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

Abstract

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 gene modules. Finally, knockout mutants 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.

Transcriptome analysis in the maize-Ustilago maydisinteraction identifies maize-line-specific activity of fungal effectors

“…Protein phosphorylation occurs during kinase signalling processes. A predominant role of genes related to metabolism as well as kinase-signalling cascades for QDR has been proposed before (Delplace et al 2020). Taken together, this suggests that maize line-specific responses to U. maydis involved various cellular activities, consistent with the complex nature of QDR.…”

“…In general, QDR can be hypothesised as an intricate network integrating various response pathways to pathogen determinants and environmental factors (Roux et al 2014). Additionally, studies of QDR by RNA-Seq approaches have indicated highly interconnected and multifaceted defence responses, which were mostly distinct from functions previously identified for plant immunity (Kebede et al 2018; Pan et al 2018; Delplace et al 2020).…”

Comparative transcriptome profiling identifies maize line specificity of fungal effectors in the maize–Ustilago maydis interaction

“…Protein phosphorylation occurs during kinase signalling processes. A predominant role of genes related to metabolism as well as kinase signalling cascades for QDR has been proposed before (Delplace et al ., 2020). Together, this suggests that maize line‐specific responses to U. maydis involve various cellular activities, consistent with the complex nature of QDR.…”

“…Thus, compared to qualitative resistance, the molecular functions underlying QDR seem to be highly diverse. Additionally, studies of QDR by RNA sequencing (RNA‐Seq) approaches have indicated highly interconnected and multifaceted defence responses, which were mostly distinct from functions previously identified for plant immunity (Delplace et al ., 2020; Kebede et al ., 2018; Pan et al ., 2018).…”

Comparative genomics and transcriptomics analyses reveal genetic complexity of soybean anthracnose caused by >i<Colletotrichum>/i< species

“…Even if it is considered the predominant resistance found in nature, genes and mechanisms involved in QDR are poorly understood (Bartoli and Roux, 2017;Delplace et al, 2020), and resistance involving the QDR is more difficult to select due the involvement of several genes (Corwin and Kliebenstein, 2017). Because of the reduced selective pressure on the pathogen and the possibility of providing broad-spectrum resistance for more than one species and/or race of a pathogen, QDR has great potential to be more durable in the field (Krattinger et al, 2009;Corwin and Kliebenstein, 2017;Pilet-Nayel et al, 2017;Nelson et al, 2018).…”