A key antisense sRNA modulates the oxidative stress response and virulence in Xanthomonas oryzae pv. oryzicola

Abstract

Pathogens integrate multiple environmental signals to navigate the host and control the expression of virulence genes. In this process, small regulatory noncoding RNAs (sRNAs) may function in gene expression as post-transcriptional regulators. In this study, the sRNA Xonc3711 functioned in the response of the rice pathogen, Xanthomonas oryzae pv. oryzicola ( Xoc), to oxidative stress. Xonc3711 repressed production of the DNA-binding protein Xoc_3982 by binding to the xoc_3982 mRNA within the coding region. Mutational analysis showed that regulation required an antisense interaction between Xonc3711 and xoc_3982 mRNA, and RNase E was needed for degradation of the xoc_3982 transcript. Deletion of Xonc3711 resulted in a lower tolerance to oxidative stress due to the repression of flagella-associated genes and reduced biofilm formation. Furthermore, ChIP-seq and electrophoretic mobility shift assays showed that Xoc_3982 repressed the transcription of effector xopC2, which contributes to virulence in Xoc BLS256. This study describes how sRNA Xonc3711 modulates multiple traits in Xoc via signals perceived from the external environment.

Author summary

Small, stable RNA species perform diverse functions in both prokaryotes and eukaryotes. In this study, the sRNA Xonc3711 decreased the production of DNA-binding protein Xoc_3982 in the bacterium Xanthomonas oryzae pv. oryzicola ( Xoc) by base pairing with the xoc_3982 transcript. When Xonc3711 was mutated, Xoc was impaired in its ability to form flagella and produce biofilms, which reduced Xoc tolerance to oxidative stress. We also discovered that the DNA-binding protein Xoc_3982 represses the expression of xopC2, which encodes an effector protein, and reduces its expression. Our results show that Xonc3711 modulates and integrates multiple systems in Xoc to protect cells from oxidative damage.