Tuning the herbivore‐induced ethylene burst: the role of transcript accumulation and ethylene perception in Nicotiana attenuata

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Abstract
Caterpillar-induced ethylene emissions play an important role in plant–herbivore interactions. The ethylene burst that ensues after attack exceeds wound-induced ethylene emissions, but the mechanisms responsible remain unknown. Adding larval oral secretions (OS) to wounds mimics this ethylene burst. We demonstrate that fatty acid–amino acid conjugates are the responsible elicitors in Manduca sexta OS, and identify genes that are important in OS-elicited ethylene biosynthesis and perception in the larvae’s host, Nicotiana attenuata, by examining the consequences of gene silencing on OS-elicited ethylene emissions, as quantified by photo-acoustic spectroscopy. OS elicitation increased transcript accumulation of ACC synthase (ACS), virus-induced gene silencing of ACS halved the OS-elicited ethylene release, and ACC supplementation to ACS-silenced plants restored ethylene emissions, demonstrating that ACS activity limits the rate of release. Silencing three wound- or OS-elicited ACC oxidase (ACO) genes with an ACO consensus fragment abolished the OS-elicited ethylene release. Virus-induced gene silencing of each ACO individually revealed that only NaACO2a and NaACO3 regulate the OS-elicited ethylene release. Transforming plants with various etr1-1 constructs rendered them differentially ‘deaf’ to ethylene, and dramatically increased the OS-elicited ethylene burst, largely without regulating the transcripts of biosynthetic genes. The volume of the OS-elicited ethylene ‘scream’ was proportional to the plant’s deafness, as determined by 1-MCP treatments. We conclude that the OS-elicited ethylene burst is tuned by a tag-team of transcriptional responses and ethylene perception. Ethylene signaling is shown to be essential in regulating two traits that are important in the N. attenuata–M. sexta interaction: OS-induced nicotine levels and floral longevity.