The phosphatase PC1 switches off catalase to balance salt tolerance and growth

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Cong Liu, Jianzhong Lin, and Xuanming Liu and colleagues show that the protein phosphatase PC1 dephosphorylates and deactivates CatC to negatively regulate H2O2 homeostasis and salt tolerance in rice.

https://doi.org/10.1093/plcell/koad167

By Cong Liu, Jianzhong Lin, and Xuanming Liu

Background: Soil salinity is a worldwide problem that threatens the growth and yield of crops and prevents the sustainable development of modern agriculture. Catalase is a type of hydrogen peroxide (H2O2)–scavenging enzyme that plays a central role in stress responses as well as growth and development. Catalase is a phosphoprotein whose function can be tightly regulated by phosphorylation. Several catalase kinases have been extensively studied, but its phosphatase remains unclear.

Question: How is catalase switched off by phosphatases to balance stress response and growth?

Findings: We identified a protein phosphatase of the catalase CatC (PC1) that dephosphorylates CatC at the Ser-9 residue in rice. Upon salt stress, PC1 is inhibited and leaves the catalase tetramer intact, an oligomeric form essential for high catalase activity, leading to improved salt tolerance. Once salt stress is alleviated, PC1 is activated and dephosphorylates CatC at Ser-9 to accelerate its disassociation to monomers, thereby keeping an appropriate H2O2 level to sustain rice growth and development. Thus, PC1 plays an important role during the transition from salt stress to normal growth conditions. Moreover, genetic manipulation of PC1 can limit yield loss in rice grain under salt stress.

Next steps: The functional analysis of PC1 sheds light on the switch-off mechanisms of CAT in plants. The kinase that phosphorylates CatC at Ser-9 and how PC1 is activated and inhibited require further investigation.

Reference:

Cong Liu, Jian-Zhong Lin, Yan Wang, Ye Tian, He-Ping Zheng, Zheng-Kun Zhou, Yan-Biao Zhou, Xiao-Dan Tang, Xin-Hui Zhao, Ting Wu, Shi-Long Xu, Dong-Ying Tang, Ze-Cheng Zuo, Hang He, Lian-Yang Bai, Yuan-Zhu Yang and Xuan-Ming Liu The Protein Phosphatase PC1 Dephosphorylates and Deactivates CatC to Negatively Regulate H2O2 Homeostasis and Salt Tolerance in Rice (2023) https://doi.org/10.1093/plcell/koad167

A single phosphorylation event alters root behavior

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Siao et al. demonstrate that single phosphorylation on a protein alters root behavior in Arabidopsis.

https://doi.org/10.1093/plcell/koad141

By Wei Siao and Eugenia Russinova, VIB-UGent Center for Plant Systems Biology

Background: Plant roots react to their environment by using hormone signaling pathways, which enable their cells to respond to external cues such as gravity and soil properties. Endocytosis is a cellular process in which membrane proteins or other external substances are internalized, and it can affect hormone signaling and cell communication. Therefore, changes in endocytosis can impact how a plant root responds to external stimuli. Understanding the role of endocytosis in plant root behavior can be useful in developing effective strategies to improve plant root growth and enhance nutrient-seeking behavior in the soil.

Questions: Is there a mechanism that can regulate components of the endocytic machinery? Can phosphorylation, a post-translational modification, be involved in this process?

Findings: ADAPTOR-ASSOCIATED PROTEIN KINASE 1 (AAK1) phosphorylates the medium subunit of the Adaptor Protein-2 complex (AP2M), on a single amino acid residue. Mutations in the AAK1 gene or preventing AP2M phosphorylation in Arabidopsis alter the root gravitropism and touch response to hard surfaces. Introducing a phospho-mimic form of AP2M into an aak1 mutant restored the altered root behavior to the wild-type level. Our findings show that a single phosphorylation event on AP2M by AAK1 can alter root behavior while maintaining normal plant growth and development.

Next steps: Scientists are working to decode the complex behavior of roots in order to enhance their ability to adapt to different and changing soil environments. Future studies will investigate how endocytosis coordinates different signaling pathways involved in various root tropisms, as well as identify new regulators of endocytosis that can affect root behavior.

