Tuning the herbivore-induced ethylene burst: the role of transcript accumulation and ethylene perception in Nicotiana attenuata.
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.
von Dahl
Caroline C
CC
Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Beutenberg Campus, Hans-Knöll-Strasse 8, Jena, Germany.
Winz
Robert A
RA
Halitschke
Rayko
R
Kühnemann
Frank
F
Gase
Klaus
K
Baldwin
Ian T
IT
D000598:Amino Acids, Cyclic / Q000378:metabolism / Q000494:pharmacology; D000818:Animals; D005030:Ethylenes / Q000378:metabolism*; D005247:Feeding Behavior; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D020868:Gene Silencing; D018402:Manduca / Q000502:physiology*; D018749:RNA, Plant / Q000235:genetics / Q000378:metabolism*; D014026:Nicotiana / Q000235:genetics* / Q000378:metabolism*; D014158:Transcription, Genetic
D000598:Amino Acids, Cyclic; D005030:Ethylenes; D018749:RNA, Plant; C023863:1-aminocyclopropane-1-carboxylic acid; C036216:ethylene