The Role of ECT8 in Decoding Salt Stress Resistance in Plants

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Zhihe Cai (Synthetic and Functional Biomolecules Center, Beijing National Laboratory for Molecular Sciences, Key Laboratory of Bioorganic Chemistry and Molecular Engineering of Ministry of Education, College of Chemistry and Molecular Engineering, Peking University, Beijing 100871, China)

https://doi.org/10.1093/plcell/koae149

Background: We’ve been studying a protein named ECT8 in a common plant called Arabidopsis. This protein can spot and catch a specific tag, known as m6A, on the plant’s RNA – a molecule that carries out the DNA’s instructions.

Question: We wanted to know how ECT8 interacts with this tagged RNA and what happens to the RNA afterwards, especially when the plant is dealing with too much salt.

Findings: We found out that ECT8 helps break down this tagged RNA faster, especially when the plant is under salt stress. But, when we messed with ECT8, the plant became more sensitive to salt because it started making more proteins that make it less salt-tolerant.

Next Steps: The question now is how we can use this new understanding of ECT8 to help plants better handle stress. This could change crop cultivation in challenging environments.

Reference:

Zhihe Cai, Qian Tang, Peizhe Song, Enlin Tian, Junbo Yang, Guifang Jia (2024) The m6A reader ECT8 is an abiotic stress sensor that accelerates mRNA decay in Arabidopsis https://doi.org/10.1093/plcell/koae149

Ethylene antagonizes gibberellin signaling to accelerate petal senescence

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Lu, Zhang et al. investigate the mechanisms of phytohormone cross-talk underlying rose petal senescence

By Jingyun Lu, Guifang Zhang, Yunhe Jiang, and Junping Gao

China Agricultural University

https://doi.org/10.1093/plcell/koae035

 Background:

Rose (Rosa hybrida) is the queen of flowers, cultivated worldwide for its great economic, symbolic, and cultural importance. Petal senescence is vital for ensuring optimal offspring production, but delaying petal senescence and extending a flower’s longevity have applications in the ornamental flower industry. The timing of petal senescence determines flower longevity and is regulated by phytohormones. Ethylene is the major phytohormone promoting petal senescence, while gibberellic acid (GA) represses this process. The molecular mechanisms underlying the crosstalk between these phytohormones in regulating rose petal senescence remain largely unclear.

Question:

How does ethylene antagonize the effects of GA to accelerate petal senescence?

Findings:

The ethylene-induced F-box protein SENESCENCE-ASSOCIATED F-BOX (RhSAF) accelerates petal senescence by repressing GA signaling in rose. At the early stages of flower opening, the RhGID1 GA receptors are stabilized, as low ethylene levels in petals fail to induce RhSAF expression. During the late stages of flower opening, ethylene levels increase and upregulate RhSAF expression. RhSAF then recognizes RhGID1s and triggers their ubiquitin-mediated degradation through the 26S proteasome, which attenuates GA signaling and accelerates petal senescence.

Next steps:

The present work indicates that additional proteins are RhSAF substrates. It will be interesting to explore their function in phytohormone crosstalk and in regulating petal senescence.

Reference:

Jingyun Lu, Guifang Zhang, Chao Ma, Yao Li, Chuyan Jiang, Yaru Wang, Bingjie Zhang, Rui Wang, Yuexuan Qiu, Yanxing Ma, Yangchao Jia, Cai-Zhong Jiang, Xiaoming Sun, Nan Ma, Yunhe Jiang, Junping Gao. (2024). The F-box protein RhSAF destabilizes the gibberellic acid receptor RhGID1 to mediate ethylene-induced petal senescence in rose. https://doi.org/10.1093/plcell/koae035

A chromatin remodeler and a histone chaperone help repair DNA

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Fan et al. investigate the proteins involved in DNA base excision repair

https://doi.org/10.1093/plcell/koae052

By Tianyi Fan and Yan Zhu

Background: DNA bases are susceptible to damage from environmental factors such as UV light or reactive oxygen species. Base excision repair (BER) can eliminate modified or damaged DNA bases. However, chromatin structures pose natural obstacles to the recognition and repair of DNA lesions. The mechanisms governing BER within the context of chromatin are imperative for maintaining genome integrity. However, the factors or mechanisms involved in facilitating chromatin mobility to aid BER remain poorly elucidated, particularly in plants, which experience extensive DNA base damage due to their stationary lifestyle and oxidative stress associated with photosynthesis.

