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

Koichi Sugimoto, Kenji Matsui, Yoko Iijima, Yoshihiko Akakabe, Shoko Muramoto, Rika Ozawa, Masayoshi Uefune, Ryosuke Sasaki, Kabir Md Alamgir, Shota Akitake, Tatsunori Nobuke, Ivan Galis, Koh Aoki, Daisuke Shibata, Junji Takabayashi

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81 Citations (Scopus)

Abstract

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.

Original languageEnglish
Pages (from-to)7144-7149
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume111
Issue number19
DOIs
Publication statusPublished - May 13 2014

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Keywords

  • Defense induction
  • Glycosylation
  • Green leaf volatiles
  • Herbivore-infested plant volatiles
  • Plant-plant signaling

ASJC Scopus subject areas

  • General

Cite this

Sugimoto, K., Matsui, K., Iijima, Y., Akakabe, Y., Muramoto, S., Ozawa, R., Uefune, M., Sasaki, R., Alamgir, K. M., Akitake, S., Nobuke, T., Galis, I., Aoki, K., Shibata, D., & Takabayashi, J. (2014). Intake and transformation to a glycoside of (Z)-3-hexenol from infested neighbors reveals a mode of plant odor reception and defense. Proceedings of the National Academy of Sciences of the United States of America, 111(19), 7144-7149. https://doi.org/10.1073/pnas.1320660111