(−)‐Loliolide is a general signal of plant stress that activates jasmonate‐related responses

• Published in: The New phytologist Vol. 238; no. 5; pp. 2099 - 2112
• Main Authors: Li, Lei‐Lei, Li, Zheng, Lou, Yonggen, Meiners, Scott J., Kong, Chui‐Hua
• Format: Journal Article
• Language: English
• Published: England Wiley Subscription Services, Inc 01.06.2023
• Subjects: (−)‐loliolide; abiotic stress; belowground signaling interactions; benzoxazinoids; biotic and abiotic stressors; Chemical defence; Chemical defense; chemical defenses; Competitors; cyanogenic glycosides; Cyclopentanes - metabolism; defense‐related genes; defensive metabolites; Flavonoids; Flowers & plants; Gene expression; genes; Glycosides; Herbivores; Hydrogen peroxide; Jasmonic acid; jasmonic acid (JA); Metabolites; Oxylipins - metabolism; Pathogens; Phenolic acids; Phenols; Plant species; Plant stress; Plants; Plants - metabolism; reactive oxygen species (ROS); rice; root transcriptome; Signal transduction; Signaling; Terpenes; terpenoids; transcription (genetics); transcriptome; Transcriptomes; wheat; jasmonic acid (JA); defense-related genes; defensive metabolites; root transcriptome; (−)-loliolide; reactive oxygen species (ROS); belowground signaling interactions; biotic and abiotic stressors
• ISSN: 0028-646X; 1469-8137; 1469-8137
• DOI: 10.1111/nph.18644

Summary The production of defensive metabolites in plants can be induced by signaling chemicals released by neighboring plants. Induction is mainly known from volatile aboveground signals, with belowground signals and their underlying mechanisms largely unknown. We demonstrate that (−)‐loliolide triggers defensive metabolite responses to competitors, herbivores, and pathogens in seven plant species. We further explore the transcriptional responses of defensive pathways to verify the signaling role of (−)‐loliolide in wheat and rice models with well‐known defensive metabolites and gene systems. In response to biotic and abiotic stressors, (−)‐loliolide is produced and secreted by roots. This, in turn, induces the production of defensive compounds including phenolic acids, flavonoids, terpenoids, alkaloids, benzoxazinoids, and cyanogenic glycosides, regardless of plant species. (−)‐Loliolide also triggers the expression of defense‐related genes, accompanied by an increase in the concentration of jasmonic acid and hydrogen peroxide (H2O2). Transcriptome profiling and inhibitor incubation indicate that (−)‐loliolide‐induced defense responses are regulated through pathways mediated by jasmonic acid, H2O2, and Ca 2+. These findings argue that (−)‐loliolide functions as a common belowground signal mediating chemical defense in plants. Such perception‐dependent plant chemical defenses will yield critical insights into belowground signaling interactions. See also the Commentary on this article by Frost, 238: 1749–1751.