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Epigenetic regulation of transcriptional reprogramming in susceptible cells of Arabidopsis in response to Xanthomonas infection

Applicant Yuan You, Ph.D.
Subject Area Organismic Interactions, Chemical Ecology and Microbiomes of Plant Systems
Term from 2019 to 2024
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 427105396
 
Final Report Year 2024

Final Report Abstract

Bacterial pathogens cause diseases on numerous crop species resulting in drastic yield losses at a global scale. To infect host plants, bacteria enter host plants via natural openings (e.g.,stomata or hydathodes) or wounds, and subsequently encounter cells that are accessible from the apoplastic lumen. Virulent gram-negative bacteria can inject low amounts of proteinaceous effectors into these cells using a syringe-like type-III secretion system (T3SS). Inside host cells, these effectors are translocated into different subcellular compartments and manipulate host cellular processes to subvert immune surveillance systems and create a favourable environment for bacterial colonization and dissemination. However, the molecular mechanisms of how bacterial effectors promote disease and impact other aspects of host physiology and development are largely unknown. Particularly, bacterial effector-induced epigenetic regulation of transcriptional reprogramming in host plant cells has largely eluded analysis so far, mostly because of the technical challenges of isolating effector-targeted cells for epigenomic analyses. In this project, I have developed a novel technique, effector-inducible isolation of nuclei tagged in specific cell types (eINTACT), for isolating biotin-labelled nuclei from Arabidopsis plant cells that have received Xanthomonas bacterial effectors by using streptavidin-coated magnetic beads. Analysis of purified nuclei reveals that the Xanthomonas effector XopD manipulates the expression of Arabidopsis abscisic acid signalling-related genes and activates OSCA1.1, a gene encoding a calcium-permeable channel required for stomatal closure in response to osmotic stress. The loss of OSCA1.1 causes leaf wilting and reduced bacterial growth in infected leaves, suggesting that OSCA1.1 promotes host susceptibility. eINTACT allows us to uncover that XopD exploits host OSCA1.1/abscisic acid osmosignalling-mediated stomatal closure to create a humid habitat that favours bacterial growth and opens a new avenue for accurately elucidating functions of effectors from numerous gram-negative plant bacteria in native infection contexts. In summary, my project has not only contributed to our understanding of molecular pathogenesis of Xanthomonas in general, but also advanced the methodology in the research field of plant pathology. The outcomes are paramount to designing effective and sustainable strategies for combating bacterial disease in crops.

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