A Ralstonia solanacearum type III effector alters the actin and microtubule cytoskeleton to promote bacterial virulence in plants

Authors: HILES, RACHEL - Purdue University; ROGERS, ABIGAIL - Purdue University; Jaiswal, Namrata; ZHANG, WEIWEI - Purdue University; BUTCHACAS, JULES - The Ohio State University; MERFA, MARCUS - The Ohio State University; KLASS, TAYLOR - The Ohio State University; BARUA, PRAGYA - Purdue University; THIRUMALAIKUMAR, VENKATESH - Purdue University; JACOBS, JOHNATHAN - The Ohio State University; STAIGER, CHRISTOPHER - Purdue University; Helm, Matthew; IYER-PASCUZZI, ANJALI - Purdue University

Submitted to: PLoS Pathogens
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/7/2024
Publication Date: 12/26/2024
Citation: Hiles, R., Rogers, A., Jaiswal, N., Zhang, W., Butchacas, J., Merfa, M.V., Klass, T., Barua, P., Thirumalaikumar, V.P., Jacobs, J.M., Staiger, C.J., Helm, M.D., Iyer-Pascuzzi, A.S. 2024. A Ralstonia solanacearum type III effector alters the actin and microtubule cytoskeleton to promote bacterial virulence in plants. PLoS Pathogens. https://doi.org/10.1371/journal.ppat.1012814.
DOI: https://doi.org/10.1371/journal.ppat.1012814

Interpretive Summary: Bacterial plant pathogens need to suppress the plant immune system to promote their growth and sustain bacterial colonization. To do this, bacteria often inject specialized molecules known as effectors directly inside plant cells where they function to shut-off the plant immune system, thereby allowing the pathogen to colonize the host. One such bacterial pathogen, Ralstonia solanacearum, uses effector molecules to cause a disease called bacterial wilt disease. Importantly, bacterial wilt disease affects many important crop plants including potato, pepper, and tomato. Though agriculturally important, very little is known about this bacterial pathogen uses effector molecules to cause disease. In this study, we show that one effector molecule, which we have termed, RipU, suppress plant immune responses by interfering with plant cell proteins that are involved in maintaining the plant cytoskeleton. Our work presented here provide valuable insights into the host processes potentially manipulated by this bacterial pathogen.

Technical Abstract: Cellular responses to biotic stress frequently involve signaling pathways that are conserved across eukaryotes. These pathways include the cytoskeleton, a proteinaceous network that senses external cues at the cell surface and signals to interior cellular components. During biotic stress, dynamic cytoskeletal rearrangements serve as a platform from which early immune-associated processes are organized and activated. Bacterial pathogens of plants and animals use proteins called type III effectors (T3Es) to interfere with host immune signaling, thereby promoting virulence. We previously found that RipU, a T3E from the soilborne phytobacterial pathogen Ralstonia solanacearum K60 (Rs K60), co-localizes with the plant cytoskeleton. Here, we show that RipU from Rs K60 (RipUK60) physically associates with and disrupts both the actin and microtubule cytoskeleton. We find that pharmacological disruption of the tomato (Solanum lycopersicum) cytoskeleton promotes Rs K60 colonization. RipUK60 suppresses flg22-mediated reactive oxygen species (ROS) production. Importantly, tomato plants inoculated with Rs K60 lacking RipUK60 ('ripUK60) had reduced wilting symptoms and significantly reduced root colonization when compared to plants inoculated with wild-type Rs K60. Collectively, our data suggest that Rs K60 uses the type III effector RipUK60 to remodel cytoskeletal organization, thereby promoting pathogen virulence.