Cross-Kingdom Gene Coexpression Analysis Using a Stemphylium botryosum–Lens ervoides System Revealed Plasticity of Intercommunication Between the Pathogen Secretome and the Host Immune Systems

Abstract

Necrotrophic pathogens are responsible for significant declines in crop yield and quality worldwide. During the infection process, a pathogen releases a series of secretory proteins to counteract the plant immune system, and this interaction of pathogen and host molecules determines whether the pathogen will successfully invade the host plant tissues. In this study, we adopted co-transcriptomic approaches to analyze the Lens ervoides–Stemphylium botryosum system, with a focus on 1,216 fungal genes coding for secretory proteins and 8,810 disease-responsive genes of the host 48, 96, and 144 h postinoculation, captured in two F9 recombinant inbred lines (RILs) displaying contrasting disease responses. By constructing in planta gene coexpression networks (GCNs) for S. botryosum, we found that the pathogen tended to co-upregulate genes regulating cell wall degradation enzymes, effectors, oxidoreductases, and peptidases to a much higher degree in the susceptible host LR-66-577 than in the resistant RIL LR-66-637, indicating that the promotion of these digestive enzymes and toxins increased S. botryosum virulence. Construction of cross-kingdom GCNs between pathogen and plant for the two RILs revealed that the co-upregulation of these fungal digestive enzymes and toxins simultaneously promoted a series of defense responses such as redox change, expression of membrane-related genes and serine/threonine kinase, and stress and disease responses in the susceptible RIL which was not observed in the resistant RIL, indicating that these activities exacerbated susceptibility to S. botryosum. [Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .