Universal gene co-expression network reveals receptor-like protein genes conferring broad-spectrum resistance in pepper (Capsicum annuum L.)

Abstract

Receptor-like proteins (RLPs) on the plant cell surface have been implicated in immune responses and developmental processes. Although hundreds of RLP genes have been identified in plants, only a few RLPs have been functionally characterized in a limited number of plant species. Here, we identified RLPs in the pepper (Capsicum annuum) genome, and performed comparative transcriptomics coupled with the analysis of conserved gene co-expression networks (GCNs) to reveal the role of core RLP regulators in pepper-pathogen interactions. A total of 102 RNA-seq datasets of pepper plants infected with four pathogens were used to construct CaRLP-targeted GCNs (CaRLP-GCN). All resistance-responsive CaRLP-GCNs were merged to construct a universal GCN. Fourteen hub CaRLPs, tightly connected with defense related gene clusters, were identified in eight modules. Based on the CaRLP-GCNs, we experimentally tested whether hub CaRLPs in the universal GCN are involved in biotic stress response. Of the nine hub CaRLPs tested by virus-induced gene silencing (VIGS), three genes (CaRLP264, CaRLP277, and CaRLP351) showed defense suppression with less hypersensitive response (HR)-like cell death in race-specific and non-host resistance response to viruses and bacteria, respectively, and consistently enhanced susceptibility to Ralstonia solanacearum and/or Phytophthora capsici. These data suggest that key CaRLPs exhibit conserved functions in response to multiple biotic stresses and can be used for engineering of a plant with broad-spectrum resistance. Altogether, we show that generation of a universal GCN using comprehensive transcriptome datasets could provide important clues for uncovering genes involved in various biological processes.