HY5a regulates winter dormancy in poplar

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Gao, Chen et al. explore the regulatory mechanisms governing winter dormancy in trees.

https://doi.org/10.1093/plcell/koae022

Yongfeng Gao, Zihao Chen and Yinan Yao

School of Life Science and Engineering, Southwest University of Science and Technology, 621010 Mianyang, China

Background: Winter dormancy, a process where growth stops and plants acquire a dormant and freezing-tolerant state, is crucial for the survival of woody plants in boreal and temperate regions. The seasonal growth of perennial woody plants is controlled by dormancy entry and release, which are regulated by complex and precise mechanisms influenced by environmental cues. Dormancy entry is mainly induced by short photoperiods and is characterized by growth cessation and bud set. The central activator of flowering, FLOWERING LOCUS T (FT), is also the key target for winter dormancy induction. To satisfy distinct needs in dormancy or flowering, woody plants likely use different pathways than herbaceous plants use to regulate FT. Although a LATE ELONGATED HYPOCOTYL (LHY)–FT regulatory pathway analogous to that in herbaceous plants exists in woody plants, its efficacy in preventing dormancy in trees is limited.

Question: Do other regulatory mechanisms regulate winter dormancy in trees? 

Findings: We determined that PtoHY5a, a poplar (Populus tomentosa) ortholog of Arabidopsis (Arabidopsis thaliana) ELONGATED HYPOCOTYL5 (HY5), mediates dormancy induction downstream of photoreceptor PHYB signaling. PtoHY5a directly and indirectly regulates the key target for winter dormancy induction, FT2, via two transcriptional modules. Moreover, PtoHY5a controls gibberellic acid levels in apical buds to inhibit bud break in poplar.

Next steps: The next step would be to explore PtoHY5a as a key target for genetic modification in trees. Genetic modification of PtoHY5a could be particularly useful when introducing trees to different latitudes; for instance, from northern regions to high-altitude southern areas, such as from the Tibetan Plateau to the South Asian Highlands, or vice versa. By understanding and manipulating PtoHY5a, we could potentially optimize tree adaptation to new environments, thereby enhancing their survival and productivity.

Reference:

Yongfeng Gao, Zihao Chen, Qian Feng, Tao Long, Jihua Ding, Peng Shu, Heng Deng, Peizhi Yu, Wenrong Tan, Siqin Liu, Lucas Gutierrez Rodriguez, Lijun Wang, Víctor Resco de Dios, Yinan Yao. (2024). ELONGATED HYPOCOTYL 5a modulates FLOWERING LOCUS T2 and gibberellin levels to control dormancy and bud-break in poplar. https://doi.org/10.1093/plcell/koae022

Enhancing plants’ capability of P uptake to feed the world

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Hu et al. uncover a major regulatory model that can enhance plants’ P uptake from soils.

https://doi.org/10.1093/plcell/koae041

By Dandan Hua, Hengyou Zhangb and Dan Zhanga

a Collaborative Innovation Center of Henan Grain Crops, College of Agronomy, Henan Agricultural University, Zhengzhou, China;

bState Key Laboratory of Black Soils Conservation and Utilization, Key Laboratory of Soybean Molecular Design Breeding, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Harbin, China

Background: Phosphorus (P), produced from non-renewable phosphate rock, is an essential nutrient for plant growth and development. However, ~40% of the world’s arable land is P deficient. Plants have evolved a series of complex strategies that allow them to adapt to P deficient soils, including phosphate activation, absorption, transport, storage, and reuse. The growth of soybean, a major source of plant-based protein worldwide, requires a large amount of P. Therefore, the availability of P in soils is key to ensuring optimal soybean yields. There is thus an urgent need to develop a genetic solution to improve P uptake and conserve phosphate resources globally.

Question: Do soybean plants themselves hold the key to developing new high-yield soybean varieties? Can a deeper understanding of the molecular mechanisms underlying phosphate absorption and utilization in soybean help us develop strategies to improve P uptake and use efficiency in this important crop?

