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Tripartite parasitic and symbiotic interactions as a possible mechanism of horizontal gene transfer

Herbivory is a highly sophisticated feeding behavior that requires abilities of plant defense suppression, phytochemical detoxification, and plant macromolecule digestion. For plant‐sucking insects, salivary glands (SGs) play important roles in herbivory by secreting and injecting proteins into plan...

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Autores principales: Zhao, Chaoyang, Miao, Shaoming, Yin, Yanfang, Zhu, Yanjuan, Nabity, Paul, Bansal, Raman, Liu, Chenxi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8207144/
https://www.ncbi.nlm.nih.gov/pubmed/34141272
http://dx.doi.org/10.1002/ece3.7550
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author Zhao, Chaoyang
Miao, Shaoming
Yin, Yanfang
Zhu, Yanjuan
Nabity, Paul
Bansal, Raman
Liu, Chenxi
author_facet Zhao, Chaoyang
Miao, Shaoming
Yin, Yanfang
Zhu, Yanjuan
Nabity, Paul
Bansal, Raman
Liu, Chenxi
author_sort Zhao, Chaoyang
collection PubMed
description Herbivory is a highly sophisticated feeding behavior that requires abilities of plant defense suppression, phytochemical detoxification, and plant macromolecule digestion. For plant‐sucking insects, salivary glands (SGs) play important roles in herbivory by secreting and injecting proteins into plant tissues to facilitate feeding. Little is known on how insects evolved secretory SG proteins for such specialized functions. Here, we investigated the composition and evolution of secretory SG proteins in the brown marmorated stink bug (Halyomorpha halys) and identified a group of secretory SG phospholipase C (PLC) genes with highest sequence similarity to the bacterial homologs. Further analyses demonstrated that they were most closely related to PLCs of Xenorhabdus, a genus of Gammaproteobacteria living in symbiosis with insect‐parasitizing nematodes. These suggested that H. halys might acquire these PLCs from Xenorhabdus through the mechanism of horizontal gene transfer (HGT), likely mediated by a nematode during its parasitizing an insect host. We also showed that the original HGT event was followed by gene duplication and expansion, leading to functional diversification of the bacterial‐origin PLC genes in H. halys. Thus, this study suggested that an herbivore might enhance adaptation through gaining genes from an endosymbiont of its parasite in the tripartite parasitic and symbiotic interactions.
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spelling pubmed-82071442021-06-16 Tripartite parasitic and symbiotic interactions as a possible mechanism of horizontal gene transfer Zhao, Chaoyang Miao, Shaoming Yin, Yanfang Zhu, Yanjuan Nabity, Paul Bansal, Raman Liu, Chenxi Ecol Evol Original Research Herbivory is a highly sophisticated feeding behavior that requires abilities of plant defense suppression, phytochemical detoxification, and plant macromolecule digestion. For plant‐sucking insects, salivary glands (SGs) play important roles in herbivory by secreting and injecting proteins into plant tissues to facilitate feeding. Little is known on how insects evolved secretory SG proteins for such specialized functions. Here, we investigated the composition and evolution of secretory SG proteins in the brown marmorated stink bug (Halyomorpha halys) and identified a group of secretory SG phospholipase C (PLC) genes with highest sequence similarity to the bacterial homologs. Further analyses demonstrated that they were most closely related to PLCs of Xenorhabdus, a genus of Gammaproteobacteria living in symbiosis with insect‐parasitizing nematodes. These suggested that H. halys might acquire these PLCs from Xenorhabdus through the mechanism of horizontal gene transfer (HGT), likely mediated by a nematode during its parasitizing an insect host. We also showed that the original HGT event was followed by gene duplication and expansion, leading to functional diversification of the bacterial‐origin PLC genes in H. halys. Thus, this study suggested that an herbivore might enhance adaptation through gaining genes from an endosymbiont of its parasite in the tripartite parasitic and symbiotic interactions. John Wiley and Sons Inc. 2021-04-06 /pmc/articles/PMC8207144/ /pubmed/34141272 http://dx.doi.org/10.1002/ece3.7550 Text en © 2021 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research
Zhao, Chaoyang
Miao, Shaoming
Yin, Yanfang
Zhu, Yanjuan
Nabity, Paul
Bansal, Raman
Liu, Chenxi
Tripartite parasitic and symbiotic interactions as a possible mechanism of horizontal gene transfer
title Tripartite parasitic and symbiotic interactions as a possible mechanism of horizontal gene transfer
title_full Tripartite parasitic and symbiotic interactions as a possible mechanism of horizontal gene transfer
title_fullStr Tripartite parasitic and symbiotic interactions as a possible mechanism of horizontal gene transfer
title_full_unstemmed Tripartite parasitic and symbiotic interactions as a possible mechanism of horizontal gene transfer
title_short Tripartite parasitic and symbiotic interactions as a possible mechanism of horizontal gene transfer
title_sort tripartite parasitic and symbiotic interactions as a possible mechanism of horizontal gene transfer
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8207144/
https://www.ncbi.nlm.nih.gov/pubmed/34141272
http://dx.doi.org/10.1002/ece3.7550
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