SKIPping over JAZs to improve seed maturation and viability

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Vishal Varshney and Manoj Majee, National Institute of Plant Genome Research (NIPGR), Aruna Asaf Ali Marg, New Delhi 110067, India

https://doi.org/10.1093/plcell/koad199

Vishal Varshney et al. investigate the F-box protein SKIP31 in Arabidopsis, revealing a role for this protein in seed maturation, with potential applications in modulating seed vigor.

Background: Seed maturation is a highly complex physiological program during which seeds acquire adaptive features such as seed desiccation tolerance and deposition of seed storage reserves. These features allow seeds to extend their viability and germinability while remaining in a desiccated state for long periods of time. To achieve this feat, seeds engage multi-layered regulatory networks that activate many genes involved in various mechanisms that ultimately improve seed survival and vigor upon maturity. Among these networks, the phytohormone abscisic acid (ABA) and ABA-responsive master regulators play a key role in modulating seed maturation.

Question: The regulatory role of Jasmonate ZIM domain (JAZ) proteins was recently reported in repressing ABA signaling by suppressing ABSCISIC ACID INSENSITIVE3 (ABI3) and ABI5 transcriptional activity during germination. However, how ABI-related transcription factors are repressed by JAZ and how the ABA signaling is de-repressed during seed maturation is unclear.

Findings: We identified the SKIP31–JAZ–ABI5 module as a regulator of seed maturation and seed vigor in Arabidopsis. We show that SKIP31, an F box protein, targets JAZ proteins for proteasomal degradation in a jasmonate (JA)-isoleucine (Ile)-independent manner to alleviate the inhibition imposed by JAZ proteins on ABI5. ABA-mediated downstream signaling thus becomes activated, which is essential for seed maturation, desiccation tolerance and establishment of seed vigor and viability.

Next step: We will test whether other transcription factors and/or regulatory proteins besides ABI5 contribute to the SKIP31–JAZ–ABI5 module to regulate seed maturation. Additionally, we will ask if SKIP31 influences JA-Ile-dependent regulation of the JAZ–MYC module in the JA signaling pathway and JA responses.

Reference:

Vishal Varshney, Abhijit Hazra, Venkateswara Rao, Shraboni Ghosh, Nitin Uttam Kamble, Rakesh Kumar Achary, Shikha Gautam, Manoj Majee (2023) The Arabidopsis F-box protein SKIP31 modulates seed maturation and seed vigor by targeting JAZ proteins independently of jasmonic acid-isoleucine. https://doi.org/10.1093/plcell/koad199

A New Look at Virus Movement: An Unexpected Role of dsRNA-Induced Immunity

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Huang et al. investigate the mechanisms of dsRNA-induced pattern-triggered immunity against viruses.

https://doi.org/10.1093/plcell/koad176

Manfred Heinlein (Institut de biologie moléculaire des plantes, CNRS, Université de Strasbourg, 67000 Strasbourg, France)

Background: Plants use different defense mechanisms against pathogens. The major mechanism that plants use for defense against viruses is known as RNA silencing. This mechanism is triggered by the presence of viral double-stranded (ds)RNA and uses small RNAs to inhibit viral replication by targeting the viral genome for degradation. Recently, it was found that dsRNA elicits antiviral defense also through a protein-mediated mechanism known as pattern-triggered immunity (PTI). However, the underlying mechanism of antiviral PTI and how viruses overcome this plant defense mechanism to cause infection is unknown.

Question: In this study we asked how dsRNA-induced PTI acts to inhibit virus infection and whether we can identify components of the PTI signaling pathway. Moreover, we wanted to know how viruses overcome this plant host defense response in order to cause infection.

Findings: We demonstrate that dsRNA-induced PTI targets plasmodesmata (PD), the intercellular communication conduits in plant cell walls that viruses use to spread infection from cell to cell. By inducing the deposition of callose, dsRNA-induced PTI reduces PD permeability, thus restricting virus movement. We identified PTI signaling components required for dsRNA-induced PD callose deposition and delineate a PTI pathway showing important difference to PTI pathways triggered by microbial elicitors. Moreover, viral movement proteins (MPs) suppress the dsRNA-induced callose deposition response at PD.  This leads to a model of how plant immune signaling constrains virus movement and how viruses counteract this layer of immunity.

