Integration of transcriptomics and network analysis reveals co-expressed genes in Frankliniella occidentalis larval guts that respond to tomato spotted wilt virus infection

Abstract Background The gut is the first barrier to infection by viruses that are internally borne and transmitted persistently by arthropod vectors to plant and animal hosts. Tomato spotted wilt virus (TSWV), a plant-pathogenic virus, is transmitted exclusively by thrips vectors in a circulative-pr...

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Autores principales:	Jinlong Han, Dorith Rotenberg
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Orthotospovirus Thysanoptera Virus-vector interactions Tomato spotted wilt virus Western flower thrips Larvae Biotechnology TP248.13-248.65 Genetics QH426-470
Acceso en línea:	https://doaj.org/article/ece0261cdd434e2a9a5ba7c288398dfc
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spelling	oai:doaj.org-article:ece0261cdd434e2a9a5ba7c288398dfc2021-11-14T12:26:44ZIntegration of transcriptomics and network analysis reveals co-expressed genes in Frankliniella occidentalis larval guts that respond to tomato spotted wilt virus infection10.1186/s12864-021-08100-41471-2164https://doaj.org/article/ece0261cdd434e2a9a5ba7c288398dfc2021-11-01T00:00:00Zhttps://doi.org/10.1186/s12864-021-08100-4https://doaj.org/toc/1471-2164Abstract Background The gut is the first barrier to infection by viruses that are internally borne and transmitted persistently by arthropod vectors to plant and animal hosts. Tomato spotted wilt virus (TSWV), a plant-pathogenic virus, is transmitted exclusively by thrips vectors in a circulative-propagative manner. Frankliniella occidentalis (western flower thrips), the principal thrips vector of TSWV, is transmission-competent only if the virus is acquired by young larvae. To begin to understand the larval gut response to TSWV infection and accumulation, a genome-assisted, transcriptomic analysis of F. occidentalis gut tissues of first (early L1) and second (early L2 and late L2) instar larvae was conducted using RNA-Seq to identify differentially-expressed transcripts (DETs) in response to TSWV compared to non-exposed cohorts. Results The larval gut responded in a developmental stage-dependent manner, with the majority of DETs (71%) associated with the early L1 stage at a time when virus infection is limited to the midgut epithelium. Provisional annotations of these DETs inferred roles in digestion and absorption, insect innate immunity, and detoxification. Weighted gene co-expression network analysis using all assembled transcripts of the gut transcriptome revealed eight gene modules that distinguish larval development. Intra-module interaction network analysis of the three most DET-enriched modules revealed ten central hub genes. Droplet digital PCR-expression analyses of select network hub and connecting genes revealed temporal changes in gut expression during and post exposure to TSWV. Conclusions These findings expand our understanding of the developmentally-mediated interaction between thrips vectors and orthotospoviruses, and provide opportunities for probing pathways for biomarkers of thrips vector competence.Jinlong HanDorith RotenbergBMCarticleOrthotospovirusThysanopteraVirus-vector interactionsTomato spotted wilt virusWestern flower thripsLarvaeBiotechnologyTP248.13-248.65GeneticsQH426-470ENBMC Genomics, Vol 22, Iss 1, Pp 1-17 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Orthotospovirus Thysanoptera Virus-vector interactions Tomato spotted wilt virus Western flower thrips Larvae Biotechnology TP248.13-248.65 Genetics QH426-470
spellingShingle	Orthotospovirus Thysanoptera Virus-vector interactions Tomato spotted wilt virus Western flower thrips Larvae Biotechnology TP248.13-248.65 Genetics QH426-470 Jinlong Han Dorith Rotenberg Integration of transcriptomics and network analysis reveals co-expressed genes in Frankliniella occidentalis larval guts that respond to tomato spotted wilt virus infection
description	Abstract Background The gut is the first barrier to infection by viruses that are internally borne and transmitted persistently by arthropod vectors to plant and animal hosts. Tomato spotted wilt virus (TSWV), a plant-pathogenic virus, is transmitted exclusively by thrips vectors in a circulative-propagative manner. Frankliniella occidentalis (western flower thrips), the principal thrips vector of TSWV, is transmission-competent only if the virus is acquired by young larvae. To begin to understand the larval gut response to TSWV infection and accumulation, a genome-assisted, transcriptomic analysis of F. occidentalis gut tissues of first (early L1) and second (early L2 and late L2) instar larvae was conducted using RNA-Seq to identify differentially-expressed transcripts (DETs) in response to TSWV compared to non-exposed cohorts. Results The larval gut responded in a developmental stage-dependent manner, with the majority of DETs (71%) associated with the early L1 stage at a time when virus infection is limited to the midgut epithelium. Provisional annotations of these DETs inferred roles in digestion and absorption, insect innate immunity, and detoxification. Weighted gene co-expression network analysis using all assembled transcripts of the gut transcriptome revealed eight gene modules that distinguish larval development. Intra-module interaction network analysis of the three most DET-enriched modules revealed ten central hub genes. Droplet digital PCR-expression analyses of select network hub and connecting genes revealed temporal changes in gut expression during and post exposure to TSWV. Conclusions These findings expand our understanding of the developmentally-mediated interaction between thrips vectors and orthotospoviruses, and provide opportunities for probing pathways for biomarkers of thrips vector competence.
format	article
author	Jinlong Han Dorith Rotenberg
author_facet	Jinlong Han Dorith Rotenberg
author_sort	Jinlong Han
title	Integration of transcriptomics and network analysis reveals co-expressed genes in Frankliniella occidentalis larval guts that respond to tomato spotted wilt virus infection
title_short	Integration of transcriptomics and network analysis reveals co-expressed genes in Frankliniella occidentalis larval guts that respond to tomato spotted wilt virus infection
title_full	Integration of transcriptomics and network analysis reveals co-expressed genes in Frankliniella occidentalis larval guts that respond to tomato spotted wilt virus infection
title_fullStr	Integration of transcriptomics and network analysis reveals co-expressed genes in Frankliniella occidentalis larval guts that respond to tomato spotted wilt virus infection
title_full_unstemmed	Integration of transcriptomics and network analysis reveals co-expressed genes in Frankliniella occidentalis larval guts that respond to tomato spotted wilt virus infection
title_sort	integration of transcriptomics and network analysis reveals co-expressed genes in frankliniella occidentalis larval guts that respond to tomato spotted wilt virus infection
publisher	BMC
publishDate	2021
url	https://doaj.org/article/ece0261cdd434e2a9a5ba7c288398dfc
work_keys_str_mv	AT jinlonghan integrationoftranscriptomicsandnetworkanalysisrevealscoexpressedgenesinfrankliniellaoccidentalislarvalgutsthatrespondtotomatospottedwiltvirusinfection AT dorithrotenberg integrationoftranscriptomicsandnetworkanalysisrevealscoexpressedgenesinfrankliniellaoccidentalislarvalgutsthatrespondtotomatospottedwiltvirusinfection
_version_	1718429262682259456

Integration of transcriptomics and network analysis reveals co-expressed genes in Frankliniella occidentalis larval guts that respond to tomato spotted wilt virus infection

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