are converted to soluble sugars and transported to the energy-demanding developing seeds during grain filling (Figure 1). Despite the importance of NSC remobilization during grain filling in rice, the molecular regulators that control sheath-to-panicle sugar transport are still largely unknown. Figure 1 Open in new tabDownload slide Schematic representation of the role of SnRK1 in carbohydrate remobilization in Nipponbare rice sheaths. During vegetative growth and up to 10 days following anthesis, leaves and sheaths accumulate carbohydrates via photosynthesis. Excess carbon is stored as large starch granules in rice sheaths. During grain filling, nonstructural carbohydrates from the sheaths are remobilized to the panicles in a SnRK1-dependent manner. SnRK1a gene expression is induced, SnRK1a proteins accumulate, and their catalytic domain is phosphorylated for activation. Levels of the SnRK1-inhibiting compound T6P decrease. Finally, the main sucrose transporter in sheaths, Oryza sativa SUCROSE TRANSPORTER1 (OsSUT1), is transcriptionally activated. S, starch; C, chloroplast; G, glucose; SUC, sucrose. Arrows on the plants represent the carbon flow. Figure 1 Open in new tabDownload slide Schematic representation of the role of SnRK1 in carbohydrate remobilization in Nipponbare rice sheaths. During vegetative growth and up to 10 days following anthesis, leaves and sheaths accumulate carbohydrates via photosynthesis. Excess carbon is stored as large starch granules in rice sheaths. During grain filling, nonstructural carbohydrates from the sheaths are remobilized to the panicles in a SnRK1-dependent manner. SnRK1a gene expression is induced, SnRK1a proteins accumulate, and their catalytic domain is phosphorylated for activation. Levels of the SnRK1-inhibiting compound T6P decrease. Finally, the main sucrose transporter in sheaths, Oryza sativa SUCROSE TRANSPORTER1 (OsSUT1), is transcriptionally activated. S, starch; C, chloroplast; G, glucose; SUC, sucrose. Arrows on the plants represent the carbon flow. In the current issue of Plant Physiology, Hu et al. (2022) present a study on NSC remobilization during grain filling in Nipponbare, a rice cultivar with a sequenced genome. Using a detailed time-course analysis to measure multiple physiological and biochemical parameters during the period following anthesis, Hu et al. found that the sheath is a major source of NSC for grain filling. During vegetative development, sheaths accumulated large amounts of sugars, stored as massive starch granules in the chloroplasts (Figure 1). Peak starch accumulation in sheaths and sheath biomass was detected approximately 10 days after anthesis, after which the sheaths become a carbon source tissue and redistribute NSC to sugar-demanding organs. Interestingly, in Nipponbare, the decrease of biomass and starch content in sheaths was more pronounced than in stems, suggesting an important role for sheaths in sugar remobilization during grain filling. To study NSC sheath-to-grain transport, the authors developed an assay that artificially induces NSC remobilization. Cutting the plant’s leaves triggered a rapid activation of starch-degrading amylases and the Oryza sativaSUCROSE TRANSPORTER1, which is one of the main transporters in sheaths and actively pumps sucrose into the phloem (Chen and Wang, 2008; Scofield et al., 2009). Consequently, starch content in sheaths decreased rapidly upon leaf cutting, validating that the leaf-cutting assay can induce the physiological processes mimicking those occurring during grain filling. In Arabidopsis (Arabidopsis thaliana), one of the most important kinases regulating sugar availability and distribution between organs/tissues is Sucrose nonfermenting1-RELATED PROTEIN KINASE1 (SnRK1). SnRK1 fine-tunes sucrose availability by activating a transcription factor that induces expression of amylases and by regulating key enzymes in sucrose synthesis. In rice, two subfamilies of SnRK1, SnRK1a, and SnRK1b, have been identified. Hu et al. found that the expression and protein abundance of SnRK1a increases in sheaths when sheaths transition from sugar sinks to sugar sources (Figure 1). Similar changes in SnRK1a were also observed with the leaf-cutting assay. Subsequently, the authors investigated possible factors regulating SnRK1 activity during grain filling. On the one hand, the SnRK1 catalytic subunit requires phosphorylation to be active, and leaf cutting increased SnRK1 phosphorylation. On the other hand, high levels of trehalose-6-phosphate (T6P) can reduce SnRK1 activity. During grain filling or following leaf cutting, levels of T6P decreased in the sheaths. Altogether, the