Next steps: This study calls upon the identification of the PTI dsRNA receptor and the mechanisms of PTI signaling (involving identified components such as SERK1, BIK1, calcium channels, CML41, PDLP1/2/3) and PTI suppression by MPs, and how dsRNA-induced PTI and RNA silencing are controlled during the spread of infection.

Reference:

Caiping Huang, Ana Rocio Sede, Laura Elvira-González, Yan Yan, Miguel Rodriguez, Jerome Mutterer, Emmanuel Boutant, Libo Shan, and Manfred Heinlein.. (2023). dsRNA-Induced Immunity Targets Plasmodesmata and is Suppressed by Viral Movement Proteins https://doi.org/10.1093/plcell/koad176

Guard Cell Walls: Who Calls the Shots?

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Zheng et al. demonstrate that polar stiffening of guard cell walls is essential for stomatal functioning.

By Lin Zheng and Hongzhi Wang

Beijing Key Laboratory of Agricultural Genetic Resources and Biotechnology, Institute of Biotechnology, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China

https://doi.org/10.1093/plcell/koad19

Background: Stomata, tiny pores on plant leaves, control gas exchange between plants and their environment. The functioning of stomata relies on the properties of guard cell walls. Traditional thinking suggests that the difference in thickness between inner and outer cell walls is crucial, but a recent idea highlights the importance of reinforced stiffness in the polar regions of the guard cell walls. However, the genes responsible for these wall properties are unknown. Thus, the mechanics of stomatal movement remain a mystery.

Question: What property of guard cell walls is vital for proper functioning, and can we manipulate it through genetic engineering?

Findings: The stiffness of guard cell walls, particularly in polar regions, is crucial for stomatal movement. An important player in this process is the MYB156 transcription factor in Populus. By regulating the activity of the pectin methylesterase 6 (PME6), MYB156 influences the amount of de-esterified pectin in the polar regions of guard cell walls, thereby affecting their stiffness. Loss of MYB156 leads to increased polar stiffness, causing stomata to respond more swiftly to various stimuli. Conversely, excessive expression of MYB156 decreases polar stiffness and impairs stomatal movement. The polar stiffening of guard cell walls plays a significant role in responding to environmental changes. This study sheds light on the mechanical properties of guard cell walls during stomatal movement, with the potential to enhance plant drought tolerance by engineering this specific property.

Next steps: Our research suggests that by enhancing polar stiffening, we can improve the performance of guard cells and plant drought tolerance. Genetic engineering techniques can be employed to target the MYB156 gene and enhance the function of guard cells. Additionally, further investigation into how polar stiffening is affected in mutated guard cells can reveal additional players involved in this process.

 Reference:

Lin Zheng, Yajuan Chen, Liping Ding, Ying Zhou, Shanshan Xue, Biying Li, Jianhua Wei and Hongzhi Wang (2023). The transcription factor MYB156 controls the polar stiffening of guard cell walls in poplar. https://doi.org/10.1093/plcell/koad19

The Molecular Switch Governing the Heat Stress Response in Wheat

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Wang et al. explore how SUMOylation of a key transcription factor affects heat stress responses in wheat.

https://doi.org/10.1093/plcell/koad192

By Jie Liu and Haoran Wang; Frontiers Science Center for Molecular Design Breeding, Key Laboratory of Crop Heterosis and Utilization (MOE), Beijing Key Laboratory of Crop Genetic Improvement, College of Agronomy and Biotechnology, China Agricultural University, Beijing 100193, China

Background: In response to high temperature, plants use transcription factors to initiate protective responses; as they acclimate to extended high temperature, the plants then turn off these rapid responses. The heat shock-associated transcription factor HsfA1 plays a central role in sensing heat stress and promoting rapid transcriptional responses. At normal temperatures, HsfA1 is associated with heat shock proteins such as HSP70 and HSP90, which repress its protein activity; at high temperature, these proteins rapidly release HsfA1 to initiate heat stress responses. In addition to this well-known OFF-to-ON switch for HsfA1 activity, additional ON-to-OFF mechanisms must exist to complete the HsfA1 cycle during acclimation to long-term heat stress. Here we explored how the ON/OFF molecular regulation of HsfA1 activity occurs in wheat (Triticum aestivum).