Question: APURINIC/APYRIMIDINIC ENDONUCLEASE REDOX PROTEIN (ARP) is the predominant enzyme responsible for cleaving apurinic/apyrimidinic sites in plants. Given its preferential endonuclease activity towards naked DNA, the question arises as to which chromatin-related proteins can be specifically recruited by ARP to enhance local chromatin mobility and facilitate efficient BER in plants.

Findings: We identified the plant chromatin remodeler ERCC6 and histone chaperone NAP1 as interacting partners with ARP. In a synergistic manner, ERCC6 and NAP1 contribute to the sliding of nucleosomes and exposure of hindered endonuclease cleavage sites. Loss-of-function mutations in Arabidopsis ERCC6 or NAP1 resulted in an arp-dependent hypersensitivity of plants to a toxic agent that induces BER, leading to the accumulation of apurinic or apyrimidinic sites. Furthermore, we showed that these proteins also interact with each other in yeast cells, suggesting a conserved recruitment mechanism employed by the apurinic or apyrimidinic endonuclease to overcome chromatin barriers during BER progression.

Next Steps: Future biochemical and molecular analyses will be imperative to unravel the intricate recruitment mechanisms of specific chromatin factors in distinct BER pathways at the chromatin level. This will advance our comprehension of the co-evolutionary dynamics between epigenetic machineries, their regulatory mechanisms, and chromatin architecture across diverse organisms for genome maintenance.

Reference:

Tianyi Fan, Tianfang Shi, Ran Sui, Jingqi Wang, Huijia Kang, Yao Yu, Yan Zhu (2024) The chromatin remodeler ERCC6 and the histone chaperone NAP1 are involved in apurinic/apyrimidinic endonuclease-mediated DNA repair. https://doi.org/10.1093/plcell/koae052

Linker histone H1 drives heterochromatin condensation

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He et al. explore how histone H1 drives the formation of heterochromatin foci.

https://doi.org/10.1093/plcell/koae034

Xiaoqi Feng, Institute of Science and Technology Austria

Background: To fit into the nucleus, DNA is densely packaged into structures known as nucleosomes. These nucleosomes consist of core histone proteins around which DNA is wrapped, along with linker histone protein H1, which binds to the DNA between nucleosomes. Parts of the DNA containing repetitive sequences that do not code but can jump around the genome and disrupt genes are further condensed into structures known as heterochromatin foci. These foci appear as visible, dense structures under a microscope, and maintain the silencing of repetitive sequences. H1 proteins are required for the formation of heterochromatin foci and the silencing of repetitive sequences in animals and plants.

Questions: How does H1 induce the formation of heterochromatin foci? Is the formation of heterochromatin foci essential for H1’s functions in the chromatin? 

Findings: Our study reveals that H1 condenses heterochromatin in Arabidopsis through a phase separation mechanism. This mechanism refers to the self-aggregating property of macromolecules, leading to the formation of distinct phases. A simple example of this phenomenon is the spontaneous separation of oil and water after mixing. We find that the C-terminal domain (CTD) of H1 mediates chromatin phase separation in vitro and in vivo. Without the CTD, H1 no longer drives the formation of heterochromatin foci, or performs normal functions such as regulating nucleosomal repeat length and DNA methylation. Thus, CTD-endorsed phase separation is the primary mechanism by which histone H1 promotes heterochromatin condensation or achieves its function in heterochromatin.

 Next steps: Our data also suggest that bacterial H1-like proteins, which resemble the CTD of eukaryotic H1 proteins and have been implicated in DNA condensation, can mediate phase separation. Therefore, we propose that phase separation mediated by H1 and H1-like proteins represents an ancient mechanism for compacting chromatin and DNA. Rigorous tests are required to substantiate this idea.

