Characterization of pyrenoid-based CO2-concentrating mechanism in hornworts

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Pyrenoids are structures that concentrate carbon dioxide around Rubisco, most commonly studied in green algae such as Chlamydomonas. However, hornworts, one of the three types of bryophytes (along with liverworts and mosses) also have a pyrenoid-based CO2-concentrating mechanism (pCCM), unique among land plants. Here, Robison et al. characterize the pCCM in the model hornwort Anthoceros agrestis. The authors used electron microscopy and live-cell imaging to visualize the hornwort pCCM. They noted some differences from the pCCM of Chlamydomonas, including that hornworts have multiple pyrenoids in each chloroplast, in contrast to the single pyrenoid in Chlamydomonas. They further showed that the hornworts lack the starch sheath present in algal pyrenoids. They also used co-IP and fluorescent reporters to identify and characterize several pyrenoid-specific proteins, noting that many are present in the hornwort pCCM, but that the linker protein EPYC1 seems to be missing. As the authors report, characterizing the pCCM in hornworts provides new opportunities to engineer such structures in crops and other land plants. (Summary by Mary Williams @PlantTeaching) bioRxiv https://doi.org/10.1101/2024.06.26.600872

Tissue-specific interference reveals complex roles for auxin signalling in procambial cells during graft healing in Arabidopsis

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For hundreds of years, we have propagated plants clonally by grafting, i.e. the union of a scion and a rootstock to form a new plant. To be successful, a graft junction must heal: tissues must attach, and vascular bundles reconnect, in a process known to involve auxin. Here, Serivichyasw at et al. investigate the role of auxin signalling in different tissues during graft healing in Arabidopsis thaliana. The authors developed a platform for disturbing auxin signalling in an inducible, tissue-specific manner using promoter sequences of genes with cell type-specific expression patterns driving bdl, a nonfunctional BODENLOS/IAA12 allele that disturbs auxin signalling. Among the tested tissues, lines with procambium- and phloem precursor-localised expression of bdl saw the strongest losses in graft healing. Procambial cells expressing bdl caused failure of tissue attachment and phloem reconnection in grafts, much like what is seen for bdl-2 loss-of-function mutant lines. Although tissue attachment was successful in phloem precursor-specific bdl expression lines, phloem development in these grafts was impaired, suggesting the two processes are somewhat independent. Disturbing auxin signalling in the procambium also affected the critical callus formation stage of graft healing. Along with new insights into the biology of grafting, the expression platform developed herein could be used to better spatially resolve the role of auxin in other plant developmental processes. (Summary by John Vilasboa @vilasjohn) Plant Physiol. 10.1093/plphys/kiae257

Rice tiller production regulated by sustained expression of FON1

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Number of tillers is one of the major determinants of yield in rice. MONOCULM1 (MOC1) and MOC3 have been reported to regulate tiller formation by promoting axillary bud formation and elongation of buds. MOC1 interacts with MOC3 and promotes the expression of FLORAL ORGAN NUMBER 1 (FON1), which increases the elongation of buds and ultimately promotes tillering. MOC3 can directly bind to the promoter of FON1, but MOC1 cannot directly bind to FON1 and acts as a co-activator of MOC3. Fan et al. discovered the function of a novel gene DWARF AND LESS TILLER ON CHROMOSOME 3 (DLT3), which interacts with MOC3, recruits MOC1, and binds to the promoter of FON1. They cloned DLT3 from a mutant developed from an EMS mutagenized population and performed Mutmap sequencing to find its candidate gene, whose function was validated by complementation assay and CRISPR genome editing. They found the potential interaction of DLT3 with MOC3 in a yeast two-hybrid screen and validated it through biomolecular fluorescence complementation. This discovery has added a new player, DLT3, to the previously known tiller regulating molecular circuit FON1-MOC3-MOC1. (Summary by Asif Ali @pbgasifkalas) Plant Physiol. 10.1093/plphys/kiae367

The white lupin trehalase gene regulates cluster root formation and function under phosphorus deficiency

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Phosphorus (P) is an essential nutrient for plant growth and development. Under P deficiency, white lupin develops cluster roots (CR), specialized root structures that enhance soil exploration and nutrient acquisition. While sugar signaling, particularly sucrose, has been shown to play a role in the establishment of CR, other CR-associated features such as the root exudation of citrate and malate are independent of sucrose. Therefore, a key sugar signaling component specific to CR function remains to be identified. Using a combination of pharmacological and genetic studies, Xia and colleagues demonstrated that trehalose plays a critical role in both CR establishment and organic acid metabolism. Specific inhibition of trehalase, the only enzyme that catalyzes trehalose catabolism, by validamycin A, promotes trehalose accumulation and CR formation under P deficiency conditions. Similarly, silencing the TREHALASE1 gene also promotes CR formation, while overexpressing the gene leads to an opposite effect. This study sheds light on the close association between trehalose metabolism and P starvation response in plants. (Summary by Ching Chan @ntnuchanlab) Plant Physiology 10.1093/plphys/kiae290