Question: How is the transcriptional activation activity of HsfA1 regulated when it is released from multichaperone repression complexes during prolonged periods of high temperatures?

Findings: Genetic evidence revealed that TaHsfA1 is required for basal and acquired thermotolerance as well as normal heat-induced transcriptional reprogramming in wheat. TaHsfA1 is modified by the small peptide SUMO predominantly at its 459th amino acid (lysine, K459). SUMOylated TaHsfA1 proteins were detected at the early stage of heat stress treatment, but their levels decreased upon prolonged thermal stress. Consistent with these observations, heat stress–responsive genes were highly induced at the beginning of heat shock but were downregulated and returned to basal expression levels during long-term thermal stress. These findings support a role for the thermosensitive SUMOylation of TaHsfA1 in controlling TaHsfA1 activity and dynamic heat stress responses at different stages of thermal stress.

Next steps: We plan to introduce the K459-mutated (non-SUMOylated) form of TaHsfA1 into wheat Tahsfa1 mutants to evaluate the importance of TaHsfA1 SUMOylation in sensing heat stress and regulating responses in cereal crops. In addition, we plan to look for the protein components responsible for TaHsfA1 de-SUMOylation during long-term thermal stress.

Reference:

Haoran Wang, Man Feng, Yujie Jiang, Dejie Du, Chaoqun Dong, Zhaoheng Zhang, Wenxi Wang, Jing Liu, Xiangqing Liu, Sufang Li, Yongming Chen, Weilong Guo, Mingming Xin, Yingyin Yao, Zhongfu Ni, Qixin Sun, Huiru Peng and Jie Liu. (2023). Thermosensitive SUMOylation of TaHsfA1 defines a dynamic ON/OFF molecular switch for the heat stress response in wheat https://doi.org/10.1093/plcell/koad192

Review: Till death do us pair: Co-evolution of plant–necrotroph interactions

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This interesting and well-written review by Derbyshire and Raffaele takes a step back from the molecular interactions between plant and pathogen and discusses them in light of co-evolutionary processes. The review starts with a useful introduction and definition of concepts about “robustness” in biological systems, including multifunctionality, modularity, and compartmentalization, as well as the difference between degeneracy and robustness. The authors then apply these concepts to draw lessons about the co-evolutionary interactions between plants and necrotrophic pathogens, including that although programmed cell death is an effective strategy to combat biotrophic pathogens, it benefits necrotrophic pathogens, which obtain nutrients from dead tissues. I particularly enjoyed the discussion of the molecular factors that contribute to specialization versus generalism, such as the idea that heterogeneous host environments promote degeneracy in pathogen virulence genes.  There’s also an interesting discussion about the spatial and cell-type specific interactions that are being illuminated by single-cell sequencing. (Summary by Mary Williams @PlantTeaching) Curr. Opin. Plant Biol. 10.1016/j.pbi.2023.102457

Spotlight: Super-pangenomes for improved breeding

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Sometimes more really is better, and I think it’s safe to say that when it comes to genomic information, more is better. Here, Raza et al. highlight the great value of super-pangenomes. A pan-genome is defined as the entire set of genes within a species, created by combining sequences of many individuals. The super-pangenome as defined here expands this concept to incorporate genomes of close relatives, up to the genus level. This idea is particularly useful as a way to incorporate traits from crop wild relatives into breeding programs. Crop wild relatives often are sources of genes the provide environmental robustness that has been lost through selection for yields, but introgressions of these valuable traits can be difficult because of structural variations that have arisen over time. The authors cite examples of super-pangenome assemblies that have been developed for rice, soybean, and tomato, and how these resources have allowed the identification of several novel genes. Several strategies for breeding using information from super-pangenomes is also discussed. (Summary by Mary Williams @PlantTeaching) Mol. Plant 10.1016/j.molp.2023.08.005

