Reshaping the Primary Cell Wall: Dual Effects on Plant Resistance to Ralstonia solanacearum and Heat Stress Response

• DOI: 10.1094/mpmi-05-24-0059-r
• Publication Date: 2024-06-21T15:41:04Z
• Authors: Henri Desaint; Alessandro Gigli; Adrien Belny; Hua Cassan-Wang; Yves Martinez; Fabienne Vailleau; Fabien Mounet; Samantha Vernhettes; Richard Berthomé; Marta Marchetti
• Keywords: 570; MESH: Arabidopsis* / immunology; Arabidopsis thaliana; MESH: Arabidopsis* / physiology; [SDV]Life Sciences [q-bio]; MESH: Plant Roots / genetics; 610; MESH: Plant Roots / microbiology; Microbiology; 630; MESH: Plant Diseases* / immunology; MESH: Arabidopsis* / genetics; MESH: Arabidopsis* / microbiology; MESH: Ralstonia solanacearum* / physiology; MESH: Cell Wall* / metabolism; Arabidopsis thaliana cell wall CESA3 Ralstonia solanacearum temperature elevation; CESA3; temperature elevation; Botany; MESH: Arabidopsis Proteins / metabolism; MESH: Disease Resistance* / genetics; MESH: Gene Expression Regulation; MESH: Heat-Shock Response*; QR1-502; Plant*; MESH: Arabidopsis Proteins / genetics; MESH: Plant Diseases* / microbiology; QK1-989; MESH: Gene Expression Regulation, Plant*; [SDE]Environmental Sciences; MESH: Mutation*; Ralstonia solanacearum; cell wall

Temperature elevation drastically affects plant defense responses to Ralstonia solanacearum and inhibits the major source of resistance in Arabidopsis thaliana, which is mediated by the receptor pair RRS1-R/RPS4. In this study, we refined a previous genome-wide association (GWA) mapping analysis by using a local score approach and detected the primary cell wall CESA3 gene as a major gene involved in plant response to R. solanacearum at both 27°C and an elevated temperature, 30°C. We functionally validated CESA3 as a susceptibility gene involved in resistance to R. solanacearum at both 27 and 30°C through a reverse genetic approach. We provide evidence that the cesa3mre1 mutant enhances resistance to bacterial disease and that resistance is associated with an alteration of root cell morphology conserved at elevated temperatures. However, even by forcing the entry of the bacterium to bypass the primary cell wall barrier, the cesa3mre1 mutant still showed enhanced resistance to R. solanacearum with delayed onset of bacterial wilt symptoms. We demonstrated that the cesa3mre1 mutant had constitutive expression of the defense-related gene VSP1, which is upregulated at elevated temperatures, and that during infection, its expression level is maintained higher than in the wild-type Col-0. In conclusion, this study reveals that alteration of the primary cell wall by mutating the cellulose synthase subunit CESA3 contributes to enhanced resistance to R. solanacearum, remaining effective under heat stress. We expect that these results will help to identify robust genetic sources of resistance to R. solanacearum in the context of global warming. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .