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Comparative Plant Transcriptome Profiling of Arabidopsis thaliana Col-0 and Camelina sativa var. Celine Infested with Myzus persicae Aphids Acquiring Circulative and Noncirculative Viruses Reveals Virus- and Plant-Specific Alterations Relevant to Aphid Feeding Behavior and Transmission

Authors :
Quentin Chesnais
Victor Golyaev
Amandine Velt
Camille Rustenholz
Véronique Brault
Mikhail M. Pooggin
Martin Drucker
Santé de la vigne et qualité du vin (SVQV)
Université de Strasbourg (UNISTRA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
Plant Health Institute of Montpellier (UMR PHIM)
Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut de Recherche pour le Développement (IRD)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut Agro Montpellier
Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Université de Montpellier (UM)
Region Grand Est (Soutien aux jeunes chercheurs, reference 18_GE5_013)
ANR-18-CE20-0017,Rome,Plusieurs stratégies, un objectif. Comment les virus manipulent hôtes et vecteurs pour la transmission : Rome(2018)
Source :
Microbiology Spectrum, Microbiology Spectrum, In press, ⟨10.1128/spectrum.00136-22⟩
Publication Year :
2022
Publisher :
HAL CCSD, 2022.

Abstract

International audience; Evidence is accumulating that plant viruses alter host plant traits in ways that modify their insect vectors' behavior. These alterations often enhance virus transmission, which has led to the hypothesis that these effects are manipulations caused by viral adaptation. However, we lack a mechanistic understanding of the genetic basis of these indirect, plant-mediated effects on vectors, their dependence on the plant host, and their relation to the mode of virus transmission. Transcriptome profiling of Arabidopsis thaliana and Camelina sativa plants infected with turnip yellows virus (TuYV) or cauliflower mosaic virus (CaMV) and infested with the common aphid vector Myzus persicae revealed strong virus-and host-specific differences in gene expression patterns. CaMV infection caused more severe effects on the phenotype of both plant hosts than did TuYV infection, and the severity of symptoms correlated strongly with the proportion of differentially expressed genes, especially photosynthesis genes. Accordingly, CaMV infection modified aphid behavior and fecundity more strongly than did infection with TuYV. Overall, infection with CaMV, relying on the noncirculative transmission mode, tends to have effects on metabolic pathways, with strong potential implications for insect vector-plant host interactions (e.g., photosynthesis, jasmonic acid, ethylene, and glucosinolate biosynthetic processes), while TuYV, using the circulative transmission mode, alters these pathways only weakly. These virus-induced deregulations of genes that are related to plant physiology and defense responses might impact both aphid probing and feeding behavior on infected host plants, with potentially distinct effects on virus transmission. IMPORTANCE Plant viruses change the phenotype of their plant hosts. Some of the changes impact interactions of the plant with insects that feed on the plants and transmit these viruses. These modifications may result in better virus transmission. We examine here the transcriptomes of two plant species infected with two viruses with different transmission modes to work out whether there are plant species-specific and transmission mode-specific transcriptome changes. Our results show that both are the case. KEYWORDS caulimovirus, polerovirus, aphid vector, transmission, feeding behavior, insect-plant interactions, transcriptome profiling, RNA-seq, plant viruses M ost known plant viruses rely on vectors for transmission to a new host (for an example, see reference 1). Insects that feed on plant phloem sap, such as whiteflies and aphids, are important vectors transmitting at least 500 virus species (2). The high virus

Details

Language :
English
ISSN :
21650497
Database :
OpenAIRE
Journal :
Microbiology Spectrum, Microbiology Spectrum, In press, ⟨10.1128/spectrum.00136-22⟩
Accession number :
edsair.doi.dedup.....ba2ee752c10591f5d6e8f47d2df79162
Full Text :
https://doi.org/10.1128/spectrum.00136-22⟩