TaGW2 regulates drought tolerance in wheat

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Li, Zhang, Liu et al. demonstrate that the E3 ligase TaGW2 enhances wheat drought tolerance by promoting the degradation of the transcription factor TaARR12.

https://doi.org/10.1093/plcell/koad307

By Shumin Li, Zhensheng Kang and Hude Mao

State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University, Yangling, Shaanxi 712100, China.

Background: Drought limits crop yield, a particular concern in the context of climate change. However, the molecular modulators and mechanisms underlying the trade-off between drought tolerance and crop growth and development remain elusive. The E3 ligase Grain width and weight2 (TaGW2) regulates kernel size and weight in wheat (Triticum aestivum). Genetic variants in TaGW2 are associated with wheat drought tolerance, indicating that TaGW2 may maintain the balance between stress responses and high yield in wheat. However, the molecular mechanism(s) through which TaGW2 regulates kernel size remain unclear, as does its possible role in wheat stress responses.

Question: Is TaGW2 involved in wheat drought stress responses? If so, how does it function?

Findings: We demonstrate that TaGW2 promotes wheat drought tolerance, but limits kernel size and weight. TaGW2 directly interacts with the transcription factor TaARR12 and promotes its degradation. In contrast to TaGW2, TaARR12 represses drought tolerance but does not appear to influence kernel size and yield in wheat. Notably, TaARR12 knockdown in the tagw2 knockout mutant enhances drought tolerance and grain yield compared to wild-type plants. These findings show that the TaGW2–TaARR12 regulatory module is essential for drought responses, providing a strategy for improving stress resistance in high yield wheat varieties.

Next steps: TaGW2 is a pivotal regulator of both kernel development and drought responses in wheat. Future work will aim to identify additional regulatory targets of TaGW2 and study their functions in kernel development and stress responses. We will also explore the potential application of a TaGW2 and TaARR12 double mutant for improving drought tolerance in high yield wheat varieties.

Reference

Shumin Li, Yifang Zhang, Yuling Liu, Peiyin Zhang, Bin Chen, Li Ding, Xuemin Wang, Yingxiong Nie, Fangfang Li, Zhenbing Ma, Linying Du, Zhensheng Kang, Hude Mao. (2024). The E3 ligase TaGW2 mediates transcription factor TaARR12 degradation to promote drought tolerance in wheat. https://doi.org/10.1093/plcell/koad307

RNA composition of Processing Bodies

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Liu et al. explore the RNAs present in processing bodies, a cytoplasmic subcellular condensate.

 Andriani Mentzelopoulou

Department of Biology, University of Crete, Heraklion, Greece

Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology–Hellas, Heraklion, Greece

 Panagiotis Moschou

Department of Biology, University of Crete, Heraklion, Greece

Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology–Hellas, Heraklion, Greece

Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, Uppsala, Sweden

https://doi.org/10.1093/plcell/koad288

Background: Interactions between proteins and nucleic acids can promote the generation of droplet-like ribonucleoprotein condensates. One example of a condensate is Processing Bodies (PBs), which are found in the cytoplasm and contain many proteins and RNA molecules. Previously, we defined the proteins residing in Arabidopsis thaliana PBs using an approach known as proximity biotinylation, which can capture weak and transient interactions, such as those occurring in condensates. We did that in two conditions, normal conditions, and heat stress, showing that PBs are highly dynamic. This approach allowed us to identify a link between the core PB component known as DECAPPING 1 (DCP1) and the SCAR/WAVE actin nucleating complex.

Question: Having defined the PB proteome, we asked whether the proximity biotinylation approach can also be used to capture associated RNA molecules and what kind of RNA molecules reside in PBs.

 Findings: Herein, we used Arabidopsis thaliana seedlings and especially roots. We showed that the proximity biotinylation approach can indeed capture RNAs stably to more transiently associated with the PBs. These mainly include RNAs involved in cell wall development and regeneration, plant hormonal signaling, secondary metabolism/defense, and RNA metabolism. Furthermore, we showed that RNAs in PBs follow different paths: in small PBs, RNAs get degraded; in larger PBs, RNAs are stored. The stored RNAs are not translated until the actin-related SCAR/WAVE complex dissolves PBs and releases specific RNAs. One example of such RNA is WOUND INDUCED DEDIFFERENTIATION 1/RELATED TO AP2 4 (RAP2.4), which affects responses to the phytohormone ethylene.

