Rhizobial Nod factors modulate reactive oxygen species, jasmonates, and pattern-recognizing receptors to suppress immune response.

Abstract

Fine-tuning of the immune response plays a key role in legume-rhizobial symbiosis. Rhizobial Nod factors can suppress the defense responses during symbiosis, but the possible mechanisms of such regulation remain poorly understood. Here, we observe that Nod factors effectively suppress the expression of genes encoding defense markers (WRKYs, PRs, PALs), the reactive oxygen species (ROS) formation, and reduce the content of pattern recognition receptor (PRR) LYK9 induced by treatment with deacetylated chitooligosaccharide CO8-DA in pea roots. Since PRR LYK9 may recognize both chitin/COs and peptidoglycan, it likely plays an important role in the activation of defense responses during rhizobial inoculation. To identify potential regulators through which Nod factors suppress the immune response in plants during symbiosis with rhizobia, proteome and transcriptome analyses were performed. This allowed identifying several potential candidates activated by Nod factors, such as superoxide dismutase and catalase enzymes, which prevent excessive ROS accumulation and the development of oxidative stress. We also found ubiquitin ligases and ubiquitin-conjugating enzymes that may target PRRs activated in response to rhizobial inoculation. LYK9 degradation via ubiquitinylation was shown to prevent a hypersensitive response in plants. Nod factors activate enzymes involved in jasmonic acid biosynthesis, which in turn activates the transcription factor ABR1, suppressing the abscisic acid-induced responses and decreasing the immune response. Finally, we showed that LysM-receptor-like kinases PsLYK11/MtLYK11, probable homologs of Arabidopsis AtLYK3 in pea and Medicago, are involved in regulation of the immune response.