Reference:

Shengbo He, Yiming Yu, Liang Wang, Guohong Li, Pilong Li & Xiaoqi Feng. (2024). Linker histone H1 drives heterochromatin condensation via phase separation in Arabidopsis https://doi.org/10.1093/plcell/koae034

OsLESV cooperates with FLO6 to modulate starch biosynthesis and endosperm development

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OsLESV cooperates with FLO6 to modulate starch biosynthesis and endosperm development

Yan, Zhang, Wang et al. identify OsLESV–FLO6 as a non-enzymatic molecular module responsible for starch biosynthesis and endosperm development.

https://doi.org/10.1093/plcell/koae006

By Haigang Yan, Wenwei Zhang and Jianmin Wan

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

Background: Starch accounts for up to 75% of grain weight, and greatly affects cereal crop yield and quality. Significant advances have been made in the functional characterization of starch metabolism enzymes in cereal crops. In addition to starch metabolism enzymes, some non-enzymatic players with starch-binding domains play crucial roles in starch biosynthesis. ISOAMYLASE 1 (ISA1), a type of debranching enzyme unable to bind starch, functions in starch biosynthesis through removing superfluous branch points. However, how ISA1 is targeted to starch granules remains largely unknown.

Question: Comparable phenotypic defects between floury endosperm 9 (flo9) and isa1 prompted us to propose that LIKE EARLY STARVATION1 (OsLESV), the target protein responsible for the flo9 phenotype, might regulate rice (Oryza sativa) starch biosynthesis by associating with ISA1. Therefore, we asked whether OsLESV is a non-enzymatic player that facilitates ISA1 targeting to starch.

Findings: We determined that the rice flo9 mutant is defective in starch biosynthesis and endosperm development, similar to the reported isa1 mutants. FLO9 encodes an amyloplast-localized protein homologous to Arabidopsis (Arabidopsis thaliana) LESV. OsLESV is required for compound starch granule initiation in the endosperm. OsLESV directly binds to starch by its C-terminal Trp-rich region. We demonstrated that OsLESV interacts with the reported non-enzymatic player FLO6, and loss-of-function of either gene impairs ISA1 targeting to starch granules. Genetically, OsLESV acts synergistically with FLO6 to modulate starch biosynthesis and endosperm development. Our findings establish a molecular link between non-enzymatic players and ISA1 in rice starch biosynthesis and endosperm development.

 

Next steps: In addition to facilitating ISA1 localization on starch granules, OsLESV likely exerts other functions in starch biosynthesis and endosperm development. Therefore, it is important to identify other unknown cargos to fully understand the biological significance of OsLESV in regulating starch metabolism in future studies.

Reference:

Haigang Yan, Wenwei Zhang, Yihua Wang, Jie Jin, Hancong Xu, Yushuang Fu, Zhuangzhuang Shan, Xin Wang, Xuan Teng, Xin Li, Yongxiang Wang, Xiaoqing Hu, Wenxiang Zhang, Changyuan Zhu, Xiao Zhang, Yu Zhang, Rongqi Wang, Jie Zhang, Yue Cai, Xiaoman You, Jie Chen, Xinyuan Ge, Liang Wang, Jiahuan Xu, Ling Jiang, Shijia Liu, Cailin Lei, Xin Zhang, Haiyang Wang, Yulong Ren, and Jianmin Wan. (2023). Rice LIKE EARLY STARVATION1 cooperates with FLOURY ENDOSPERM 6 to modulate starch biosynthesis and endosperm development. https://doi.org/10.1093/plcell/koae006

Putting it together: CEPA1 functions as a Photosystem I assembly factor

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Background:

Photosystem I (PSI) is a large pigment-protein complex that participates in photosynthetic electron transfer. While its structure is well resolved, its assembly pathway is less clear.  A set of proteins mediating the step-wise assembly of PSI subunits, known as PSI assembly factors, has been previously characterized, but many key players are likely still missing.  as an entry point into the discovery of yet unknown PSI assembly factors, we screened for genes that are co-expressed with known PSI assembly factor-encoding genes in Arabidopsis.  This approach led to the identification of CO-EXPRESSED WITH PSI ASSEMBLY1 (CEPA1).