 Reference:

 Wei Siao, Peng Wang, Xiuyang Zhao, Lam Dai Vu, Ive De Smet, and Eugenia Russinova. (2023) Phosphorylation of ADAPTOR PROTEIN-2 μ-adaptin by ADAPTOR-ASSOCIATED KINASE1 regulates the tropic growth of Arabidopsis roots. https://doi.org/10.1093/plcell/koad141

A molecular module in gibberellin signaling-mediated flowering

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Zhang and Jian et al. reveal an epigenetic regulatory mechanism underlying gibberellin signaling-mediated flowering.

https://doi.org/10.1093/plcell/koad166

By Chunyu Zhang and Xingliang Hou; South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China

 Background: The timing of floral induction is tightly controlled by environmental cues and intrinsic signals. The critical role of gibberellin (GA) in this process has been extensively studied in the past decades. DELLA proteins serve as the central regulatory hubs of GA signaling. The mechanism of GA-dependent transcription involves the recruitment of DELLA proteins to transcription factors. In general, epigenetic modifiers are believed to cooperate with transcription factors to regulate gene expression, but how epigenetic regulation participates in GA-dependent transcription of the floral integrator genes in plants remains unclear.

Question: Which epigenetic modifiers participate in GA-dependent transcription of the floral integrator genes? What is the detailed molecular mechanism involved in this process?

Findings: BRAHMA (BRM), a core catalytic subunit of the SWI/SNF-type chromatin remodeling complex, is involved in GA signaling-mediated flowering via the formation of the DELLA-BRM-NF-YC module in Arabidopsis. DELLA proteins promote the interaction of BRM with the transcription factor NUCLEAR FACTOR Y-C (NF-YC), impairing the binding of NF-YC to the floral integrator gene SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1), resulting in late flowering. Meanwhile, DELLA proteins accelerate the binding of BRM to SOC1. In the presence of GA, GA-triggered DELLA degradation disturbs the DELLA-BRM-NF-YC module and the H3K4me3 level at SOC1 chromatin increases, resulting in higher gene expression and early flowering.

Next steps: We will investigate whether the BRM-NF-Y module is also responsive to other phytohormone signals and how BRM integrates different phytohormone signals during plant development.

Reference:

Chunyu Zhang, Mingyang Jian, Weijun Li, Xiani Yao, Cuirong Tan, Qian Qian, Yilong Hu, Liu Xu, Xingliang Hou. (2023). Gibberellin signaling modulates flowering via the DELLA-BRAHMA-NF-YC module in Arabidopsis https://doi.org/10.1093/plcell/koad166

Leaf starch reserves keep stomata on time

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Image credit for featured image: Gilles Pantin

 

Westgeest et al. use a high-throughput phenotyping pipeline to explore the connection between leaf starch and stomatal opening

https://doi.org/10.1093/plcell/koad158

Adrianus J. Westgeest and Florent Pantin, L’Institut Agro, Montpellier, France

Background: Leaves have tiny pores called stomata, which are surrounded by a pair of guard cells. Stomata generally open during the day to facilitate the capture of CO2 for photosynthesis, and close at night to limit the loss of water vapor. One century ago, pioneering observations under the microscope revealed that stomata preopen several hours before dawn. We know now that the circadian clock, the plant’s endogenous timer, is necessary for stomata to preopen at night. In addition to the circadian clock, leaf starch is synthesized during the day and broken down at night to generate sugars for energy, thus acting as a transitory metabolic clock.

Question: Production of sugars from starch in guard cells was recently found to be essential for light-induced stomatal opening. How does leaf starch metabolism connect with endogenous stomatal movements such as nighttime preopening?

Findings: We developed PhenoLeaks, a phenotyping pipeline to analyze the transpiration dynamics over days and nights on 150 plants at the same time. We screened a collection of Arabidopsis starch mutants and found that severe mutations in starch metabolism not only disrupt stomatal preopening at night, but also delay endogenous stomatal movements during the whole day. When the lesions in starch metabolism were confined to the guard cells, stomata showed normal endogenous movements, suggesting that starch from the rest of the leaf is able to set the tempo of stomatal movements, most likely by providing sugars that interact with the guard-cell circadian clock.

Next steps: The challenge now is to decipher the molecular dialogue between the guard cells and the rest of the leaf, and to exploit the endogenous stomatal movements to improve water use efficiency in crop species.

