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

Abstract

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. 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. HIGHLIGHTSO_LIBotrytis cinerea expressing the salicylate hydroxylase (SH) ppNahG shows enhanced virulence in Arabidopsis and bean plants. C_LIO_LIEnhanced virulence of NahG-expressing strains depends on host salicylic acid biosynthesis. C_LIO_LIThe Botrytis cinerea genome encodes four SH-like genes. C_LIO_LISH-like genes display distinct expression patterns during infection across different plant hosts. C_LI VISUAL ABSTRACT O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=128 SRC="FIGDIR/small/698134v1_ufig1.gif" ALT="Figure 1"> View larger version (24K): org.highwire.dtl.DTLVardef@135adorg.highwire.dtl.DTLVardef@16b2947org.highwire.dtl.DTLVardef@62fd40org.highwire.dtl.DTLVardef@e07e2e_HPS_FORMAT_FIGEXP M_FIG C_FIG