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Characterization of a Novel Insect-Induced Sesquiterpene Synthase GbTPS1 Based on the Transcriptome of Gossypium barbadense Feeding by Cotton Bollworm
When attacked by insect herbivores, plants initiate sophisticated defenses mediated by complex signaling networks and usually release a blend of functional volatiles such as terpenes against infestation. The extra-long staple cotton Gossypium barbadense cultivated worldwide as natural textile fiber...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9326391/ https://www.ncbi.nlm.nih.gov/pubmed/35909734 http://dx.doi.org/10.3389/fpls.2022.898541 |
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author | Zhang, Hang Liu, Enliang Huang, Xinzheng Kou, Junfeng Teng, Dong Lv, Beibei Han, Xiaoqiang Zhang, Yongjun |
author_facet | Zhang, Hang Liu, Enliang Huang, Xinzheng Kou, Junfeng Teng, Dong Lv, Beibei Han, Xiaoqiang Zhang, Yongjun |
author_sort | Zhang, Hang |
collection | PubMed |
description | When attacked by insect herbivores, plants initiate sophisticated defenses mediated by complex signaling networks and usually release a blend of functional volatiles such as terpenes against infestation. The extra-long staple cotton Gossypium barbadense cultivated worldwide as natural textile fiber crop is frequently exposed to a variety of herbivores, such as cotton bollworm Helicoverpa armigera. However, little is known about insect-induced transcriptional changes and molecular mechanisms underlying subsequent defense responses in G. barbadense. In the current study, transcriptome changes in G. barbadense infested with chewing H. armigera larvae were investigated, and we identified 5,629 differentially expressed genes (DEGs) in the infested cotton leaves compared with non-infested controls. H. armigera feeding triggered complex signaling networks in which almost all (88 out of 90) DEGs associated with the jasmonic acid (JA) pathway were upregulated, highlighting a central role for JA in the defense responses of G. barbadense against target insects. All DEGs involved in growth-related photosynthesis were downregulated, whereas most DEGs associated with defense-related transcript factors and volatile secondary metabolism were upregulated. It was noteworthy that a terpene synthase gene in the transcriptome data, GbTPS1, was strongly expressed in H. armigera-infested G. barbadense leaves. The upregulation of GbTPS1 in qPCR analysis also suggested an important role for GbTPS1 in herbivore-induced cotton defense. In vitro assays showed that recombinant GbTPS1 catalyzed farnesyl pyrophosphate and neryl diphosphate to produce three sesquiterpenes (selinene, α-gurjunene, and β-elemene) and one monoterpene (limonene), respectively. Moreover, these catalytic products of GbTPS1 were significantly elevated in G. barbadense leaves after H. armigera infestation, and elemene and limonene had repellent effects on H. armigera larvae in a dual-choice bioassay and increased larval mortality in a no-choice bioassay. These findings provide a valuable insight into understanding the transcriptional changes reprogramming herbivore-induced sesquiterpene biosynthesis in G. barbadense infested by H. armigera, which help elucidate the molecular mechanisms underlying plant defense against insect pests. |
format | Online Article Text |
id | pubmed-9326391 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-93263912022-07-28 Characterization of a Novel Insect-Induced Sesquiterpene Synthase GbTPS1 Based on the Transcriptome of Gossypium barbadense Feeding by Cotton Bollworm Zhang, Hang Liu, Enliang Huang, Xinzheng Kou, Junfeng Teng, Dong Lv, Beibei Han, Xiaoqiang Zhang, Yongjun Front Plant Sci Plant Science When attacked by insect herbivores, plants initiate sophisticated defenses mediated by complex signaling networks and usually release a blend of functional volatiles such as terpenes against infestation. The extra-long staple cotton Gossypium barbadense cultivated worldwide as natural textile fiber crop is frequently exposed to a variety of herbivores, such as cotton bollworm Helicoverpa armigera. However, little is known about insect-induced transcriptional changes and molecular mechanisms underlying subsequent defense responses in G. barbadense. In the current study, transcriptome changes in G. barbadense infested with chewing H. armigera larvae were investigated, and we identified 5,629 differentially expressed genes (DEGs) in the infested cotton leaves compared with non-infested controls. H. armigera feeding triggered complex signaling networks in which almost all (88 out of 90) DEGs associated with the jasmonic acid (JA) pathway were upregulated, highlighting a central role for JA in the defense responses of G. barbadense against target insects. All DEGs involved in growth-related photosynthesis were downregulated, whereas most DEGs associated with defense-related transcript factors and volatile secondary metabolism were upregulated. It was noteworthy that a terpene synthase gene in the transcriptome data, GbTPS1, was strongly expressed in H. armigera-infested G. barbadense leaves. The upregulation of GbTPS1 in qPCR analysis also suggested an important role for GbTPS1 in herbivore-induced cotton defense. In vitro assays showed that recombinant GbTPS1 catalyzed farnesyl pyrophosphate and neryl diphosphate to produce three sesquiterpenes (selinene, α-gurjunene, and β-elemene) and one monoterpene (limonene), respectively. Moreover, these catalytic products of GbTPS1 were significantly elevated in G. barbadense leaves after H. armigera infestation, and elemene and limonene had repellent effects on H. armigera larvae in a dual-choice bioassay and increased larval mortality in a no-choice bioassay. These findings provide a valuable insight into understanding the transcriptional changes reprogramming herbivore-induced sesquiterpene biosynthesis in G. barbadense infested by H. armigera, which help elucidate the molecular mechanisms underlying plant defense against insect pests. Frontiers Media S.A. 2022-07-13 /pmc/articles/PMC9326391/ /pubmed/35909734 http://dx.doi.org/10.3389/fpls.2022.898541 Text en Copyright © 2022 Zhang, Liu, Huang, Kou, Teng, Lv, Han and Zhang. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Plant Science Zhang, Hang Liu, Enliang Huang, Xinzheng Kou, Junfeng Teng, Dong Lv, Beibei Han, Xiaoqiang Zhang, Yongjun Characterization of a Novel Insect-Induced Sesquiterpene Synthase GbTPS1 Based on the Transcriptome of Gossypium barbadense Feeding by Cotton Bollworm |
title | Characterization of a Novel Insect-Induced Sesquiterpene Synthase GbTPS1 Based on the Transcriptome of Gossypium barbadense Feeding by Cotton Bollworm |
title_full | Characterization of a Novel Insect-Induced Sesquiterpene Synthase GbTPS1 Based on the Transcriptome of Gossypium barbadense Feeding by Cotton Bollworm |
title_fullStr | Characterization of a Novel Insect-Induced Sesquiterpene Synthase GbTPS1 Based on the Transcriptome of Gossypium barbadense Feeding by Cotton Bollworm |
title_full_unstemmed | Characterization of a Novel Insect-Induced Sesquiterpene Synthase GbTPS1 Based on the Transcriptome of Gossypium barbadense Feeding by Cotton Bollworm |
title_short | Characterization of a Novel Insect-Induced Sesquiterpene Synthase GbTPS1 Based on the Transcriptome of Gossypium barbadense Feeding by Cotton Bollworm |
title_sort | characterization of a novel insect-induced sesquiterpene synthase gbtps1 based on the transcriptome of gossypium barbadense feeding by cotton bollworm |
topic | Plant Science |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9326391/ https://www.ncbi.nlm.nih.gov/pubmed/35909734 http://dx.doi.org/10.3389/fpls.2022.898541 |
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