Pathogen cyclic lipopeptide virulence factors promote disease by inducing membrane leakage

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Pathogens deploy an array of molecules to create favorable conditions and promote infections in host plants. These molecules are well-known for suppressing host immunity, rendering them more susceptible. However, two recent reports suggest that some pathogen-produced virulence factors may also act independently of host immune suppression. Central to this are a class of molecules known as cyclic lipopeptides. In Cell Reports, Brauer et al. studied gramillin, secreted by the fungal pathogen Fusarium graminearum (causal agent of fusarium head blight), whereas in Nature Communications, Getzke and Wang et al. reported brassicapeptin A from the opportunistic bacterial pathogen Pseudomonas brassicacearum R401. Interestingly, both cyclic lipopeptides disrupt ionic balance in host plants through pore formation, with marginal suppression of host immunity. Specifically, gramillin induces reactive oxygen species (ROS) burst depending on host ILK1 and RBOHD genes but promotes disease independently of the major immune signaling pathways (such as jasmonic acid, salicylic acid, and pattern recognition receptors/PRRs). On the other hand, brassicapeptin A is salt-inducible and exhibits detrimental effects by interacting with salt in the environment, disturbing plant ion homeostasis. Together, these studies establish the multifaceted role of cyclic lipopeptides and their interactions with environmental stressors in pathogen success. (Summary by Arijit Mukherjee @ArijitM61745830) Cell Reports 10.1016/j.celrep.2024.114384, Nature Comms 10.1038/s41467-024-48517-5

Receptor-like cytoplasmic kinases of different subfamilies differentially regulate immune responses

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Cell surface receptor complexes act as the first line of defense in detecting pathogens and preventing invasion. Upon recognizing extracellular immunogenic patterns, a cascade of signaling relays occurs, mediated by phosphorylation events among a large array of membrane-associated proteins. These proteins include receptor-like kinases (RLKs), receptor-like proteins (RLPs), and receptor-like cytoplasmic kinases (RLCKs). The genomes of Arabidopsis and rice contain approximately 610 and 1,100 RLKs, respectively, though the functions of many of these proteins remain largely unknown. Despite the complex nature and origins of the patterns perceived, immune responses generally converge on a few common pathways. These include a rapid burst of reactive oxygen species (ROS), activation of mitogen-activated protein kinase (MAPK) cascades, transcriptional reprogramming, and, in some cases, programmed cell death known as the hypersensitive response (HR). Focusing on the RLCK subfamily VII, Huang and colleagues demonstrated that RLCK-VII-6, -7, and -8 are non-redundantly involved in the ROS burst upon detecting diverse patterns from both bacterial and fungal origins. Interestingly, only RLCK-VII-7 is involved in the HR response, highlighting the specific functions of RLCK subfamily members. (Summary by Ching Chan @ntnuchanlab) Nature Communications 10.1038/s41467-024-48313-1

Alternative splicing of a disease resistance gene maintains homeostasis between growth and immunity

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Plant resistance genes encode proteins that trigger immune responses when they recognize pathogen effectors. Their activation must be carefully regulated, as overexpression of activation of R genes usually causes a decrease in growth rate. Here, Sun et al. investigated the role of alternative splicing of a potato R gene called RB. They showed that in the absence of the Phythophtora infestans effector IPI-O1, the RB gene is spliced in such a way that an intron is retained, leading to a truncated, non-functional protein. However in the presence of the pathogen effector, the transcript is spliced to remove the intron, leading to a functional resistance protein. The authors showed that the IPI-O1 pathogen effector interacts with the plant splicing factor CWC15, causing it to localize to nuclear speckles and leading to increased splicing of the intron, functional protein production, and enhanced immunity. This finding sheds new light on how plants balance the trade-off between defense and growth. (Summary by Mary Williams @PlantTeaching) Plant Cell  10.1093/plcell/koae189

Maternal nitric oxide is key to female gametophyte development and plant fertility

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Wang et al. investigate how disruption of maternal nitric oxide affects female gametophyte development and fertility under both optimal and stress conditions.