Findings: We uncovered a major low P tolerance gene in soybean, GmGDPD2, through genetic methods. Overexpression of this gene significantly promoted root growth and development and increased root uptake of phosphate and yield. By contrast, knocking out this gene inhibited root growth and reduced P absorption, reducing yield. We also identified a GmGDPD2-interacting protein, GA2ox1. GmMyb73 inhibited GmGDPD2 expression by binding to its promoter region. These results allowed us to identify the Myb73-GDPD2-GA2ox1 regulatory module, which helps plants acquire more P from the soil by promoting root growth.

Next steps: We will continue examining the Myb73-GDPD2-GA2ox1 module to dissect the detailed mechanism underlying P efficiency. For example, we found that an acid phosphatase gene GmAPA17 is significantly upregulated in the gdpd2 mutant, which may be an important gene downstream of the module. More genes regulated by GmGDPD2 and their regulatory mechanisms remain to be explored.

Reference:

Dandan Hu, Ruifan Cui, Ke Wang, Yuming Yang, Ruiyang Wang, Hongqing Zhu, Mengshi He, Yukun Fan, Le Wang, Li Wang, Shanshan Chu, Jinyu Zhang, Shanshan Zhang, Yifei Yang, Xuhao Zhai, Haiyan Lv, Dandan Zhang, Jinshe Wang, Fanjiang Kong, Deyue Yu, Hengyou Zhang, Dan Zhang. (2024). The Myb73-GDPD2-GA2ox1 transcriptional regulatory module confers phosphate deficiency tolerance in soybean. https://doi.org/10.1093/plcell/koae041

A battle in rice flowers

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Li et al. investigate the mechanisms of defense and counter-defense in a floral pathosystem.

https://doi.org/10.1093/plcell/koae027

By Guo-Bang Li, Wen-Ming Wang, and Jing Fan

Background: Rice false smut is an emerging fungal disease threatening rice production worldwide. This disease not only reduces grain yield but also introduces food toxins. The causative pathogen invades rice flowers via the gap between the two bracts (lemma and palea) enclosing the floret and specifically infects the stamens and pistils. The underlying mechanisms by which rice flowers defend against the pathogen and the pathogen counteracts this defense remain largely unknown.

Question: The optimal defense theory predicts that flowers should receive protection from constitutive defenses, rather than inducible defenses against herbivores. Do rice flowers deploy constitutive or induced defense against the false smut fungus? How does the pathogen overcome rice defense?

Findings: Chitin is a vital component of fungal cell walls and often elicits plant immunity. We show that rice flowers predominantly employ chitin-induced immunity against the false smut fungus in lemmas and paleas, rather than in stamens and pistils. We identify a secreted protein, named UvGH18.1, as a core virulence factor for the false smut pathogen. UvGH18.1 breaks down chitin to prevent host immune elicitation and further targets rice chitin sensors to impair chitin signaling, suppressing host immunity exerted at lemmas and paleas to gain access to stamens and pistils. Conversely, pretreating flowers with chitin promotes rice resistance to false smut, offering a potential strategy to control this disease.

Next steps: One next step is to identify plant receptors that recognize UvGH18.1 or other molecules derived from the false smut fungus. Another is to identify chemicals that inhibit UvGH18.1 function to block pathogen infection.

Reference:

Guo-Bang Li, Jie Liu, Jia-Xue He, Gao-Meng Li, Ya-Dan Zhao, Xiao-Ling Liu, Xiao-Hong Hu, Xin Zhang, Jin-Long Wu, Shuai Shen, Xin-Xian Liu, Yong Zhu, Feng He, Han Gao, He Wang, Jing-Hao Zhao, Yan Li, Fu Huang, Yan-Yan Huang, Zhi-Xue Zhao, Ji-Wei Zhang, Shi-Xin Zhou, Yun-Peng Ji, Mei Pu, Min He, Xuewei Chen, Jing Wang, Weitao Li, Xian-Jun Wu, Yuese Ning, Wenxian Sun, Zheng-Jun Xu, Wen-Ming Wang, Jing Fan (2024). Rice false smut virulence protein subverts host chitin perception and signaling at lemma and palea for floral infection. https://doi.org/10.1093/plcell/koae027

PagMYB31 coordinates cambial cell proliferation and differentiation in poplar wood formation

