High humidity represses Cf-4/Avr4- and Cf-9/Avr9-dependent hypersensitive cell death and defense gene expression

Gene-for-gene resistance is a well-known type of plant disease resistance. It is governed by plant resistance (R) genes and their matching pathogen avirulence (Avr) genes. This resistance is characterized by a hypersensitive response (HR) resulting from the interaction between products of a complementary R and Avr gene pair. The pathosystem of tomato (Lycopersicon esculentum Mill.) and its leaf mold fungal pathogen Cladosporium fulvum is a model system to study gene-for-gene resistance. HR occurs in tomato seedlings carrying a tomato Cf resistance gene and a matching C. fulvum Avr gene, including, for example, Cf-4/Avr4 and Cf-9/Avr9. Employing Cf/Avr tomato seedlings that both express a Cf gene and the matching Avr gene, here we report that both Cf-4/Avr4- and Cf-9/Avr9-dependent HR is delayed and reduced under high humidity (95%), and that Cf-9/Avr9-dependent HR is more sensitive to high humidity when compared to Cf-4/Avr4-dependent HR. Furthermore, high humidity acts synergistically with high temperature on HR suppression, resulting in complete blocking of the HR. The transcript profile of over 60 genes, related to HR, signaling and defense, in Cf/Avr seedlings grown under high humidity and thus showing no HR, significantly differed from that of the same seedlings grown under normal humidity and thus showing HR. These results demonstrate that high humidity probably acts at a very early point of the Cf downstream signaling pathway, or alternatively influences the interaction between the Cf and the Avr proteins.