Ethylene is a local modulator of jasmonate-dependent phenolamide accumulation during Manduca sexta herbivory in Nicotiana attenuata

Abstract

AO_SCPLOWBSTRACTC_SCPLOWRapid reconfigurations of intimately connected phytohormone signaling networks allow plants to tune their physiology to constantly varying ecological conditions. During insect herbivory, most of the induced changes in defense-related leaf specialized metabolites are controlled by jasmonate (JA) signaling, which, in the wild tobacco Nicotiana attenuata, recruits MYB8, a transcription factor controlling the accumulation of phenolic-polyamine conjugates (phenolamides). In this and other plant species, herbivory also locally triggers ethylene (ET) production but the outcome of the JA-ET crosstalk at the level of secondary metabolism regulation has remained superficially investigated. Here, we analyzed local and systemic herbivory-induced changes by mass spectrometry-based metabolomics in leaves of transgenic plants impaired in JA, ET and MYB8 signaling. Parsing deregulations in this factorial data-set identified a network of JA/MYB8-dependent phenolamides for which impairment of ET signaling attenuated their accumulation only in locally-damaged leaves. Further experiments revealed that ET, albeit biochemically interrelated to polyamine metabolism via the intermediate S-adenosylmethionine, does not impart on free polyamine levels, but instead significantly modulates phenolamide levels and marginally affected transcript levels in this pathway. This study identifies ET as a local modulator of phenolamide investments and provides a metabolomics data-platform to mine associations between herbivory-induced signaling and specialized metabolite groups in N. attenuata. SO_SCPLOWUMMARYC_SCPLOWO_SCPCAP C_SCPCAPO_SCPLOWSTATEMENTC_SCPLOWHerbivory-elicited ethylene acts as a local enhancer of the production of jasmonate/MYB8-dependent phenolamides during the defense response of Nicotiana attenuata leaves against herbivory by the lepidopteran larva Manduca sexta.