Questions:

What is the fate of PSI when CEPA1 is absent? How does CEPA1 function?

Findings:

CEPA1 is targeted to the thylakoid membranes where PSI accumulates.  Arabidopsis mutants lacking CEPA1 grow autotrophically but suffer from delayed development and exhibit pigment deficiency. This phenotype is caused by a strong decrease in PSI content.  CEPA1 does not regulate plastid PSI gene expression, but instead, acts at the post-translational level. CEPA1 associates with PSI assembly intermediates in the thylakoid membrane, and interacts with the PSI assembly factor PHOTOSYSTEM 1 ASSEMBLY3 (PSA3). The currently available data suggest a model in which CEPA1 is cleaved out of the nascent PSI complexes once its assembly function is fulfilled.

Next steps:

The precise role of CEPA1 in PSI assembly will be further studies, in particular by investigating the relationship between CEPA1 and PSA3, and by characterizing CEPA1-containing protein complexes.

Reference:

David Rolo, Omar Sandoval-Ibáñez, Wolfram Thiele, Mark A Schöttler, Ines Gerlach, Reimo Zoschke, Joram Schwartzmann, Etienne H Meyer, Ralph Bock (2024) CO-EXPRESSED WITH PSI ASSEMBLY1 (CEPA1) is a photosystem I assembly factor in Arabidopsis https://doi.org/10.1093/plcell/koae042

Regulation of leaflet number in compound leaves

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He et al. investigate the molecular mechanisms of compound leaf formation in Medicago truncatula

By Liangliang He and Jianghua Chen

https://doi.org/10.1093/plcell/koae033

Background: In the plant kingdom, leaves have different shapes, with the most noticeable difference being between simple and compound leaves. Simple leaves have a single blade, while compound leaves are made up of multiple leaflets, displaying higher complexity and diversity in form. From a developmental perspective, compound leaves are initiated as simple primordia at the flanks of the shoot apical meristem (SAM), which subsequently undergo a series of coordinated morphogenetic events to develop into a complex structure with multiple leaflets. The two most important events of this process are leaflet initiation and boundary formation. Understanding the molecular mechanisms underlying and integrating these events is of particular interest.

Question: What are the molecular mechanisms responsible for regulating and integrating these intricate developmental processes during compound leaf development?

Findings: Here, we characterized a pinnate leaf-pattern mutant pinnate-like pentafoliata2 (pinna2) in Medicago truncatula, phenotypically resembling the previously reported pinna1 mutant. Through map-based cloning, we identified the PINNA2 gene encoding a GRAS transcription factor. PINNA2 is specifically expressed at organ boundaries, including the SAM-to-organ and leaflet-to-leaflet boundaries. The PINNA2 protein directly binds to the promoter of SGL1, which encodes a leaflet initiation positive regulator, to repress its transcription. Furthermore, PINNA2 works together with two other transcription factors, PINNA1 and PALM1, to repress SGL1 expression in different leaf domains, thereby ensuring accurate leaf morphogenesis. Additionally, the expression of PINNA2 at leaflet boundaries is positively regulated by a boundary-specific protein NAM/CUC, which is crucial for leaflet boundary formation. These findings provide molecular insights into the regulation and integration of intricate developmental processes during compound leaf development.

 Next steps: Future studies will focus on defining the roles and relationships of PINNA1, PINNA2, PALM1, SGL1, MtNAM and other regulators at cellular and deeper molecular levels. Additionally, we plan to apply these genes to molecular breeding in alfalfa using gene editing techniques.