Reference:

Adrianus J. Westgeest, Myriam Dauzat, Thierry Simonneau, Florent Pantin (2023) Leaf starch metabolism sets the phase of stomatal rhythm. https://doi.org/10.1093/plcell/koad158

The E3 ubiquitin ligases PUB25 and PUB26 dynamically regulate cold stress responses in plants

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Wang et al. discovered how plants dynamically respond to cold stress mediated by the E3 ligases PUB25 and PUB26.

https://doi.org/10.1093/plcell/koad159

By Xi Wang1, Xiaoyan Zhang1, Chunpeng Song3, Zhizhong Gong1,2, Shuhua Yang1 and Yanglin Ding1

1State Key Laboratory of Plant Environmental Resilience, College of Biological Sciences, China Agricultural University, Beijing 100193, China

2School of Life Sciences, Institute of Life Science and Green Development, Hebei University, Baoding, 071002, China.

3Institute of Plant Stress Biology, Collaborative Innovation Center of Crop Stress Biology, Henan University, Kaifeng, China,

Background: Plant cold stress responses inhibit growth by repressing cell division and expansion. Strict regulation of cold responsive genes balances growth and cold stress responses. For example, the expression of C-REPEAT BINDING FACTOR/DEHYDRATION-RESPONSIVE ELEMENT BINDING PROTEIN1 (CBF/DREB1) genes increases rapidly at the early stages of cold stress; however, their expression is inhibited at the late stages of cold stress. Ubiquitination is a conserved post-translational modification that modulates protein turnover and activity depending on the number and location of attached ubiquitin moieties. However, it remains unclear whether ubiquitination regulates the timing and degree of cold stress responses in plants by dynamically modulating cold responsive gene expression.

Question: Do the E3 ubiquitin ligases PLANT U-BOX 25 (PUB25) and PUB26 affect cold-regulated gene expression during cold stress in plants? Do PUB25 and PUB26 attach different ubiquitin chains to transcriptional factor INDUCER OF CBF EXPRESSION1 (ICE1) during cold stress? What is the detailed mechanism?

Findings: We discovered that PUB25 and PUB26 attach both K48- and K63-linked ubiquitin chains to ICE1 during cold stress. Notably, PUB25 and PUB26 attached a K63-linked ubiquitin chain to ICE1 after one hour of cold treatment; this modification may be required to stabilize ICE1, which then induces CBF expression. By contrast, K48-linked ICE1 ubiquitination increased after six hours of cold stress; this modification may attenuate the initial cold response. In addition, PUB25 and PUB26 mediated K48- and K63-linked ubiquitination of the transcription factor MYB15 during cold treatment. Furthermore, ICE1 interacted with MYB15 and repressed its binding to the promoters of CBFs. This study thus unravels a mechanism by which PUB25 and PUB26 add different polyubiquitin chains to ICE1 and MYB15 to modulate their stability, thereby regulating the timing and degree of cold stress responses in plants.

Next steps: How PUB25/PUB26-mediated ubiquitination crosstalks with phosphorylation at the different stages of cold stress is an important question. How many proteins are attached different ubiquitin chains in regulating cold stress in a time-dependent manner is another key issue to be investigated in future studies.

Reference:

Xi Wang, Xiaoyan Zhang, Chunpeng Song, Zhizhong Gong, Shuhua Yang, Yanglin Ding (2023) PUB25 and PUB26 dynamically modulate ICE1 stability via differential ubiquitination during cold stress in Arabidopsis. https://doi.org/10.1093/plcell/koad159

A tug-of-war in the viral replication factory: How a viral protein interferes with stress granules

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Hoffmann et al. explore replication of Cauliflower mosaic virus and how virus replication intersects RNA granule biology.

https://doi.org/10.1093/plcell/koad101

Gesa Hoffmann and Anders Hafrén, Swedish University of Agricultural Sciences

Background: Regulating RNA abundance and its availability for translation is one of the main struggles between virus and host during plant virus infections. The pararetrovirus Cauliflower mosaic virus (CaMV) shields its nucleic acids, proteins and particles from its host antiviral pathways by establishing large, amorphous condensates, termed viral factories. These condensates consist mainly of one multifunctional viral protein, the P6 protein. We have previously found that host RNA decapping proteins, canonically associated with phase-separated RNA granules, localize within these viral factories and aid in the translation of viral RNA. The interplay between virus replication and RNA granule biology is conserved among eukaryotes and likely represents an ancient mechanism.

