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

• Published in: Plant, cell and environment Vol. 44; no. 3; pp. 964 - 981
• Main Authors: Figon, Florent, Baldwin, Ian T., Gaquerel, Emmanuel
• Format: Journal Article
• Language: English
• Published: Chichester, UK John Wiley & Sons, Ltd 01.03.2021; Wiley Subscription Services, Inc; Wiley
• Subjects: Abscisic Acid - metabolism; Accumulation; Adenosylmethionine; Amides - metabolism; Animals; Attenuation; Chromatography, High Pressure Liquid; Cyclopentanes - metabolism; Damage accumulation; Deregulation; Ecological conditions; Ethylene; ethylene signalling; Ethylenes - metabolism; Herbivory; Insect ecology; Insects; jasmonate signalling; Jasmonic acid; Leaves; Life Sciences; Manduca; Mass spectrometry; Mass spectroscopy; Metabolism; Metabolites; Metabolomics; Nicotiana - metabolism; Nicotiana - physiology; Nicotiana attenuata; Oxylipins - metabolism; phenolamides; Phenolic compounds; Phenols; Plant Defense Against Herbivory; Plant Growth Regulators - metabolism; Plant Growth Regulators - physiology; Plant Leaves - metabolism; Plant Proteins - metabolism; Plant species; plant–insect interactions; Polyamines; Real-Time Polymerase Chain Reaction; Salicylic Acid - metabolism; Signaling; Tobacco; Transcription Factors - metabolism; Transgenic plants; Vegetal Biology; ethylene signalling; metabolomics; plant-insect interactions; jasmonate signalling; phenolamides
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.13955

Rapid reconfigurations of interconnected phytohormone signalling networks allow plants to tune their physiology to constantly varying ecological conditions. During insect herbivory, most of the induced changes in defence‐related leaf metabolites are controlled by jasmonate (JA) signalling, 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 cross‐talk at the level of secondary metabolism regulation has remained only superficially investigated. Here, we analysed local and systemic herbivory‐induced changes by mass spectrometry‐based metabolomics in leaves of transgenic plants impaired in JA, ET and MYB8 signalling. Parsing deregulations in this factorial data‐set identified a network of JA/MYB8‐dependent phenolamides for which impairment of ET signalling 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 alter the free polyamine levels, but instead significantly modulates phenolamide levels with marginal modulations of transcript levels. The work identifies ET as a local modulator of phenolamide accumulations and provides a metabolomics data‐platform with which to mine associations among herbivory‐induced signalling and specialized metabolites in N. attenuata. Herbivory‐elicited ethylene acts as a local enhancer of the production of jasmonate/MYB8‐dependent phenolamides during the defence response of Nicotiana attenuata leaves against herbivory by the lepidopteran larvae, Manduca sexta.