Reference:

Liangliang He, Ye Liu, Yawen Mao, Xinyuan Wu, Xiaoling Zheng, Weiyue Zhao, Xiaoyu Mo, Ruoruo Wang, Qinq Wu, Dongfa Wang, Youhan Li, Yuanfan Yang, Quanzi Bai, Xiaojia Zhang, Shaoli Zhou, Baolin Zhao, Changning Liu, Yu Liu, Million Tadege, Jianghua Chen (2024). GRAS transcription factor PINNATE-LIKE PENTAFOLIATA2 controls compound leaf morphogenesis in Medicago truncatula. https://doi.org/10.1093/plcell/koae033

Hot and SUMOylated: Heat-induced SUMOylation controls effectors in plant cells

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Li et al. examine heat-induced SUMOylation of bacteria effectors in Arabidopsis. (Plant Cell. 2024)

By Wenliang Li and Jianbin Lai (South China Normal University)

https://doi.org/10.1093/plcell/koae049

Background: Bacterial pathogens deliver effectors into plant cells to interfere with host immunity and these effectors are targeted by host cells. Environmental factors affect this interaction between bacteria and plants. SUMOylation is an important protein modification that covalently attaches small ubiquitin-related modifier (SUMO) proteins on substrates. SUMOylation increases dramatically in response to high temperatures, but its function in direct targeting of bacteria effectors is unclear in plant cells. Thus, it is valuable to study the mechanism of how heat-induced SUMOylation contributes to the interplay between plant cells and pathogen effectors under high temperatures.

Question: Are bacteria effectors SUMOylated in plant cells and how does this modification affect the interaction between bacteria and plant cells at normal and high temperatures? We tested this using Pseudomonas syringae pv. tomato (Pst) DC3000 and Arabidopsis thaliana.

Findings: Here we found that at least 16 effectors from Pst DC3000 are SUMOylation substrates in Arabidopsis thaliana. Mutation of SUMOylation sites on the effectors HopB1 and HopG1 showed that SUMOylation has different effects on the two different effectors. HopB1 function induces plant cell death by decreasing the stability of an Arabidopsis receptor kinase and SUMOylation decreased HopB1 function. HopG1 inhibits mitochondrial activity and jasmonic acid signaling in plant cells and, in contrast to HopB1, SUMOylation is essential for HopG1 function. However, heat treatment increases the SUMOylation of both HopB1 and HopG1.

Next steps: In future studies, it will be interesting to investigate the mechanisms by which SUMOylation regulates effectors in different species. The work will improve our understanding of the pathogen-plant interplay in response to environmental conditions and help us improve resistance to biotic and abiotic stresses in crops.

 Reference:

Wenliang Li, Wen Liu, Zewei Xu, Chengluo Zhu, Danlu Han, Jianwei Liao, Kun Li, Xiaoyan Tang, Qi Xie, Chengwei Yang, Jianbin Lai. (2024). Heat-induced SUMOylation affects bacterial effectors differently in plant cells. https://doi.org/10.1093/plcell/koae049

Review: Root development and symbiosis: an epigenetic perspective

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Roots do not grow in isolation but occupy a space inhabited by a variety of organisms. With certain fungi and bacteria, they form partnerships or symbiotic relationships that increase the plant’s nutrient uptake and assimilation. While the knowledge on the genetic programs required to establish these symbiotic relationships is a topic of many studies, the epigenetic regulation of the involved genes is less known. In this recent review by Zanetti et al. (2024), the authors provide a comprehensive overview of the current knowledge on epigenetic regulation of root development. Specifically, the review covers three aspects of root development, namely lateral root development, nodule formation, and symbioses with mycorrhizae, and it discusses how both DNA methylation and histone modifications act to control the relevant genes. In particular, the article highlights differences in the epigenetic regulation among different root zones, tissues, and even cell-types. The emphasis on these spatial characteristics provide interesting, novel perspective on the subject. Finally, the authors argue for more research towards unravelling the epigenetic regulation of root system architecture and symbiosis, especially with respect to the role of chromatin remodelling and histone modifications, to better understand the underlying drivers for the enormous phenotypic plasticity demonstrated by a plant root. (Summary by Thomas Depaepe @thdpaepe). Plant Physiology 10.1093/plphys/kiae333