By Junzhe Wang1,3, Xiaolong Guo1, Shengbao Xu1 and Elizabeth Vierling2
1State Key Laboratory for Crop Stress Resistance and High-Efficiency Production, College of Agronomy, Northwest A&F University, Yangling, Shaanxi 712100, China.
2Department of Biochemistry & Molecular Biology, University of Massachusetts, Amherst, MA 01003, USA.
3Hainan Yazhou Bay Seed Laboratory, Yazhou, Sanya 572025, China.

https://doi.org/10.1093/plcell/koae043

Background: In adverse environments, plants often produce more nitric oxide (NO), which plays a pivotal role in modulating plant growth and development. Additionally, under stress, the number of fertilizable female gametophytes (FGs) in plants is reduced, leading to enhanced survival of remaining offspring. The mechanisms by which the maternal plant perceives internal growth signals and external stress factors to modify FG development are still largely unknown.

Question: How does the maternal plant perceive internal growth cues and external stress conditions to regulate FG development? What are the mechanisms by which NO controls FG development?

Findings: NO homeostasis is critical for regulating FG development in Arabidopsis. NO homeostasis is precisely maintained by S-nitrosoglutathione reductase (GSNOR), an enzyme that accumulates exclusively in sporophytic tissues and indirectly governs the development of FGs prior to fertilization. Disrupted maternal NO homeostasis in hot5 mutants or addition of exogenous NO inhibits delivery of maternal auxin to the FG, thereby affecting FG development. Further, enhancing NO control capability and auxin supply can significantly increase plant fertility under stress conditions, suggesting that maternal NO homeostasis and auxin supply are key to regulating FG development. Our findings indicate that the maternal plant may integrate internal growth cues (auxin) and external stress intensity (experienced as disrupted NO homeostasis) to determine the success of FG development, providing a mechanism by which plants modulate seed set in response to fluctuating environment.

Next step: It is of interest to determine how specific changes in NO modification of proteins contribute to reducing FG development. It is also important to explore the relationship of NO homeostasis to fertility in crop species, with a focus on uncovering the potential application of these molecular mechanisms for crop improvement, particularly in the face of challenging environmental conditions.

Reference:

Junzhe Wang, Xiaolong Guo, Yijin Chen, Tianxiang Liu, Jianchu Zhu, Shengbao Xu, Elizabeth Vierling (2024) Maternal nitric oxide homeostasis impacts female gametophyte development under optimal and stress conditions. https://doi.org/10.1093/plcell/koae043

When posttranslational modifications meet splicing to regulate stress responses

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Agrofoglio et al. explore how the methylation of arginine residues on a key splicing factor affects alternative splicing.

Julieta Mateos, María José Iglesias, Yamila Agrofoglio. IFIBYNE-UBA-CONICET

https://doi.org/10.1093/plcell/koae051

Background: Plants are constantly subjected to a variety of environmental fluctuations, ranging from alterations in ambient temperature to infection by pathogens. In response to these stresses, plant cells trigger a complex reprogramming of gene expression, altering not only growth and development but also eliciting defense mechanisms. Several levels of gene regulation are involved in plant stress responses. These include transcriptional regulation, which determines which genes are activated; posttranscriptional regulation, which controls if mRNAs undergo alternative splicing; translational regulation, which controls when mRNAs are translated into proteins; and posttranslational regulation, which controls whether these proteins suffer additional modifications that influence their activity. Consequently, the interaction of the different molecular programs coordinating gene expression is essential for plant development.

Question: Previous studies established that in Arabidopsis plants, the PRMT5 methyltransferase protein methylates the arginine residues of proteins that are involved in the regulation of alternative splicing. To determine the importance of methylation in alternative splicing regulation, especially in response to stress, we employed the SM-LIKE PROTEIN 4 (LSM4) splicing factor as a model.

Findings: We show that loss of LSM4 leads to widespread missplicing, but its methylation has a restricted role in splicing under normal growth. On the other hand, LSM4 methylation responds to environmental cues associated with stress, showing antagonic response under both biotic and abiotic conditions. Bacterial infection leads to decreased LSM4 methylation, influencing the splicing of genes associated with plant immunity to enhance resistance. In contrast, salinity increases LSM4 methylation, crucial for the correct splicing of genes involved in abiotic stress responses.

Next steps: Our work shows how posttranslational modification changes RNA splicing to allow plants to acclimate to the environment. The interaction of diverse protein modifications, converging to efficiently control the RNA splicing process, has the potential to reveal key molecular mechanisms essential for plant adaptation.

Reference:

Yamila Carla Agrofoglio; María José Iglesias; Soledad Perez-Santángelo; María José de Leone; Tino Koester, Rafael Catalá; Julio Salinas; Marcelo J. Yanovsky; Dorothee Staiger; Julieta L. Mateos (2024) Arginine methylation of SM-LIKE PROTEIN 4 antagonistically affects alternative splicing during Arabidopsis stress responses. https://doi.org/10.1093/plcell/koae051