ZmTPS18-mediated β-caryophyllene biosynthesis contributes to resistance against southern corn rust in maize.

Abstract

Southern corn rust (SCR), caused by the obligate biotrophic fungus Puccinia polysora Underwood, is a major foliar disease of maize associated with substantial yield losses in many production regions. Terpenoids are important components of plant defense, but the terpene synthases and upstream regulators involved in pathogen-induced terpenoid biosynthesis in maize are still poorly defined. In this study, volatile profiling showed that β-caryophyllene emission was induced in the SCR-resistant maize inbred line Yanzi F7016K after pathogen inoculation, reaching levels 3.18-fold higher than those in the susceptible line Yanzi F7014S. Comparative transcriptome analysis identified ZmTPS18 as a strongly induced candidate associated with pathogen-induced terpenoid biosynthesis. Biochemical characterization showed that ZmTPS18, previously annotated as a monoterpene synthase, catalyzed the formation of 1,8-cineole from geranyl diphosphate and β-caryophyllene from farnesyl diphosphate in vitro, revealing previously unrecognized bifunctional catalytic activity. Functional analyses indicate that ZmTPS18 contributes to pathogen-induced β-caryophyllene accumulation and is associated with maize responses to SCR. Loss-of-function mutants exhibited reduced β-caryophyllene accumulation and increased uredinium density, whereas transient overexpression of ZmTPS18 enhanced β-caryophyllene accumulation. In vitro assays further showed that β-caryophyllene inhibited Puccinia polysora urediniospore germination in a concentration-dependent manner. In addition, ZmMYB282 was shown to directly bind to the ZmTPS18 promoter and repress its transcription. Together, these findings identify ZmTPS18 as a bifunctional terpene synthase that contributes to inducible β-caryophyllene biosynthesis and SCR resistance, and reveal a transcriptional link between ZmMYB282 and ZmTPS18 in maize volatile defense.