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Zhang et al. explore the regulation of cambium division and differentiation in poplar.

https://doi.org/10.1093/plcell/koae040

Yanhui Zhang and Quanzi Li, State Key Laboratory of Tree Genetics and Breeding, Chinese Academy of Forestry, Beijing, China

Background: In trees such as poplar (Populus spp.), wood formation involves cell division of the vascular cambium, xylem cell expansion, secondary cell wall (SCW) deposition, and programmed cell death. The ability of cambial cells to continue to divide is critical for the stems, branches, and trunks of woody plants to grow in diameter (radial growth). Therefore, understanding how plants regulate cambial cells has implications for producing trees with improved wood growth. The WUSCHEL-homeobox transcription factor WOX4 has been identified as a central regulator of cambial cell division and NAC and MYB transcription factors have been identified as key regulators of secondary cell wall thickening. However, our current knowledge on how cambial cell proliferation and differentiation are coordinately regulated is still limited.

Question: We wanted to identify which gene is involved in regulating cambium cell division and differentiation (xylem development), and understand how it regulates cambial cell proliferation and differentiation in poplar (Populus alba × Populus glandulosa).

Findings: Phenotypic characterization of mutant and overexpressing transgenic plants demonstrated that the transcription factor PagMYB31 positively regulates cambial cell proliferation and negatively regulates xylem cell expansion and secondary cell wall biosynthesis. We find that PagMYB31 plays an important role in maintaining vascular cambium homeostasis in multiple pathways to promote or inhibit WOX4 expression. We also find that PagMYB31 inhibits the expansion of cambial cells and xylem cells, and wall thickening of xylem cells, demonstrating its essential role in balancing cambial meristematic fate and differentiation. PagMYB31 can directly regulate key genes controlling cambial cell proliferation and xylem development, placing PagMYB31 at the center of the regulatory network coordinating wood formation.

Next steps: This study shows that PagMYB31 has opposite functions in regulating cambial cell proliferation and xylem development (cell expansion and wall thickening). Further analyses will be carried out to uncover what upstream cues or factors regulate PagMYB31, and explore strategies for breeding trees with augmented growth.

Reference:

Yanhui Zhang, Song Chen, Linghua Xu, Shimin Chu, Xiaojing Yan, Lanying Lin, Jialong Wen, Bo Zheng, Su Chen, Quanzi Li. (2024). Transcription factor PagMYB31 positively regulates cambium activity and negatively regulates xylem development in poplar. https://doi.org/10.1093/plcell/koae040

Plant cell-to-cell communication constrains viroid quasispecies

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Wu and Bisaro study the sequence structure of viroid quasispecies in plant cells.

https://doi.org/10.1093/plcell/koae012

 Jian Wu1,2,3 and David M. Bisaro3

1State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agroproducts, Institute of Plant Virology, Ningbo University, Ningbo 315211, China

2Key Laboratory of Biotechnology in Plant Protection of MARA and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo 315211, China

3Department of Molecular Genetics, Center for Applied Plant Sciences, Center for RNA Biology, and Infectious Diseases Institute, The Ohio State University, Columbus, Ohio, 43210, United States of America

Background: RNA viroids, minute infectious agents, have high mutation rates, resulting in diverse populations known as quasispecies.  Despite this mutability, viroid quasispecies exhibit remarkable stability in sequence structure. Typically, a few master sequences dominate, while numerous variants also exist.  Plasmodesmata, which enable communication between cells and regulate RNA movement, may play an important role in constraining viroid sequence diversity.

Question: This study employed potato spindle tuber viroid (PSTVd) to explore constraints on viroid quasispecies. In particular, we examined the role of plasmodesmata and initial viroid population sequence structure.

Findings: Unexpectedly, a higher accumulation of PSTVd variants was observed in isolated guard cells and in vitro-cultivated mesophyll protoplasts compared to whole leaves.  Remarkably, plant cells were found to be susceptible to multiple infections by the same or different variants, enabling the coexistence of multiple variants within a single cell.  Co-infection experiments revealed a higher emergence of novel variants in populations initially lacking a master sequence.  This underscores the significance of plasmodesmata-mediated cell-to-cell communication and the initial sequence composition as two key constraints on PSTVd quasispecies.