Next steps: We could use the findings from this study to define PB functions in a cell-specific manner during development of the Arabidopsis root. The approaches developed here can also be used to decipher the composition of numerous other condensates.

Reference:

Chen Liu, Andriani Mentzelopoulou, Ioannis H. Hatzianestis, Epameinondas Tzagkarakis, Vassilis Scaltsoyiannes, Xuemin Ma, Vassiliki A. Michalopoulou, Francisco J. Romero–Campero, Ana B. Romero–Losada, Panagiotis F. Sarris, Peter Marhavy, Bettina Bölter, Alexandros Kanterakis1, Emilio Gutierrez–Beltran, Panagiotis N. Moschou (2023) A proxitome-RNA-capture approach reveals that processing bodies repress co-regulated hub genes https://doi.org/10.1093/plcell/koad288

 

mRNA处理小体的RNA构成

蛋白质和核酸之间的相互作用促进了液滴状核糖核蛋白（RNP）凝聚体的形成。mRNA处理小体（PBs）就是细胞质中的一类凝聚物。这些mRNA处理小体中富含蛋白质和 RNA 分子。我们在之前的研究中曾使用一种能捕捉微弱且短暂的蛋白相互作用（如在凝聚体中发生的相互作用）的方法（即邻近生物素标记技术）来解析富集在 mRNA处理小体中的蛋白质组。我们比较了正常条件和热胁迫条件下的RNA-seq数据，结果表明 mRNA处理小体具有高度动态性。通过这种方法，我们确定了 mRNA处理小体的核心部件脱帽蛋白1-DECAPPING 1 (DCP1) 与 SCAR/WAVE 肌动蛋白成核复合体之间的紧密联系。

 

在解析了 PBs 的邻近蛋白质组之后，我们尝试研究邻近标记技术是否也能用于捕获与之关联的 RNA 分子，以及哪些类型的 RNA 分子聚集于mRNA处理小体中。

在本文中，我们以拟南芥幼苗（尤其是它的根）作为材料，揭示了邻近标记技术确实可以捕获与PBs稳定或瞬时相关的RNAs。其中主要包括参与细胞壁发育和再生、植物激素信号转导、次生代谢/防御以及RNA代谢的RNAs。实验还发现，mRNA处理小体PBs 中的 RNAs有不同的命运：在小的PBs中，RNAs 通常会被降解，而在大的PBs中，RNAs 会被储存起来。储存的 RNA不会被翻译，直到肌动蛋白相关复合物 SCAR/WAVE 促使PBs解体并释放出特定的 RNA。伤口诱导去分化 1（WOUND INDUCED DEDIFFERENTIATION 1）/AP2.4相关蛋白（RELATED TO AP2 4（RAP2.4））就是这类 RNA的一个例子，它影响植物对乙烯的应答。

该研究结果可用于以细胞特异性的方式沿着发育的拟南芥根轴来确定mRNA处理小体PBs 的功能。而该研究提出的方法可用于破译许多其他类似凝聚体的构成。

凝聚体、液液相分离、邻近标记技术、乙烯

 

Barley MLA3 recognizes the blast effector Pwl2, an effector involved in host range dynamics

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Brabham et al. explore the mechanisms of resistance to fungal pathogens in barley.

Helen J. Brabham1,2, Diana Gómez De La Cruz1, Matthew J. Moscou,3

1The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, Norwich, NR4 7UH, UK

22Blades, 1630 Chicago Avenue, Suite 1312, Evanston IL 60201, USA

3USDA-ARS, Cereal Disease Laboratory, St. Paul, MN 55108, USA

https://doi.org/10.1093/plcell/koad266

Background: Nucleotide-binding leucine-rich repeat (NLR) proteins are intracellular immune receptors that recognize molecules from plant pathogens, known as effectors. The majority of NLRs confer resistance to one pathogen by recognizing a specific effector. In barley (Hordeum vulgare), the Mla locus contains multiple NLR genes and alleles of the NLR Mla recognize Blumeria graminis, the causal agent of powdery mildew. In the barley cultivar Baronesse, resistance to the blast pathogen Magnaporthe oryzae has been mapped to the Mla locus, but the causal gene within this locus is unknown.

