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A green leaf volatile, (Z)-3-hexenyl-acetate, mediates differential oviposition by Spodoptera frugiperda on maize and rice

BACKGROUND: Insects rely on chemosensory perception, mainly olfaction, for the location of mates, food sources, and oviposition sites. Plant-released volatile compounds guide herbivorous insects to search for and locate their host plants, further helping them to identify suitable positions for ovipo...

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Autores principales: Wang, Jiali, Wei, Jiaqi, Yi, Ting, Li, Ya-Ya, Xu, Tian, Chen, Li, Xu, Hanhong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10280969/
https://www.ncbi.nlm.nih.gov/pubmed/37337192
http://dx.doi.org/10.1186/s12915-023-01642-x
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author Wang, Jiali
Wei, Jiaqi
Yi, Ting
Li, Ya-Ya
Xu, Tian
Chen, Li
Xu, Hanhong
author_facet Wang, Jiali
Wei, Jiaqi
Yi, Ting
Li, Ya-Ya
Xu, Tian
Chen, Li
Xu, Hanhong
author_sort Wang, Jiali
collection PubMed
description BACKGROUND: Insects rely on chemosensory perception, mainly olfaction, for the location of mates, food sources, and oviposition sites. Plant-released volatile compounds guide herbivorous insects to search for and locate their host plants, further helping them to identify suitable positions for oviposition. The fall armyworm Spodoptera frugiperda (S. frugiperda) was found to invade China in 2019 and has since seriously threatened multiple crops, particularly maize and rice. However, the chemical and molecular mechanisms underlying oviposition preference in this pest are not fully understood. Here, the oviposition preference of S. frugiperda on maize and rice plants was investigated. RESULTS: GC-EAD and GC–MS/MS techniques were used to identify the antennally active volatiles from maize and rice plants. The attraction and oviposition stimulation of identified components to female adults were tested in both laboratory and field settings. The odorant receptors (ORs) on female antennae were expressed in Xenopus oocytes, and their functions evaluated by RNAi. Ten and eleven compounds of maize and rice plants, respectively, were identified to possess electrophysiological activity from headspace volatiles. Among these compounds, (Z)-3-hexenyl-acetate specifically presented in maize volatiles was found to play a critical role in attracting females and stimulating oviposition compared to rice volatiles. Among the cloned ORs on the antennae of both sexes, SfruOR23 with highly female-biased expression mediated the responses of females to (Z)-3-hexenyl-acetate. Knockdown of SfruOR23 using RNAi markedly reduced the electrophysiological response of female antennae and oviposition preference to the compound. CONCLUSIONS: (Z)-3-Hexenyl-acetate is a key volatile mediating the host and oviposition preference of S. frugiperda on maize. The olfactory receptor of (Z)-3-hexenyl-acetate was identified to be SfruOR23, which is mainly expressed in the antennae of S. frugiperda. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01642-x.
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spelling pubmed-102809692023-06-21 A green leaf volatile, (Z)-3-hexenyl-acetate, mediates differential oviposition by Spodoptera frugiperda on maize and rice Wang, Jiali Wei, Jiaqi Yi, Ting Li, Ya-Ya Xu, Tian Chen, Li Xu, Hanhong BMC Biol Research Article BACKGROUND: Insects rely on chemosensory perception, mainly olfaction, for the location of mates, food sources, and oviposition sites. Plant-released volatile compounds guide herbivorous insects to search for and locate their host plants, further helping them to identify suitable positions for oviposition. The fall armyworm Spodoptera frugiperda (S. frugiperda) was found to invade China in 2019 and has since seriously threatened multiple crops, particularly maize and rice. However, the chemical and molecular mechanisms underlying oviposition preference in this pest are not fully understood. Here, the oviposition preference of S. frugiperda on maize and rice plants was investigated. RESULTS: GC-EAD and GC–MS/MS techniques were used to identify the antennally active volatiles from maize and rice plants. The attraction and oviposition stimulation of identified components to female adults were tested in both laboratory and field settings. The odorant receptors (ORs) on female antennae were expressed in Xenopus oocytes, and their functions evaluated by RNAi. Ten and eleven compounds of maize and rice plants, respectively, were identified to possess electrophysiological activity from headspace volatiles. Among these compounds, (Z)-3-hexenyl-acetate specifically presented in maize volatiles was found to play a critical role in attracting females and stimulating oviposition compared to rice volatiles. Among the cloned ORs on the antennae of both sexes, SfruOR23 with highly female-biased expression mediated the responses of females to (Z)-3-hexenyl-acetate. Knockdown of SfruOR23 using RNAi markedly reduced the electrophysiological response of female antennae and oviposition preference to the compound. CONCLUSIONS: (Z)-3-Hexenyl-acetate is a key volatile mediating the host and oviposition preference of S. frugiperda on maize. The olfactory receptor of (Z)-3-hexenyl-acetate was identified to be SfruOR23, which is mainly expressed in the antennae of S. frugiperda. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01642-x. BioMed Central 2023-06-19 /pmc/articles/PMC10280969/ /pubmed/37337192 http://dx.doi.org/10.1186/s12915-023-01642-x Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Wang, Jiali
Wei, Jiaqi
Yi, Ting
Li, Ya-Ya
Xu, Tian
Chen, Li
Xu, Hanhong
A green leaf volatile, (Z)-3-hexenyl-acetate, mediates differential oviposition by Spodoptera frugiperda on maize and rice
title A green leaf volatile, (Z)-3-hexenyl-acetate, mediates differential oviposition by Spodoptera frugiperda on maize and rice
title_full A green leaf volatile, (Z)-3-hexenyl-acetate, mediates differential oviposition by Spodoptera frugiperda on maize and rice
title_fullStr A green leaf volatile, (Z)-3-hexenyl-acetate, mediates differential oviposition by Spodoptera frugiperda on maize and rice
title_full_unstemmed A green leaf volatile, (Z)-3-hexenyl-acetate, mediates differential oviposition by Spodoptera frugiperda on maize and rice
title_short A green leaf volatile, (Z)-3-hexenyl-acetate, mediates differential oviposition by Spodoptera frugiperda on maize and rice
title_sort green leaf volatile, (z)-3-hexenyl-acetate, mediates differential oviposition by spodoptera frugiperda on maize and rice
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10280969/
https://www.ncbi.nlm.nih.gov/pubmed/37337192
http://dx.doi.org/10.1186/s12915-023-01642-x
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