The Involvement of Jasmonic Acid, Ethylene, and Salicylic Acid in the Signaling Pathway of Clonostachys rosea-Induced Resistance to Gray Mold Disease in Tomato

Tomato gray mold disease caused by Botrytis cinerea is a serious disease that threatens tomato production around the world. Clonostachys rosea has been used successfully as a biocontrol agent against divergent plant pathogens, including B. cinerea. To understand the signal transduction pathway of C. rosea-induced resistance to tomato gray mold disease, the effects of C. rosea on gray mold tomato leaves along with changes in the activities of three defense enzymes (phenylalanine ammonialyase [PAL], polyphenol oxidase [PPO], and catalase [CAT]), second messengers (nitric oxide [NO], hydrogen peroxide [H2O2], and superoxide anion radical [O-2(-)]), and stress-related genes (mitogenactivated protein kinase [MAPK], WRKY, Lexyl2, and atpA) in four different hormone-deficient (jasmonic acid [JA], ethylene [ET], salicylic acid [SA], and gibberellin) tomato mutants were investigated. The results revealed that C. rosea significantly inhibited the growth of mycelia and spore germination of B. cinerea. Furthermore, it reduced the incidence of gray mold disease, induced higher levels of PAL and PPO, and induced lower levels of CAT activities in tomato leaves. Moreover, it also increased NO, H2O2, and O-2(-) levels and the gene expression levels of WRKY, MAPK, atpA, and Lexyl2. The incidence of gray mold disease in four hormone-deficient mutants was higher than that in the corresponding wild-type tomato plants. Among all of these hormone-deficient tomato mutants, JA had the most significant effect in regulating the different signal molecules. Additional study suggested that JA upregulated the expression of Lexyl2, MAPK, and WRKY but downregulated atpA. Furthermore, JA also enhanced the activity of PAL, PPO, and CAT and the production of NO and H2O2. SA downregulated CAT and PAL, whereas ET upregulated PAL but downregulated CAT. This study is of significance in understanding the regulatory pathways and biocontrol mechanism of C. rosea against B. cinerea.