Abstract
In this work, we investigated the chemical process underlying the interplay between two rice sheath pathogens: Pseudomonas fuscovaginae, the causal agent of sheath brown rot, and Rhizoctonia solani AG 1-IA, which causes sheath blight. Specifically, we studied the fate of the bacterial cyclic lipopeptides (CLiPs) syringotoxin and fuscopeptin in this interaction. Both compounds exhibit potent antifungal activity against R. solani and induce phytotoxic effects. Ultra-performance liquid chromatography-tandem mass spectrometry analysis demonstrated that R. solani AG 1-IA likely secretes two distinct enzymes: an esterase that hydrolyzes the ester bond in syringotoxin, producing a linear derivative, and a protease that cleaves the glycine-alanine bond within the peptide backbone of fuscopeptin. The degradation products lack antifungal and phytotoxic activities, nullifying the competitive advantage of P. fuscovaginae. These enzymatic effects showed increased activity at 28°C. In contrast, R. solani AG 2-2 did not degrade CLiPs. Further analysis with a broader range of R. solani isolates revealed that CLiP degradation is a common trait among AG 1-IA isolates. This study provides the first evidence that R. solani AG 1-IA actively neutralizes the antifungal and phytotoxic activities of P. fuscovaginae through targeted enzymatic degradation.IMPORTANCERice is a global staple crop that is susceptible to various pathogens, including Pseudomonas fuscovaginae, causing sheath brown rot, and Rhizoctonia solani AG 1-IA, which causes sheath blight. Notably, P. fuscovaginae primarily occurs at lower temperatures, whereas R. solani AG 1-IA is more prevalent under warmer conditions. Previous research demonstrated that P. fuscovaginae produces higher levels of the virulence-associated cyclic lipopeptides (CLiPs) syringotoxin and fuscopeptin at 18°C, potentially explaining its pathogenicity on rice plants grown at high altitudes. Conversely, R. solani AG 1-IA, which is sensitive to these CLiPs, was found to secrete CLiP-degrading enzymes, with degradation activity enhanced at 28°C. When combined with the reduced CLiP production by P. fuscovaginae at higher temperatures, this enzymatic degradation may confer a competitive advantage to R. solani in warmer environments. The absence of reports documenting the co-occurrence of both pathogens in field conditions may, at least in part, be explained by this temperature-dependent antagonism.