Loliolide, a Carotenoid Metabolite, Is a Potential Endogenous Inducer of Herbivore Resistance

Mika Murata, Yusuke Nakai, Kei Kawazu, Masumi Ishizaka, Hideyuki Kajiwara, Hiroshi Abe, Kasumi Takeuchi, Yuki Ichinose, Ichiro Mitsuhara, Atsushi Mochizuki, Shigemi Seo

Research output: Contribution to journalArticle

Abstract

Jasmonic acid (JA) plays an important role in the induction of herbivore resistance in many plants. However, JA-independent herbivore resistance has been suggested. An herbivore-resistance-inducing substance was isolated from Tobacco mosaic virus-infected tobacco (Nicotiana tabacum) leaves in which a hypersensitive response (HR) was induced and identified as loliolide, which has been identified as a β-carotene metabolite. When applied to tomato (Solanum lycopersicum) leaves, loliolide decreased the survival rate of the two-spotted spider mite, Tetranychus urticae, egg deposition by the same pest, and the survival rate of larvae of the common cutworm Spodoptera litura without exhibiting toxicity against these herbivores. Endogenous loliolide levels increased not only with an infestation by Slitura larvae, but also with the exogenous application of their oral secretions in tomato. A microarray analysis identified cell-wall-associated defense genes as loliolide-responsive tomato genes, and exogenous JA application did not induce the expression of these genes. Suppressor of zeaxanthin-less (szl), an Arabidopsis (Arabidopsis thaliana) mutant with a point mutation in a key gene of the β-carotene metabolic pathway, exhibited the decreased accumulation of endogenous loliolide and increased susceptibility to infestation by the western flower thrip (Frankliniella occidentalis). A pretreatment with loliolide decreased susceptibility to thrips in the JA-insensitive Arabidopsis mutant coronatine-insensitive1 Exogenous loliolide did not restore reduced electrolyte leakage in szl in response to a HR-inducing bacterial strain. These results suggest that loliolide functions as an endogenous signal that mediates defense responses to herbivores, possibly independently of JA, at least in tomato and Arabidopsis plants.

Original languageEnglish
Pages (from-to)1822-1833
Number of pages12
JournalPlant physiology
Volume179
Issue number4
DOIs
Publication statusPublished - Apr 1 2019

Fingerprint

Herbivory
Carotenoids
jasmonic acid
carotenoids
herbivores
metabolites
Lycopersicon esculentum
tomatoes
Arabidopsis
Frankliniella occidentalis
Tetranychus urticae
zeaxanthin
hypersensitive response
carotenes
Thysanoptera
survival rate
cutworms
mutants
Spodoptera litura
Tobacco mosaic virus

ASJC Scopus subject areas

  • Physiology
  • Genetics
  • Plant Science

Cite this

Murata, M., Nakai, Y., Kawazu, K., Ishizaka, M., Kajiwara, H., Abe, H., ... Seo, S. (2019). Loliolide, a Carotenoid Metabolite, Is a Potential Endogenous Inducer of Herbivore Resistance. Plant physiology, 179(4), 1822-1833. https://doi.org/10.1104/pp.18.00837

Loliolide, a Carotenoid Metabolite, Is a Potential Endogenous Inducer of Herbivore Resistance. / Murata, Mika; Nakai, Yusuke; Kawazu, Kei; Ishizaka, Masumi; Kajiwara, Hideyuki; Abe, Hiroshi; Takeuchi, Kasumi; Ichinose, Yuki; Mitsuhara, Ichiro; Mochizuki, Atsushi; Seo, Shigemi.

In: Plant physiology, Vol. 179, No. 4, 01.04.2019, p. 1822-1833.

Research output: Contribution to journalArticle

Murata, M, Nakai, Y, Kawazu, K, Ishizaka, M, Kajiwara, H, Abe, H, Takeuchi, K, Ichinose, Y, Mitsuhara, I, Mochizuki, A & Seo, S 2019, 'Loliolide, a Carotenoid Metabolite, Is a Potential Endogenous Inducer of Herbivore Resistance', Plant physiology, vol. 179, no. 4, pp. 1822-1833. https://doi.org/10.1104/pp.18.00837
Murata M, Nakai Y, Kawazu K, Ishizaka M, Kajiwara H, Abe H et al. Loliolide, a Carotenoid Metabolite, Is a Potential Endogenous Inducer of Herbivore Resistance. Plant physiology. 2019 Apr 1;179(4):1822-1833. https://doi.org/10.1104/pp.18.00837
Murata, Mika ; Nakai, Yusuke ; Kawazu, Kei ; Ishizaka, Masumi ; Kajiwara, Hideyuki ; Abe, Hiroshi ; Takeuchi, Kasumi ; Ichinose, Yuki ; Mitsuhara, Ichiro ; Mochizuki, Atsushi ; Seo, Shigemi. / Loliolide, a Carotenoid Metabolite, Is a Potential Endogenous Inducer of Herbivore Resistance. In: Plant physiology. 2019 ; Vol. 179, No. 4. pp. 1822-1833.
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