Chloroplast proteostasis prevents aggregation of Huntington’s disease-causing human polyQ protein

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Certain human neurodegenerative disorders are caused by aggregation of disordered proteins. In particular, Huntington’s disease is caused by aggregation of a protein called huntingtin, which contains long stretches of glutamine (Q). Llama et al. observed that proteins with long stretches of glutamine are also present in plants, but they do not seem to cause disease. To investigate how plants control aggregation of these polyQ-containing proteins, the authors generated transgenic Arabidopsis thaliana expressing a fragment of human huntingtin labelled with a fluorophore. Using confocal microscopy, they observed that huntingtin remains soluble in plant cells in normal growth conditions but becomes aggregated under heat stress. They found that the expressed protein interacts with components of chloroplast protein import and chloroplast proteases, and that impairment of these chloroplast functions caused aggregation of huntingtin in plant cells. Thus, the authors concluded that plants use chloroplast proteostasis to control aggregation of polyglutamine proteins. Expression of a chloroplast protease, the chloroplast stromal processing peptidase (SPP), can also prevent aggregation of huntingtin both in a human cell line and in nematodes. This work presents plant chloroplast proteostasis as a novel path towards developing treatments for human neurodegenerative diseases. (Summary by Ángel Vergara @ngelVerCru) ) Nature Aging 10.1038/s43587-023-00502-1

Altering chloroplast biogenesis leads to increased yields in rice

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Transcription of chloroplast genes is carried out by the plastid encoded polymerase (PEP) with help from PAPs (PEP-associated proteins). PAP3 is important for chloroplast development in Arabidopsis thaliana and Nicotiana benthamiana, however its role in crops has not been fully elucidated. Here Seo et al. transformed rice to express OsPAP3 under the constitutively active 35S promoter. These plants had a 40-fold increase in PAP3 expression and were greener due to a significant increase in chlorophyll content. To assess the effect of PAP3 overexpression on chloroplast development, they quantified chloroplast number in one-week old protoplasts. For wild type plants there were approximately 14 chloroplasts per protoplast, whilst for the overexpression lines chloroplast number increased and there was an average of 21 chloroplasts per protoplast. To see if this caused an increase in plant productivity, the overexpression lines were grown in a paddy field for three consecutive years, and it was found that these plants had a 18-30% increase in yield. Hence altering chloroplast biogenesis could be an effective strategy to increase yields in crops. (Summary by Rose McNelly @Rose_McN) Plant Physiol. 10.1093/plphys/kiad536

Staining starch granules in living plants

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Starch granules are synthesized in the leaves of chloroplast during the day and degraded in the subsequent night. To visualise starch granules the tissue usually has to be fixed, which prevents live imaging. Here Ichikawa et al. set out to find a highly specific dye to image starch granules in living tissues. They tested a range of fluorescent dyes on Arabidopsis thaliana leaves and found that fluorescein stained granular structures in the mesophyll, guard cells and root tip. To test whether these were starch granules, they treated plants expressing the genetically encoded starch granule marker GBSSI-tagRFP (GRANULE BOUND STARCH SYNTHASE-RED FLUORESCENT PROTEIN) with fluorescein. The fluorescein signal overlapped with the RFP signal, confirming that fluorescein stains starch granules. The authors tested whether fluorescein could be used in other species and found it successfully stained starch granules in the bryophyte Marchantia polymorpha, and other flowering plants including strawberry, tomato and lettuce. Hence fluorescein provides an easy way to image starch granules in different species. (Summary by Rose McNelly @Rose_McN) Plant Physiol.10.1093/plphys/kiad528