Question: How is the barley cultivar Baronesse resistant to multiple pathogens? Which gene in the Mla locus provides resistance to the rice blast pathogen? Does the Mla allele Mla3 in Baronesse recognize M. oryzae in addition to B. graminis? What effector is being recognized from M. oryzae?

Findings: We show that the barley NLR MLA3 recognizes the effector Pwl2 from M. oryzae. Resistance to blast disease was mapped to the Mla locus. Three candidate genes were cloned and introduced into a susceptible barley cultivar. Infection assays with M. oryzae in transgenic barley lines found that only barley carrying Mla3 showed resistance and required multiple copies. To identify the M. oryzae effector recognized by Mla3, mutants were generated by randomly knocking genes out in M. oryzae using UV mutagenesis. Sequencing mutants found that the effector gene PWL2 was always lost. PWL2 was first discovered in 1995, as it prevents blast isolates from infecting weeping lovegrass (Eragrostis curvula). MLA3 was shown to directly recognize and associate with Pwl2 through expression and protein-protein assays.

Next steps: The main question that remains to be addressed is how does MLA3 recognize M. oryzae and B. graminis? Future efforts will involve finding the molecular principles of Pwl2 recognition by MLA3 and identifying the recognized effector of B. graminis to understand the mechanism by which MLA3 recognizes multiple pathogens.

Reference:

Helen J. Brabham, Diana Gómez De La Cruz, Vincent Were, Motoki Shimizu, Hiromasa Saitoh, Inmaculada Hernández-Pinzón, Phon Green, Jennifer Lorang, Koki Fujisaki, Kazuhiro Sato, István Molnár, Hana Šimková, Jaroslav Doležel, James Russell, Jodie Taylor, Matthew Smoker, Yogesh Kumar Gupta, Tom Wolpert, Nicholas J. Talbot, Ryohei Terauchi, Matthew J. Moscou (2023) Barley MLA3 recognizes the host-specificity effector Pwl2 from Magnaporthe oryzae. https://doi.org/10.1093/plcell/koad266

Review. Chloroplast ATP synthase: From structure to engineering

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I remember how amazed I was the first time I saw an animation of ATP synthase doing its job. This fantastic engine is largely conserved across the domains of life, with some variation as highlighted in this review of the chloroplast ATP synthase by Rühle et al. The plastid form is a rotary form, written as cF1F0. The cF0 subunit is embedded in the thylakoid membrane, whereas the cF1 subunit protrudes into the stroma. Protons move through it (driven by proton-motive force generated by photosynthesis) from within the lumen across the membrane into the stroma, and their movement is coupled with the phosphorylation of ADP to ATP. The review is divided into three parts: structure, assembly, and engineering, and I particularly enjoyed the discussion of how the chloroplast enzyme is regulated by redox, pH, and in turn regulates the light reactions including the balance between cyclic and linear electron flow and PSII and PSI activities. Because of the intricate connection between protons, electrons, light reactions and ATP, efforts to make the ATPase more efficient are challenging but intriguing. However, given the many efforts to improve other components of photosynthetic machinery, such as the introduction of carbon-concentrating mechanisms, understanding how such efforts might need to also be supported through engineering the chloroplast ATPase is critical. Note that this review is part of an upcoming Plant Cell Focus Issue on Photosynthesis. (Summary by Mary Williams @PlantTeaching) Plant Cell 10.1093/plcell/koae081

Review: Evolution of ROS targets for plant development

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Reactive oxygen species (ROS) are agents of damage but also potent signals. Here, Singh et al. review the cellular targets that support ROS signaling across the green kingdom. Many of the signaling roles for ROS have been uncovered in Arabidopsis and other angiosperms, so it is interesting to look at their presence in other plant types. Most of the ROS signaling targets are present in green algae and thus predate terrestrialization, but there has also been a notable diversification of these gene families in terrestrial plants. The article has a particular focus on the roles of ROS in root and leaf developmental programs, and how they interact with phytohormones. (Summary by Mary Williams @PlantTeaching) Trends Plant Sci. 10.1016/j.tplants.2024.03.005

