Comprehensive transcriptomic analysis reveals turnip mosaic virus infection and its aphid vector Myzus persicae cause large changes in gene regulatory networks and co-transcription of alternative spliced mRNAs in Arabidopsis thaliana

Abstract Background Virus infection and herbivory can alter the expression of stress-responsive genes in plants. This study employed high-throughput transcriptomic and alternative splicing analysis to understand the separate and combined impacts on host gene expression in Arabidopsis thaliana by Myz...

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Main Authors: Venura Herath, Clare L. Casteel, Jeanmarie Verchot
Format: Article
Language:English
Published: BMC 2025-01-01
Series:BMC Plant Biology
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Online Access:https://doi.org/10.1186/s12870-024-06014-3
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author Venura Herath
Clare L. Casteel
Jeanmarie Verchot
author_facet Venura Herath
Clare L. Casteel
Jeanmarie Verchot
author_sort Venura Herath
collection DOAJ
description Abstract Background Virus infection and herbivory can alter the expression of stress-responsive genes in plants. This study employed high-throughput transcriptomic and alternative splicing analysis to understand the separate and combined impacts on host gene expression in Arabidopsis thaliana by Myzus persicae (green peach aphid), and turnip mosaic virus (TuMV). Results By investigating changes in transcript abundance, the data shows that aphids feeding on virus infected plants intensify the number of differentially expressed stress responsive genes compared to challenge by individual stressors. This study presents evidence that the combination of virus-vector-host interactions induces significant changes in hormone and secondary metabolite biosynthesis, as well as downstream factors involved in feedback loops within hormone signaling pathways. This study also shows that gene expressions are regulated through alternative pre-mRNA splicing and the use of alternative transcription start and termination sites. Conclusions These combined data suggest that complex genetic changes occur as plants adapt to the combined challenges posed by aphids and the viruses they vector. This study also provides more advanced analyses that could be used in the future to dissect the genetic mechanisms mediating tripartite interactions and inform future breeding programs.
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publishDate 2025-01-01
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series BMC Plant Biology
spelling doaj-art-a56d440d07c04df2a577a62a77c74ea72025-02-02T12:15:25ZengBMCBMC Plant Biology1471-22292025-01-0125111810.1186/s12870-024-06014-3Comprehensive transcriptomic analysis reveals turnip mosaic virus infection and its aphid vector Myzus persicae cause large changes in gene regulatory networks and co-transcription of alternative spliced mRNAs in Arabidopsis thalianaVenura Herath0Clare L. Casteel1Jeanmarie Verchot2Department of Agricultural Biology, Faculty of Agriculture, University of PeradeniyaDepartment of Plant Pathology and Plant-Microbe Biology, Cornell UniversityDepartment of Plant Pathology & Microbiology, Texas A&M UniversityAbstract Background Virus infection and herbivory can alter the expression of stress-responsive genes in plants. This study employed high-throughput transcriptomic and alternative splicing analysis to understand the separate and combined impacts on host gene expression in Arabidopsis thaliana by Myzus persicae (green peach aphid), and turnip mosaic virus (TuMV). Results By investigating changes in transcript abundance, the data shows that aphids feeding on virus infected plants intensify the number of differentially expressed stress responsive genes compared to challenge by individual stressors. This study presents evidence that the combination of virus-vector-host interactions induces significant changes in hormone and secondary metabolite biosynthesis, as well as downstream factors involved in feedback loops within hormone signaling pathways. This study also shows that gene expressions are regulated through alternative pre-mRNA splicing and the use of alternative transcription start and termination sites. Conclusions These combined data suggest that complex genetic changes occur as plants adapt to the combined challenges posed by aphids and the viruses they vector. This study also provides more advanced analyses that could be used in the future to dissect the genetic mechanisms mediating tripartite interactions and inform future breeding programs.https://doi.org/10.1186/s12870-024-06014-3PotyvirusAphidsHormone signalingTranscriptomics
spellingShingle Venura Herath
Clare L. Casteel
Jeanmarie Verchot
Comprehensive transcriptomic analysis reveals turnip mosaic virus infection and its aphid vector Myzus persicae cause large changes in gene regulatory networks and co-transcription of alternative spliced mRNAs in Arabidopsis thaliana
BMC Plant Biology
Potyvirus
Aphids
Hormone signaling
Transcriptomics
title Comprehensive transcriptomic analysis reveals turnip mosaic virus infection and its aphid vector Myzus persicae cause large changes in gene regulatory networks and co-transcription of alternative spliced mRNAs in Arabidopsis thaliana
title_full Comprehensive transcriptomic analysis reveals turnip mosaic virus infection and its aphid vector Myzus persicae cause large changes in gene regulatory networks and co-transcription of alternative spliced mRNAs in Arabidopsis thaliana
title_fullStr Comprehensive transcriptomic analysis reveals turnip mosaic virus infection and its aphid vector Myzus persicae cause large changes in gene regulatory networks and co-transcription of alternative spliced mRNAs in Arabidopsis thaliana
title_full_unstemmed Comprehensive transcriptomic analysis reveals turnip mosaic virus infection and its aphid vector Myzus persicae cause large changes in gene regulatory networks and co-transcription of alternative spliced mRNAs in Arabidopsis thaliana
title_short Comprehensive transcriptomic analysis reveals turnip mosaic virus infection and its aphid vector Myzus persicae cause large changes in gene regulatory networks and co-transcription of alternative spliced mRNAs in Arabidopsis thaliana
title_sort comprehensive transcriptomic analysis reveals turnip mosaic virus infection and its aphid vector myzus persicae cause large changes in gene regulatory networks and co transcription of alternative spliced mrnas in arabidopsis thaliana
topic Potyvirus
Aphids
Hormone signaling
Transcriptomics
url https://doi.org/10.1186/s12870-024-06014-3
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AT clarelcasteel comprehensivetranscriptomicanalysisrevealsturnipmosaicvirusinfectionanditsaphidvectormyzuspersicaecauselargechangesingeneregulatorynetworksandcotranscriptionofalternativesplicedmrnasinarabidopsisthaliana
AT jeanmarieverchot comprehensivetranscriptomicanalysisrevealsturnipmosaicvirusinfectionanditsaphidvectormyzuspersicaecauselargechangesingeneregulatorynetworksandcotranscriptionofalternativesplicedmrnasinarabidopsisthaliana