biochemical data support a model in which SnRK1 abundance and activity are increased during grain filling in rice (Figure 1). To validate that SnRK1 participates in NSC remobilization from sheaths during grain filling, the authors generated a snrk1a mutant. By using the CRISPR–Cas9 (Clustered Regularly Interspaced Short Palindromic Repeats–CRISPR-associated protein 9) system, they generated a truncated SnRK1a protein lacking the C-terminal regulatory domain of an important SnRK1 subunit. In this mutant, SnRK1 activity in the sheaths decreased, sheaths contained more starch, and plants displayed incomplete grain filling. Seed setting rate, an important parameter determining rice yield, was also drastically reduced. That the grain filling process is clearly affected in the snrk1a mutants underscores the importance of SnRK1 in sheath-to-panicle NSC remobilization during grain filling in rice. Finally, the authors used the CRISPR-edited snrk1a mutants to identify SnRK1 targets via phosphoproteomics at different time points during grain filling. About 600 unique phosphosites were present to a different extent in the wild type versus the snrk1a mutant. Some of the enriched motifs corresponded to the well-known SnRK1 target sites. The authors clustered the identified phosphosites based on their occurrence over time and further analyzed the clusters that showed a clear decrease or increase in abundance during grain filling. Using this elegant approach, they found clusters enriched for proteins related to carbohydrate catabolism and NSC transport. Taken together, the phenotypical and biochemical analyses presented in Hu et al. (2022) offer insights in the process of grain filling in rice. SnRK1, an essential kinase for plant development and growth, was shown to play a critical role in NSC remobilization from sheaths to grain. The identification of such a central regulator opens possibilities for biotechnological engineering of rice with increased yields (Slewinski, 2012). For example, engineering faster NSC remobilization from the sheaths post floral initiation could redirect energy use from shoot growth toward grain filling, improving grain filling of all grains of the panicle (Mullet, 2017). This method has been successful in other cereals, such as maize, where altering T6P metabolism reduced shoot growth but increased seed yield (Nuccio et al., 2015). The possibility to initiate, and potentially also complete grain filling in a reduced time lapse, is of particular importance for rice plants growing in suboptimal climates where drought stress often threatens the yield at the end of the season. Funding M.D. is a postdoctoral fellow of Flanders Research Foundation (FWO-12Q7919N). Conflict of interest statement. None declared. References Chen H-J , Wang S-J ( 2008 ) Molecular regulation of sink–source transition in rice leaf sheaths during the heading period . Acta Physiol Plant 30 : 639 – 649 Google Scholar Crossref Search ADS WorldCat Hu Y , Liu J, Lin Y, Xu X, Xia Y, Bai J, Yu Y, Xiao F, Ding Y, Ding C, et al. ( 2022 ) Sucrose non-fermenting-1-related protein kinase 1 regulates sheath-to-panicle transport of non-structural carbohydrates during rice grain filling . Plant Physiol https://doi.org/10.1093/plphys/kiac124 Google Scholar OpenURL Placeholder Text WorldCat Mullet JE ( 2017 ) High-biomass C4 grasses - filling the yield gap . Plant Sci 261 : 10 – 17 Google Scholar Crossref Search ADS PubMed WorldCat Nuccio ML , Wu J, Mowers R, Zhou H-P, Meghji M, Primavesi LF, Paul MJ, Chen X, Gao Y, Haque E, et al. ( 2015 ) Expression of trehalose-6-phosphate phosphatase in maize ears improves yield in well-watered and drought conditions . Nat Biotechnol 33 : 862 – 869 Google Scholar Crossref Search ADS PubMed WorldCat Okamura M , Arai-Sanoh Y, Yoshida H, Mukouyama T, Adachi S, Yabe S, Nakagawa H, Tsutsumi K, Taniguchi Y, Kobayashi N, et al ( 2018 ) Characterization of high-yielding rice cultivars with different grain-filling properties to clarify limiting factors for improving grain yield . Field Crop Res 219 : 139 – 147 Google Scholar Crossref Search ADS WorldCat Slewinski TL ( 2012 ) Non-structural carbohydrate partitioning in grass stems: a target to increase yield stability, stress tolerance, and biofuel production . J Exp Bot 63 : 4647 – 4670 Google Scholar Crossref Search ADS PubMed WorldCat Scofield GN , Ruuska SA, Aoki N, Lewis DC, Tabe LM, Jenkins CLD ( 2009 ) Starch storage in the stems of wheat plants: localization and temporal changes . Ann Bot 103 : 859 – 868 Google Scholar Crossref Search ADS PubMed WorldCat © The Author(s) 2022. 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.