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. 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.
Graduate School of Medicine (Faculty of Agriculture), Yamaguchi University, Yoshida 1677-1, Yamaguchi 753-8515, Japan;Center for Ecological Research, Kyoto University, Otsu, Shiga 520-2113, Japan;
Koichi
K
Sugimoto
Graduate School of Medicine (Faculty of Agriculture), Yamaguchi University, Yoshida 1677-1, Yamaguchi 753-8515, Japan; matsui@yamaguchi-u.ac.jp.
Kenji
K
Matsui
Kazusa DNA Research Institute, Kisarazu, Chiba 292-0818, Japan; and.
Yoko
Y
Iijima
Graduate School of Medicine (Faculty of Agriculture), Yamaguchi University, Yoshida 1677-1, Yamaguchi 753-8515, Japan;
Yoshihiko
Y
Akakabe
Graduate School of Medicine (Faculty of Agriculture), Yamaguchi University, Yoshida 1677-1, Yamaguchi 753-8515, Japan;
Shoko
S
Muramoto
Center for Ecological Research, Kyoto University, Otsu, Shiga 520-2113, Japan;
Rika
R
Ozawa
Center for Ecological Research, Kyoto University, Otsu, Shiga 520-2113, Japan;
Masayoshi
M
Uefune
Kazusa DNA Research Institute, Kisarazu, Chiba 292-0818, Japan; and.
Ryosuke
R
Sasaki
Institute of Plant Science and Resources, Okayama University, Kurashiki, Okayama 710-0046, Japan.
Kabir Md
KM
Alamgir
Graduate School of Medicine (Faculty of Agriculture), Yamaguchi University, Yoshida 1677-1, Yamaguchi 753-8515, Japan;
Shota
S
Akitake
Graduate School of Medicine (Faculty of Agriculture), Yamaguchi University, Yoshida 1677-1, Yamaguchi 753-8515, Japan;
Tatsunori
T
Nobuke
Institute of Plant Science and Resources, Okayama University, Kurashiki, Okayama 710-0046, Japan.
Ivan
I
Galis
Kazusa DNA Research Institute, Kisarazu, Chiba 292-0818, Japan; and.
Koh
K
Aoki
Kazusa DNA Research Institute, Kisarazu, Chiba 292-0818, Japan; and.
Daisuke
D
Shibata
Center for Ecological Research, Kyoto University, Otsu, Shiga 520-2113, Japan;
Junji
J
Takabayashi
D000818:Animals; D003517:Cyclopentanes / Q000378:metabolism / Q000494:pharmacology; D006027:Glycosides / Q000378:metabolism; D060434:Herbivory / Q000502:physiology; D000441:Hexanols / Q000378:metabolism*; D007814:Larva / Q000502:physiology; D018551:Solanum lycopersicum / Q000187:drug effects / Q000378:metabolism* / Q000469:parasitology*; D009812:Odorants; D054883:Oxylipins / Q000378:metabolism / Q000494:pharmacology; D018515:Plant Leaves / Q000378:metabolism; D018411:Spodoptera / Q000254:growth & development*; D055549:Volatile Organic Compounds / Q000378:metabolism
D003517:Cyclopentanes; D006027:Glycosides; D000441:Hexanols; D054883:Oxylipins; D055549:Volatile Organic Compounds; C011006:jasmonic acid
defense induction; glycosylation; green leaf volatiles; herbivore-infested plant volatiles; plant–plant signaling