Next steps: Subsequent research should delve into the molecular intricacies involved, unraveling the contributions of initial viroid sequences and cell-to-cell communication to quasispecies evolution.  This deeper understanding holds potential implications for devising strategies to manage viroid infections in plants.

Reference:

Jian Wu and David M. Bisaro. (2024). Cell-cell communication and initial population composition shape the structure of potato spindle tuber viroid quasispecies. https://doi.org/10.1093/plcell/koae012

Role of chlorophyll degradation during the biosynthesis of tocopherol (vitamin E) and phylloquinone (vitamin K)

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Romer et al. study the origin of the lipid side chain phytol in tocopherol and phylloquinone synthesis in Arabidopsis.

https://doi.org/10.1093/plcell/koad316

 

By J. Romer, K. Gutbrod and P. Dörmann

Background: Isoprenoid lipids in Arabidopsis chloroplasts include chlorophyll, carotenoids, tocopherols (vitamin E) and phylloquinone (vitamin K). Their biosynthesis depends on the availability of the isoprenoid precursors geranylgeranyl-diphosphate and phytyl-diphosphate. The geranylgeranyl moiety can first be incorporated into chlorophyll where it is reduced to the phytyl group and subsequently hydrolyzed. Phytol kinase (VTE5) phosphorylates phytol, and phytol-phosphate kinase (VTE6) produces phytyl-diphosphate which is employed for tocopherol and phylloquinone synthesis. While the vte5 mutant of Arabidopsis contains reduced amounts of tocopherol, the vte6 mutant is deficient in tocopherol and phylloquinone.

Questions: Why do tocopherol and phylloquinone synthesis differentially depend on phytol phosphorylation by phytol kinase (VTE5)? Does another kinase contribute to phytol phosphorylation?

Findings: Arabidopsis contains one paralog to VTE5, FOLK (farnesol kinase), which is involved in farnesol phosphorylation. We show here that FOLK also phosphorylates phytol. While the vte5 folk double mutant is completely devoid of tocopherol, it still accumulates residual amounts of phylloquinone. The amounts of chlorophyll and carotenoids are not affected in the vte5 folk mutant. Ectopic expression of FOLK partially complements tocopherol deficiency in vte5. Therefore, VTE5 and FOLK are essential to provide phytol-phosphate for tocopherol synthesis, but alternative pathways exist to provide the phytyl group during phylloquinone synthesis.

Next steps: Further research is required to elucidate the contribution of the different pathways to geranylgeraniol and phytol metabolism for isoprenoid lipid synthesis in chloroplasts.

Reference:

Jill Romer, Katharina Gutbrod, Antonia Schuppener, Michael Melzer, Stefanie J. Müller-Schüssele, Andreas J. Meyer, Peter Dörmann (2024). Tocopherol and phylloquinone biosynthesis in chloroplasts requires the phytol kinase VTE5 and the farnesol kinase FOLK. https://doi.org/10.1093/plcell/koad316

A zinc finger protein promotes salt signaling in rice via transphosphorylation

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Tian et al. identify the zinc finger protein DHHC09 as a regulator of rice salt tolerance.

https://doi.org/10.1093/plcell/koae001

 

By Ye Tian, Xuan-Ming Liu, and Jian-Zhong Lin

Background: Soil salinity results in oxidative stress and heavy losses to crop production. S-acylation of proteins occurs extensively in plants and plays important roles in many essential cellular functions. Receptor-like kinases (RLKs) often act as receptors to perceive extracellular signals or stimuli, resulting in dimerization followed by autophosphorylation and activation of receptor-like cytoplasmic kinases (RLCKs) by transphosphorylation. Activated RLCKs then phosphorylate downstream target proteins to initiate the stress response. The S-acylated RLCK protein SALT TOLERANCE RECEPTOR-LIKE CYTOPLASMIC KINASE 1 (STRK1) phosphorylates and activates CATALASE C (CATC) to improve rice (Oryza sativa L.) salt tolerance, but the molecular mechanism underlying its S-acylation in salt signal transduction awaits elucidation.