Review. From stressed to success: Unveiling the secret memory of gymnosperms

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Epigenetic stress memory in gymnosperms is the topic of a new review by Fossdal et al. Gymnosperms are long-lived, cone-bearing, tough trees, known to tolerate episodic stress. Their adaptive traits to stress are not passed on in a straightforward way, conforming to classical Mendelian inheritance. Instead, adaptive responses in gymnosperms are a result of epigenetic changes, including DNA methylation, histone modification, and small RNAs, which enable dynamic changes in gene expression, thus, phenotypic expression. As an example of a epigenetic-controlled trait, in Norway spruce tree (Picea abies) the epigenetic memory of photoperiod and temperature experienced during embryogenesis and seed development influences bud phenology and the progenies’ frost tolerance many years later. The authors also highlight that most of our understanding of epigenetic regulations in plants comes from angiosperms, flowering plants. Studying epigenetic regulation in gymnosperms is more challenging due to their long lifecycle, rendering patterns of inheritance difficult to observe. Furthermore, the woody structure of gymnosperms makes the use of conventional nucleotide extraction methods less effective, and the only existing high quality reference genome belongs to Chinese pine (Pinus tabuliformis). Therefore, Fossdal et al., emphasize the need of improved sequencing technologies to decipher the large genomes of gymnosperms. (Summary by Kumanan N Govaichelvan, @NGKumanan) Plant Physiol. 10.1093/plphys/kiae051/7595554

Making genome editing a success story in Africa

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The introduction of CRISPR-Cas technology in 2012 marked a significant advancement in global genome editing, yet its potential remains largely untapped in Africa, where it could address crucial challenges in agriculture, public health, and medicine. However, several obstacles hinder its full realization, as addressed in this article by Abkallo et al. These include regulatory uncertainty, limited access to laboratories, equipment, reagents, and overall funding. Additionally, there is a shortage of skilled professionals and insufficient public support, resulting in a lack of political will for change. To overcome these challenges, various solutions have been proposed. These include establishing incentive programs to retain talent, increasing public awareness and education to facilitate informed decision-making, developing GMO regulatory frameworks and harmonizing them across the continent, and encouraging private investment. Furthermore, funding from global bodies such as the World Health Organization should be utilized to establish infrastructure suitable for genome-editing technologies. By implementing these measures, Africa can unlock the transformative potential of genome editing, fostering innovation and development throughout the continent. (Summary by Villő Bernád) Nature Biotech. 10.1038/s41587-024-02187-2

Viewpoint: Unheard voices from the Global South speak up

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For many reasons, the voices of researchers from the Global South often go unheard. Many of these reasons are financial; big international conferences are frequently held at places that require distant travel, and registration and travel fees can be beyond the reach of modestly-funded scientists.  Visa challenges and systemic biases also contribute. In 2023, Auge and Estévez coordinated a concurrent symposium at the International Conference on Arabidopsis Research (ICAR) to highlight these unheard voices. In this article, the authors further amplify the voices of the symposium speakers but also the impediments to their being heard, and they provide recommendations to secure greater diversity in academic conferences. (Summary by Mary Williams @PlantTeaching) J. Exp. Bot. 10.1093/jxb/erae027

Thylakoid membrane remodelling during the dark-to-light transition

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In the dark, plants modify thylakoid stacking to alter electron transport and reduce photodamage. More photosystem II (PSII) is located in thylakoids within stacked grana, which promotes cyclic electron transport. Upon light exposure, there is granal unstacking, which increases the amount of linear electron transport for carbon assimilation. Here Garty et al. used freeze fracture cryo scanning electron microscopy and transmission electron microscopy to study thylakoid membrane structure during the dark-to-light transition at high resolution. They categorized thylakoids in wild type Arabidopsis thaliana leaf chloroplasts into four groups – singular thylakoids exposed to the stroma on both sides, thylakoids within a granal stack, those on the edge of a granal stack and those in a thylakoid pair, which they called ‘stacked thylakoid doublets’. On the dark-to-light transition, the percentage of thylakoids in granal stacks decreased from 44% to 33%, whilst the percentage of stacked thylakoid doublets increased from 13% to 26%. Modelling these changes showed that the formation of stacked thylakoid doublets increased the fraction of PSII in proximity to PSI from 0.44 to 0.59, this allowed for more efficient linear electron transport. Hence, this study provides the first observations of stacked thylakoid doublets which are an ideal platform for linear electron transport. (Summary by Rose McNelly @Rose_McN) Nature Plants 10.1038/s41477-024-01628-9