Groundnut Bud Necrosis Virus Modulates the Expression of Innate Immune, Endocytosis, and Cuticle Development-Associated Genes to Circulate and Propagate in Its Vector, Thrips palmi

Thrips palmi (Thysanoptera: Thripidae) is the predominant tospovirus vector in Asia-Pacific region. It transmits economically damaging groundnut bud necrosis virus (GBNV, family Tospoviridae) in a persistent propagative manner. Thrips serve as the alternate host, and virus reservoirs making tospovir...

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Main Authors: Deepak Kumar Mahanta, Sumit Jangra, Priti, Amalendu Ghosh, Parva Kumar Sharma, Mir Asif Iquebal, Sarika Jaiswal, Virendra Kumar Baranwal, Vinay Kumari Kalia, Subhas Chander
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-03-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.773238/full
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author Deepak Kumar Mahanta
Deepak Kumar Mahanta
Sumit Jangra
Priti
Amalendu Ghosh
Parva Kumar Sharma
Mir Asif Iquebal
Sarika Jaiswal
Virendra Kumar Baranwal
Vinay Kumari Kalia
Subhas Chander
author_facet Deepak Kumar Mahanta
Deepak Kumar Mahanta
Sumit Jangra
Priti
Amalendu Ghosh
Parva Kumar Sharma
Mir Asif Iquebal
Sarika Jaiswal
Virendra Kumar Baranwal
Vinay Kumari Kalia
Subhas Chander
author_sort Deepak Kumar Mahanta
collection DOAJ
description Thrips palmi (Thysanoptera: Thripidae) is the predominant tospovirus vector in Asia-Pacific region. It transmits economically damaging groundnut bud necrosis virus (GBNV, family Tospoviridae) in a persistent propagative manner. Thrips serve as the alternate host, and virus reservoirs making tospovirus management very challenging. Insecticides and host plant resistance remain ineffective in managing thrips–tospoviruses. Recent genomic approaches have led to understanding the molecular interactions of thrips–tospoviruses and identifying novel genetic targets. However, most of the studies are limited to Frankliniella species and tomato spotted wilt virus (TSWV). Amidst the limited information available on T. palmi–tospovirus relationships, the present study is the first report of the transcriptome-wide response of T. palmi associated with GBNV infection. The differential expression analyses of the triplicate transcriptome of viruliferous vs. nonviruliferous adult T. palmi identified a total of 2,363 (1,383 upregulated and 980 downregulated) significant transcripts. The Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analyses showed the abundance of differentially expressed genes (DEGs) involved in innate immune response, endocytosis, cuticle development, and receptor binding and signaling that mediate the virus invasion and multiplication in the vector system. Also, the gene regulatory network (GRN) of most significant DEGs showed the genes like ABC transporter, cytochrome P450, endocuticle structural glycoprotein, gamma-aminobutyric acid (GABA) receptor, heat shock protein 70, larval and pupal cuticle proteins, nephrin, proline-rich protein, sperm-associated antigen, UHRF1-binding protein, serpin, tyrosine–protein kinase receptor, etc., were enriched with higher degrees of interactions. Further, the expression of the candidate genes in response to GBNV infection was validated in reverse transcriptase-quantitative real-time PCR (RT-qPCR). This study leads to an understanding of molecular interactions between T. palmi and GBNV and suggests potential genetic targets for generic pest control.
