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

Abstract

Tomato gray mold disease caused by <i>Botrytis cinerea</i> is a serious disease that threatens tomato production around the world. <i>Clonostachys rosea</i> has been used successfully as a biocontrol agent against divergent plant pathogens, including <i>B. cinerea</i>. To understand the signal transduction pathway of <i>C. rosea</i>-induced resistance to tomato gray mold disease, the effects of <i>C. rosea</i> 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 [O₂^-]), and stress-related genes (<i>mitogen-activated protein kinase</i> [<i>MAPK</i>], <i>WRKY</i>, <i>Lexyl2</i>, and <i>atpA</i>) in four different hormone-deficient (jasmonic acid [JA], ethylene [ET], salicylic acid [SA], and gibberellin) tomato mutants were investigated. The results revealed that <i>C. rosea</i> significantly inhibited the growth of mycelia and spore germination of <i>B. cinerea</i>. 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 O₂^- levels and the gene expression levels of <i>WRKY</i>, <i>MAPK</i>, <i>atpA</i>, and <i>Lexyl2</i>. 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 <i>Lexyl2</i>, <i>MAPK</i>, and <i>WRKY</i> but downregulated <i>atpA</i>. 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 <i>C. rosea</i> against <i>B. cinerea</i>.