Robustness of plant quantitative disease resistance is provided by a decentralized immune network

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 117; no. 30; pp. 18099 - 18109
• Main Authors: Delplace, Florent, Huard-Chauveau, Carine, Dubiella, Ullrich, Khafif, Mehdi, Alvarez, Eva, Langin, Gautier, Roux, Fabrice, Peyraud, Rémi, Roby, Dominique
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 28.07.2020
• Subjects: Biological Sciences; Complexity; Computational Biology - methods; Deregulation; Disease resistance; Disease Resistance - immunology; Disease Susceptibility - immunology; Gene expression; Gene Expression Profiling; Gene Expression Regulation, Plant; Genes; Genes, Plant; Host-Pathogen Interactions - genetics; Host-Pathogen Interactions - immunology; Immunity; Immunomodulation; Life Sciences; Metabolism; Models, Biological; Modules; Mutation; Natural populations; Pathogens; Phenotype; Phytopathology and phytopharmacy; Plant diseases; Plant Diseases - etiology; Plant Immunity; Protein Interaction Mapping; Protein Interaction Maps; Proteins; Quantitative trait loci; Robustness; Signaling; Transcriptome; Vegetal Biology; systems biology; immunity; quantitative disease resistance; regulatory networks; plant pathogen interactions
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.2000078117

Quantitative disease resistance (QDR) represents the predominant form of resistance in natural populations and crops. Surprisingly, very limited information exists on the biomolecular network of the signaling machineries underlying this form of plant immunity. This lack of information may result from its complex and quantitative nature. Here, we used an integrative approach including genomics, network reconstruction, and mutational analysis to identify and validate molecular networks that control QDR in Arabidopsis thaliana in response to the bacterial pathogen Xanthomonas campestris. To tackle this challenge, we first performed a transcriptomic analysis focused on the early stages of infection and using transgenic lines deregulated for the expression of RKS1, a gene underlying a QTL conferring quantitative and broad-spectrum resistance to X. campestris. RKS1-dependent gene expression was shown to involve multiple cellular activities (signaling, transport, and metabolism processes), mainly distinct from effector-triggered immunity (ETI) and pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) responses already characterized in A. thaliana. Protein–protein interaction network reconstitution then revealed a highly interconnected and distributed RKS1-dependent network, organized in five genemodules. Finally, knockoutmutants for 41 genes belonging to the different functional modules of the network revealed that 76% of the genes and all gene modules participate partially in RKS1-mediated resistance. However, these functional modules exhibit differential robustness to genetic mutations, indicating that, within the decentralized structure of the QDR network, some modules are more resilient than others. In conclusion, our work sheds light on the complexity of QDR and provides comprehensive understanding of a QDR immune network.