Question: Our first aim was to further characterize the viral factory of CaMV and observe the behavior of host proteins within these condensates. Our second aim was to dissect the interaction of the viral P6 protein with RNA granules and RNA granule proteins, as well as its effect on translation in the context of condensation.

Findings: Unlike the rigid P6 matrix, RNA granule proteins can rapidly shuffle between viral factories and the surrounding cytoplasm. Several RNA granule proteins can bind viral RNA; however, their binding capacities seem to be specific for certain viral RNA species. Stress granule proteins preferentially bind to the non-coding highly abundant 8s RNA, which may dampen stress granule responses in the plant. The P6 protein, by contrast, strongly localizes to stress granules and hinders their establishment due to its remarkable ability to enhance global translation levels. Importantly, the efficiency with which P6 exerts its functions is in part coupled to its condensation level, which likely represents a self-attenuation mechanism of CaMV during prolonged infections.

Next steps: We have merely scratched the surface of the viral factory-localized host proteome and RNAome. Are there common features of the plant proteins and RNAs that accumulate within the viral factories? Elucidating which host factors are co-opted by the virus will further our understanding of virus disease in plants.

Reference:

Gesa Hoffmann, Silvia López-González, Amir Mahboubi, Johannes Hansonc, and Anders Hafrén (2023) Cauliflower mosaic virus protein P6 is a multivalent node for RNA granule proteins and interferes with stress granule responses during plant infection. https://doi.org/10.1093/plcell/koad101

 

Tip swelling of SI pollen tubes in pear

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Tang and Wang et al. explore the mechanism underlying pollen tube tip swelling in the self-incompatibility response.

https://doi.org/10.1093/plcell/koad162

By Chao Tang1,2, Peng Wang1,2, Shaoling Zhang1,2 and Juyou Wu1,2,3

1 Sanya Institute of Nanjing Agricultural University, State Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, Nanjing Agricultural University, Nanjing 210095, China

2 Jiangsu Engineering Research Center for Pear, Nanjing 210014, China

3 Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Nanjing 210014, China

Background: Self-incompatibility is a widespread genetic mechanism in flowering plants that prevents self-fertilization and promotes outbreeding. S-RNase-based SI is characterized by the arrest of pollen tube growth through the pistil, resulting in disrupted and swollen pollen tube tips that do not reach the ovule and therefore fail to complete fertilization. However, the underlying molecular mechanism responsible for pollen tube tip swelling is still largely unknown.

Question: Which factors play roles in pollen tube tip swelling during the self-incompatibility response?

Findings: Here we report that the swelling at the tips of incompatible pollen tubes in pear is mediated by self-incompatibility–induced acetylation of the soluble inorganic pyrophosphatase PbrPPA5. Acetylation at Lys-42 of PbrPPA5 by the acetyltransferase PbrGNAT1 caused PbrPPA5 to accumulate in the nucleus. Acetylated PbrPPA5 bound to the transcription factor PbrbZIP77 to form a transcriptional repression complex that inhibited the expression of the pectin methylesterase gene PbrPME44. Downregulating PbrPME44 resulted in increased levels of methyl esterified pectins in growing pollen tubes, leading to swelling at their tips.

Next steps: In future studies, we aim to further investigate how the acetyltransferase PbrGNAT1 responds to self-incompatibility signaling and how the soluble inorganic pyrophosphatase PbrPPA5 accumulates in the nucleus.

Reference:

Chao Tang, Peng Wang, Xiaoxuan Zhu, Kaijie Qi, Zhihua Xie, Hao Zhang, Xiaoqiang Li, Hongru Gao, Tingting Gu, Chao Gu, Shan Li, Barend H. J. de Graaf, Shaoling Zhang, Juyou Wu. (2023). Acetylation of inorganic pyrophosphatase by S-RNase signaling induces pollen tube tip swelling by repressing pectin methylesterase. https://doi.org/10.1093/plcell/koad162

Epigenetic regulation during rice domestication and de-domestication

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Cao et al. investigate the role of epigenetic variation in rice domestication and de-domestication. The Plant Cell (2023).

https://doi.org/10.1093/plcell/koad160

By Shuai Cao1,2 and Qingxin Song1

1 State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, China

2 Temasek Life Sciences Laboratory, National University of Singapore, Singapore

Background: Humans have domesticated hundreds of plant and animal species as sources of food and materials. For example, rice (Oryza sativa) feeds more than a third of the global population. Cultivated rice was domesticated from a wild progenitor ~9000 years ago, which was accompanied by dramatic changes in morphological and physiological traits. Importantly, cultivated rice can turn back into ‘wild-like’ plants under natural selection, by de-domestication. DNA methylation is a conserved epigenetic mark in most eukaryotes that plays important roles in plant development and environmental responses. However, whether epigenetics contributes to domestication and de-domestication of rice is largely unknown.

Question: We wished to know whether and how variation in DNA methylation affected gene expression during rice domestication (cultivars vs wild rice) and de-domestication (weedy rice vs cultivars).

Findings: We generated single-base resolution DNA methylomes from 95 accessions of wild, cultivated and weedy rice. We detected a significant decrease in DNA methylation during rice domestication. By contrast, DNA methylation dramatically increased following rice de-domestication. Notably, hypomethylated sites from wild to cultivated rice and hypermethylated sites from cultivated to weedy rice were largely not shared. We determined that variation in DNA methylation affected the binding of transcription factors and chromatin accessibility to regulate expression of nearby and distal genes, which would be expected to cause morphological changes during domestication and de-domestication of rice.

Next steps: Future efforts will focus on identification of DNA methylation variants associated with changes for agronomic traits during rice domestication, which could help breeders facilitate rice improvement through epigenetic engineering and breeding.

Reference:

Shuai Cao, Kai Chen, Kening Lu, Shiting Chen, Xiyu Zhang, Congcong Shen, Shuangbin Zhu, Yanan Niu, Longjiang Fan, Z. Jeffrey Chen, Jianlong Xu, and Qingxin Song. (2023). Asymmetric variation in DNA methylation during domestication and de-domestication of rice. https://doi.org/10.1093/plcell/koad160

SnRK1 and TOR—in a different light

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Saile et al. explore the role of SnRK1 and TOR in light-dependent seedling development and splicing.

https://doi.org/10.1093/plcell/koad168

Jennifer Saile and Andreas Wachter

Institute for Molecular Physiology (imP), University of Mainz

Background: Plants adjust their development to light and metabolic signals to make best use of their available resources. Dark-grown seedlings undergo etiolation with increased hypocotyl elongation, while illumination causes greening of leaves to initiate photosynthesis. These alternative developmental programs require reprograming of many genes via various mechanisms. Accordingly, exposing etiolated seedlings to light or sugar causes changes in splicing, a critical step in the generation of mature mRNAs. Key sensors for metabolic signals are SnRK1 (SNF1-RELATED KINASE 1) and TOR (TARGET OF RAPAMYCIN), which were shown to be activated under conditions of limited and ample energy availability, respectively.

Question: Given the importance of SnRK1 and TOR in sensing the metabolic state, we examined their role in light-dependent seedling development and splicing. We were particularly interested in establishing if they have opposing functions and whether this differs for seedlings grown in the presence or absence of light.

Findings: We have established mutants in the model plant Arabidopsis thaliana for inducible repression of SnRK1 and TOR. Mutant analysis revealed that both components are needed for regular seedling development in darkness and light. Furthermore, SnRK1 and TOR are involved in controlling light-regulated splicing events. Knockdown of either SnRK1 or TOR caused similar changes in splicing as those observed upon exposing etiolated seedlings to light or sucrose. Our findings demonstrate that concurring activities of these two energy sensors are indispensable for proper regulation of gene expression and seedling development.

Next steps: SnRK1 and TOR are assumed to have antagonistic functions in energy sensing. Resolving their crosstalk in various developmental conditions will be a key aspect of future research. Moreover, it will be of interest to examine the mechanism by which SnRK1 and TOR can alter the splicing outcome.

Reference:

Jennifer Saile, Theresa Wießner-Kroh, Katarina Erbstein, Dominik M. Obermüller, Anne Pfeiffer, Denis Janocha, Jan Lohmann, and Andreas Wachter. (2023). SNF1-RELATED KINASE 1 and TARGET OF RAPAMYCIN control light-responsive splicing events and developmental characteristics in etiolated Arabidopsis seedlings. https://doi.org/10.1093/plcell/koad168