Question: What is the molecular mechanism underlying S-acylation in RLK/RLCK-mediated salt signal transduction?

Findings: We identified the DHHC-type zinc finger protein DHHC09, which S-acylates STRK1 at several cysteine residues and positively regulates salt tolerance in rice. DHHC09-mediated S-acylation mainly determines STRK1 targeting to the plasma membrane and promotes salt signaling from STRK1 to CATC via transphosphorylation, thereby regulating H2O2 homeostasis and improving rice salt tolerance. DHHC09 deficiency impairs this signaling cascade and causes hypersensitivity to salt stress. Moreover, DHHC09 overexpression in rice mitigates grain yield loss under salt stress.

Next steps: The plasma membrane is highly compartmentalized into lipid nanodomains, which play a pivotal role in cellular signal transduction. The unknown upstream RLK of STRK1 and the micro-environment of lipid nanodomains in which S-acylated STRK1 resides require further investigation.

Reference:

Ye Tian, Hui Zeng, Ji-Cai Wu, Gao-Xing Dai, He-Ping Zheng, Cong Liu, Yan Wang, Zheng-Kun Zhou, Dong-Ying Tang, Guo-Fu Deng, Wen-Bang Tang, Xuan-Ming Liu, Jian-Zhong Lin. (2024). The zinc finger protein DHHC09 S-acylates the kinase STRK1 to regulate H2O2 homeostasis and promote salt tolerance in rice. https://doi.org/10.1093/plcell/koae001

Review: Strategies to improve photosynthesis

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Photosynthesis is the process by which plants assimilate carbon by using light energy. However, with the solar energy conversion efficiency of many crop plants less than 1%, it is inefficient. Therefore, there is interest in manipulating photosynthesis for increased efficiency. Here, Croce et al. identifying nine strategies that have, or could be, implemented to achieve this. At the light absorption level, one strategy is to alter the light that plants absorb to include far-red light, by using cyanobacterial chlorophylls. On the biochemistry side, increasing the expression or activity of sedoheptulose 1,7-bisphosphatase and fructose 1,6-bisphosphate aldolase, which are enzymes of the Calvin-Benson-Bassham cycle, can increase photosynthesis. The authors also suggest some high-risk, high-reward strategies for increasing the activity of RuBisCo, a major rate limiting enzyme in the Calvin-Benson-Bassham cycle. These include engineering carbon concentrating mechanisms from green algae into plants, or replacing native RuBisCo with a higher efficiency version found in red algae. Finally, they consider leaf physiology, such as how increasing stomatal density can increase photosynthesis, although this can also lead to increased water loss. Overall, there are a plethora of strategies which could be used to improve photosynthesis, and these need to be integrated together for the maximum efficiency. (Summary by Rose McNelly @Rose_McN) Plant Cell 10.1093/plcell/koae132

Review: Optimizing nutrient transporters to enhance disease resistance in rice

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Plants rely on an array of mineral nutrients for their growth, development, and reproductive processes. The molecular mechanisms governing the uptake, translocation, storage, and utilization of these essential minerals are orchestrated by specific nutrient transporters and their associated regulatory elements, including microRNAs and the ubiquitylation system. Intriguingly, mounting evidence indicates that beyond the traditional roles in plant physiology, mineral nutrients also play pivotal roles in bolstering plant defense mechanisms against pathogens. On one front, the modulation of plant nutrient status, achieved through adjustments in external nutrient availability or the manipulation of nutrient transporter expression, can significantly impact the output of the plant’s immune response. Conversely, the expression levels of nutrient transporters themselves can be influenced by pathogen invasion. This intricate bi-directional interplay underscores the close nexus between nutrient status and the efficacy of plant immunity. Hui and colleagues offer a comprehensive review of existing literature, elucidating the connections between nutrient transporters and disease resistance in rice. Their work not only underscores the pivotal role of nutrient transporters in fortifying plant defenses but also presents promising avenues for enhancing disease resistance in rice through genetic engineering strategies targeting these transporters. (Summary by Ching Chan @ntnuchanlab) J. Exp. Bot. 10.1093/jxb/erae087