TY - JOUR
T1 - Loliolide, a carotenoid metabolite, is a potential endogenous inducer of herbivore resistance
AU - Murata, Mika
AU - Nakai, Yusuke
AU - Kawazu, Kei
AU - Ishizaka, Masumi
AU - Kajiwara, Hideyuki
AU - Ab, Hiroshi
AU - Takeuchi, Kasumi
AU - Ichinose, Yuki
AU - Mitsuhara, Ichiro
AU - Mochizuki, Atsushi
AU - Seoa, Shigemi
N1 - Funding Information:
This work was supported by The Japanese Program for the Promotion of Basic and Applied Researches for Innovations in Biooriented Industry (BRAIN) and the Ministry of Education, Culture, Sports, Science and Technology (MEXT KAKENHI grant no. 25292037).
Funding Information:
1This work was supported by The Japanese Program for the Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry (BRAIN) and the Ministry of Education, Culture, Sports, Science and Technology (MEXT KAKENHI grant no. 25292037). 2These authors contributed equally to this article. 3Present address: Kyoyu Agri Co., Ltd., Nagano, 381-0006, Japan. 4Deceased November 2017. 5Author for contact: sseo71@affrc.go.jp. 6Senior author. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Shigemi Seo (sseo71@affrc.go.jp). S.S., M.M., Y.N., A.M., and I.M. designed the research;. M.M. and K.K. performed all assays using herbivores; M.M. and Y.N. conducted the molecular analysis of plants; S.S. performed the molecular analysis of plants and purification of loliolide; M.I. and H.K. conducted the mass spectrum analysis of loliolide; H.A., K.T., and Y.I. analyzed data; S.S., M.M., and Y.N. wrote the manuscript. [OPEN]Articles can be viewed without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.18.00837
Publisher Copyright:
© 2019 American Society of Plant Biologists. All rights reserved.
PY - 2019/4
Y1 - 2019/4
N2 - 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 virusinfected tobacco (Nicotiana tabacum) leaves in which a hypersensitive response (HR) was induced and identified as loliolide, which has been identified as a b-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 S. litura 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 b-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.
AB - 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 virusinfected tobacco (Nicotiana tabacum) leaves in which a hypersensitive response (HR) was induced and identified as loliolide, which has been identified as a b-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 S. litura 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 b-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.
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U2 - 10.1104/pp.18.00837
DO - 10.1104/pp.18.00837
M3 - Article
C2 - 30700538
AN - SCOPUS:85064195531
VL - 179
SP - 1822
EP - 1833
JO - Plant Physiology
JF - Plant Physiology
SN - 0032-0889
IS - 4
ER -