Salicylic acid contributes to plant defense against a necrotroph: evidence from a transgenic NahG-expressing strain in Botrytis cinerea

Botrytis cinerea is a plant pathogen that causes significant agricultural losses worldwide. Although this necrotroph disrupts extensive plant hormonal networks, the role of salicylic acid (SA) in plant defense against B. cinerea remains controversial across plant species. To investigate its role from a pathogen perspective, B. cinerea mutants constitutively expressing the Pseudomonas putida salicylate hydroxylase NahG, an enzyme that catalyzes salicylic acid degradation, were generated. The NahG-expressing B. cinerea mutants exhibited enhanced in vitro growth on SA-supplemented media, indicating that SA catabolism confers an advantage. In planta, these mutants displayed increased virulence in Arabidopsis thaliana and Phaseolus vulgaris. Notably, the increase in lesion formation was strictly dependent on host SA biosynthesis, as no differences were observed when infecting the SA-deficient Arabidopsis sid2-2 mutant. This result provides evidence that SA degradation increases the virulence of B. cinerea in the interaction with A. thaliana. Importantly, expression of canonical SA- and JA-responsive marker genes PR1 and PDF1.2 was similarly induced during infection with "wild-type" B05.10 and NahG-expressing B. cinerea strains, indicating that enhanced virulence is not associated with major alterations in classical defense gene activation. Genome inspection revealed that the fungus encodes four salicylate hydroxylase-like genes. Analysis of publicly available transcriptomic data from virulence assays across multiple plant hosts revealed that all these genes are expressed during the plant-pathogen interaction, with distinct expression patterns across infection stages and hosts. Together, these observations suggest that B. cinerea may have endogenous mechanisms for SA degradation during host colonization, thereby conferring the capacity to control its accumulation during the infection process.