Intake and transformation to a glycoside of (Z)-3-hexenol from infested neighbors reveals a mode of plant odor reception and defense

Plants receive volatile compounds emitted by neighboring plants that are infested by herbivores, and consequently the receiver plants begin to defend against forthcoming herbivory. However, to date, how plants receive volatiles and, consequently, how they fortify their defenses, is largely unknown....

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Published in:	Proceedings of the National Academy of Sciences - PNAS Vol. 111; no. 19; pp. 7144 - 7149
Main Authors:	Sugimoto, Koichi, Matsui, Kenji, Iijima, Yoko, Akakabe, Yoshihiko, Muramoto, Shoko, Ozawa, Rika, Uefune, Masayoshi, Sasaki, Ryosuke, Alamgir, Kabir Md, Akitake, Shota, Nobuke, Tatsunori, Galis, Ivan, Aoki, Koh, Shibata, Daisuke, Takabayashi, Junji
Format:	Journal Article
Language:	English
Published:	United States National Academy of Sciences 13-05-2014 National Acad Sciences
Series:	From the Cover
Subjects:	Animals Artificial diets Biological Sciences Biosynthesis Cyclopentanes - metabolism Cyclopentanes - pharmacology Diet Glycosides Glycosides - metabolism Herbivores Herbivory - physiology Hexanols - metabolism Larva - physiology Leaves Lycopersicon esculentum Lycopersicon esculentum - drug effects Lycopersicon esculentum - metabolism Lycopersicon esculentum - parasitology Odorants Odors Oxylipins - metabolism Oxylipins - pharmacology Plant cells Plant Leaves - metabolism Plants Polyphenols Spodoptera - growth & development Survival rates Tomatoes Volatile Organic Compounds - metabolism Weight gain Worms green leaf volatiles defense induction glycosylation herbivore-infested plant volatiles plant–plant signaling
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Summary:	Plants receive volatile compounds emitted by neighboring plants that are infested by herbivores, and consequently the receiver plants begin to defend against forthcoming herbivory. However, to date, how plants receive volatiles and, consequently, how they fortify their defenses, is largely unknown. In this study, we found that undamaged tomato plants exposed to volatiles emitted by conspecifics infested with common cutworms (exposed plants) became more defensive against the larvae than those exposed to volatiles from uninfested conspecifics (control plants) in a constant airflow system under laboratory conditions. Comprehensive metabolite analyses showed that only the amount of (Z)-3-hexenylvicianoside (HexVic) was higher in exposed than control plants. This compound negatively affected the performance of common cutworms when added to an artificial diet. The aglycon of HexVic, (Z)-3-hexenol, was obtained from neighboring infested plants via the air. The amount of jasmonates (JAs) was not higher in exposed plants, and HexVic biosynthesis was independent of JA signaling. The use of (Z)-3-hexenol from neighboring damaged conspecifics for HexVic biosynthesis in exposed plants was also observed in an experimental field, indicating that (Z)-3-hexenol intake occurred even under fluctuating environmental conditions. Specific use of airborne (Z)-3-hexenol to form HexVic in undamaged tomato plants reveals a previously unidentified mechanism of plant defense.
Bibliography:	http://dx.doi.org/10.1073/pnas.1320660111 ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by Rodney B. Croteau, Washington State University, Pullman, WA, and approved March 20, 2014 (received for review November 2, 2013) Author contributions: K.S., K.M., and J.T. designed research; K.S., Y.A., S.M., K.M.A., S.A., T.N., and I.G. performed research; Y.I., R.S., K.A., and D.S. contributed new reagents/analytic tools; K.S., K.M., Y.I., R.O., M.U., and J.T. analyzed data; and K.S., K.M., and J.T. wrote the paper. 3Present address: Graduate School of Life and Environmental Sciences, Osaka Prefectural University, Gakuen-cho 1-1, Nakaku, Sakai, Osaka 599-8531, Japan. 2Present address: Department of Nutrition and Life Science, Kanagawa Institute of Technology, Shimo-ogino 1030, Atsugi, Kanagawa 243-0292, Japan.
ISSN:	0027-8424 1091-6490
DOI:	10.1073/pnas.1320660111