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spelling doaj.art-ce242ae4871e45558e3b5d9ab44291292022-12-22T00:03:45ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-03-011310.3389/fmicb.2022.773238773238Groundnut Bud Necrosis Virus Modulates the Expression of Innate Immune, Endocytosis, and Cuticle Development-Associated Genes to Circulate and Propagate in Its Vector, Thrips palmiDeepak Kumar Mahanta0Deepak Kumar Mahanta1Sumit Jangra2 Priti3Amalendu Ghosh4Parva Kumar Sharma5Mir Asif Iquebal6Sarika Jaiswal7Virendra Kumar Baranwal8Vinay Kumari Kalia9Subhas Chander10Insect Vector Laboratory, Advanced Centre for Plant Virology, ICAR-Indian Agricultural Research Institute, New Delhi, IndiaDivision of Entomology, ICAR-Indian Agricultural Research Institute, New Delhi, IndiaInsect Vector Laboratory, Advanced Centre for Plant Virology, ICAR-Indian Agricultural Research Institute, New Delhi, IndiaInsect Vector Laboratory, Advanced Centre for Plant Virology, ICAR-Indian Agricultural Research Institute, New Delhi, IndiaInsect Vector Laboratory, Advanced Centre for Plant Virology, ICAR-Indian Agricultural Research Institute, New Delhi, IndiaCenter for Agricultural Bioinformatics, ICAR-Indian Agricultural Statistics Research Institute, New Delhi, IndiaCenter for Agricultural Bioinformatics, ICAR-Indian Agricultural Statistics Research Institute, New Delhi, IndiaCenter for Agricultural Bioinformatics, ICAR-Indian Agricultural Statistics Research Institute, New Delhi, IndiaInsect Vector Laboratory, Advanced Centre for Plant Virology, ICAR-Indian Agricultural Research Institute, New Delhi, IndiaDivision of Entomology, ICAR-Indian Agricultural Research Institute, New Delhi, IndiaICAR- National Research Centre for Integrated Pest Management, New Delhi, IndiaThrips palmi (Thysanoptera: Thripidae) is the predominant tospovirus vector in Asia-Pacific region. It transmits economically damaging groundnut bud necrosis virus (GBNV, family Tospoviridae) in a persistent propagative manner. Thrips serve as the alternate host, and virus reservoirs making tospovirus management very challenging. Insecticides and host plant resistance remain ineffective in managing thrips–tospoviruses. Recent genomic approaches have led to understanding the molecular interactions of thrips–tospoviruses and identifying novel genetic targets. However, most of the studies are limited to Frankliniella species and tomato spotted wilt virus (TSWV). Amidst the limited information available on T. palmi–tospovirus relationships, the present study is the first report of the transcriptome-wide response of T. palmi associated with GBNV infection. The differential expression analyses of the triplicate transcriptome of viruliferous vs. nonviruliferous adult T. palmi identified a total of 2,363 (1,383 upregulated and 980 downregulated) significant transcripts. The Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analyses showed the abundance of differentially expressed genes (DEGs) involved in innate immune response, endocytosis, cuticle development, and receptor binding and signaling that mediate the virus invasion and multiplication in the vector system. Also, the gene regulatory network (GRN) of most significant DEGs showed the genes like ABC transporter, cytochrome P450, endocuticle structural glycoprotein, gamma-aminobutyric acid (GABA) receptor, heat shock protein 70, larval and pupal cuticle proteins, nephrin, proline-rich protein, sperm-associated antigen, UHRF1-binding protein, serpin, tyrosine–protein kinase receptor, etc., were enriched with higher degrees of interactions. Further, the expression of the candidate genes in response to GBNV infection was validated in reverse transcriptase-quantitative real-time PCR (RT-qPCR). This study leads to an understanding of molecular interactions between T. palmi and GBNV and suggests potential genetic targets for generic pest control.https://www.frontiersin.org/articles/10.3389/fmicb.2022.773238/fullmelon thripstospovirusvirus–vector relationshipRT-qPCRtranscriptome
spellingShingle Deepak Kumar Mahanta
Deepak Kumar Mahanta
Sumit Jangra
Priti
Amalendu Ghosh
Parva Kumar Sharma
Mir Asif Iquebal
Sarika Jaiswal
Virendra Kumar Baranwal
Vinay Kumari Kalia
Subhas Chander
Groundnut Bud Necrosis Virus Modulates the Expression of Innate Immune, Endocytosis, and Cuticle Development-Associated Genes to Circulate and Propagate in Its Vector, Thrips palmi
Frontiers in Microbiology
melon thrips
tospovirus
virus–vector relationship
RT-qPCR
transcriptome
title Groundnut Bud Necrosis Virus Modulates the Expression of Innate Immune, Endocytosis, and Cuticle Development-Associated Genes to Circulate and Propagate in Its Vector, Thrips palmi
title_full Groundnut Bud Necrosis Virus Modulates the Expression of Innate Immune, Endocytosis, and Cuticle Development-Associated Genes to Circulate and Propagate in Its Vector, Thrips palmi
title_fullStr Groundnut Bud Necrosis Virus Modulates the Expression of Innate Immune, Endocytosis, and Cuticle Development-Associated Genes to Circulate and Propagate in Its Vector, Thrips palmi
title_full_unstemmed Groundnut Bud Necrosis Virus Modulates the Expression of Innate Immune, Endocytosis, and Cuticle Development-Associated Genes to Circulate and Propagate in Its Vector, Thrips palmi
title_short Groundnut Bud Necrosis Virus Modulates the Expression of Innate Immune, Endocytosis, and Cuticle Development-Associated Genes to Circulate and Propagate in Its Vector, Thrips palmi
title_sort groundnut bud necrosis virus modulates the expression of innate immune endocytosis and cuticle development associated genes to circulate and propagate in its vector thrips palmi
topic melon thrips
tospovirus
virus–vector relationship
RT-qPCR
transcriptome
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.773238/full
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