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A binary interaction map between turnip mosaic virus and Arabidopsis thaliana proteomes.

ABSTRACT: Viruses are obligate intracellular parasites that have co-evolved with their hosts to establish an intricate network of protein-protein interactions. Here, we followed a high-throughput yeast two-hybrid screening to identify 378 novel protein-protein interactions between turnip mosaic virus (TuMV) and its natural host Arabidopsis thaliana. We identified the RNA-dependent RNA polymerase NIb as the viral protein with the largest number of contacts, including key salicylic acid-dependent transcription regulators. We verified a subset of 25 interactions in planta by bimolecular fluorescence complementation assays. We then constructed and analyzed a network comprising 399 TuMV-A. thaliana interactions together with intravirus and intrahost connections. In particular, we found that the host proteins targeted by TuMV are enriched in different aspects of plant responses to infections, are more connected and have an increased capacity to spread information throughout the cell proteome, display higher expression levels, and have been subject to stronger purifying selection than expected by chance. The proviral or antiviral role of ten host proteins was validated by characterizing the infection dynamics in the corresponding mutant plants, supporting a proviral role for the transcriptional regulator TGA1. Comparison with similar studies with animal viruses, highlights shared fundamental features in their mode of action.

SUBMITTER: Martinez F

PROVIDER: S-EPMC9834402 | biostudies-literature | 2023 Jan

REPOSITORIES: biostudies-literature

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A binary interaction map between turnip mosaic virus and Arabidopsis thaliana proteomes.

Martínez Fernando F Carrasco José L JL Toft Christina C Hillung Julia J Giménez-Santamarina Silvia S Yenush Lynne L Rodrigo Guillermo G Elena Santiago F SF

Communications biology 20230111 1

Viruses are obligate intracellular parasites that have co-evolved with their hosts to establish an intricate network of protein-protein interactions. Here, we followed a high-throughput yeast two-hybrid screening to identify 378 novel protein-protein interactions between turnip mosaic virus (TuMV) and its natural host Arabidopsis thaliana. We identified the RNA-dependent RNA polymerase NIb as the viral protein with the largest number of contacts, including key salicylic acid-dependent transcript ...[more]

PMID: 36631662

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Project description:Plants produce glutathione as a response to the intercellular redox state. Glutathione actively participates in the reactive oxygen species (ROS)-dependent signaling pathway, especially under biotic stress conditions. Most of the glutathione S-transferases (GSTs) are induced in cells during the defense response of plants not only through highly specific glutathione-binding abilities but also by participating in the signaling function. The tau class of GSTs has been reported to be induced as a response under stress conditions. Although several studies have focused on the role of the tau class of GSTs in plant-pathogen interactions, knowledge about their contribution to the response to virus inoculation is still inadequate. Therefore, in this study, the response of Atgstu19 and Atgstu24 knockout mutants to mechanical inoculation of Turnip mosaic virus (TuMV) was examined. The systemic infection of TuMV was more dynamically promoted in Atgstu19 mutants than in wild-type (Col-0) plants, suggesting the role of GSTU19 in TuMV resistance. However, Atgstu24 mutants displayed virus limitation and downregulation of the relative expression of TuMV capsid protein, accompanied rarely by TuMV particles only in vacuoles, and ultrastructural analyses of inoculated leaves revealed the lack of virus cytoplasmic inclusions. These findings indicated that Atgstu24 mutants displayed a resistance-like reaction to TuMV, suggesting that GSTU24 may suppress the plant resistance. In addition, these findings confirmed that GSTU1 and GSTU24 are induced and contribute to the susceptible reaction to TuMV in the Atgstu19-TuMV interaction. However, the upregulation of GSTU19 and GSTU13 highly correlated with virus limitation in the resistance-like reaction in the Atgstu24-TuMV interaction. Furthermore, the highly dynamic upregulation of GST and glutathione reductase (GR) activities resulted in significant induction (between 1 and 14 days post inoculation [dpi]) of the total glutathione pool (GSH + GSSG) in response to TuMV, which was accompanied by the distribution of active glutathione in plant cells. On the contrary, in Atgstu19, which is susceptible to TuMV interaction, upregulation of GST and GR activity only up to 7 dpi symptom development was reported, which resulted in the induction of the total glutathione pool between 1 and 3 dpi. These observations indicated that GSTU19 and GSTU24 are important factors in modulating the response to TuMV in Arabidopsis thaliana. Moreover, it was clear that glutathione is an important component of the regulatory network in resistance and susceptible response of A. thaliana to TuMV. These results help achieve a better understanding of the mechanisms regulating the Arabidopsis-TuMV pathosystem.

Project description:Respiratory burst oxidase homologs (Rbohs) play crucial and diverse roles in plant tissue-mediated production of reactive oxygen species during the development, growth, and response of plants to abiotic and biotic stress. Many studies have demonstrated the contribution of RbohD and RbohF in stress signaling in pathogen response differentially modulating the immune response, but the potential role of the Rbohs-mediated response in plant-virus interactions remains unknown. The present study analyzed, for the first time, the metabolism of glutathione in rbohD-, rbohF-, and rbohD/F-transposon-knockout mutants in response to Turnip mosaic virus (TuMV) infection. rbohD-TuMV and Col-0-TuMV interactions were characterized by susceptible reaction to TuMV, associated with significant activity of GPXLs (glutathione peroxidase-like enzymes) and induction of lipid peroxidation in comparison to mock-inoculated plants, with reduced total cellular and apoplastic glutathione content observed at 7-14 dpi and dynamic induction of apoplast GSSG (oxidized glutathione) at 1-14 dpi. Systemic virus infection resulted in the induction of AtGSTU1 and AtGSTU24, which was highly correlated with significant downregulation of GSTs (glutathione transferases) and cellular and apoplastic GGT (γ-glutamyl transferase) with GR (glutathione reductase) activities. On the contrary, resistant rbohF-TuMV reactions, and especially enhanced rbohD/F-TuMV reactions, were characterized by a highly dynamic increase in total cellular and apoplastic glutathione content, with induction of relative expression of AtGGT1, AtGSTU13, and AtGSTU19 genes. Moreover, virus limitation was highly correlated with the upregulation of GSTs, as well as cellular and apoplastic GGT with GR activities. These findings clearly indicate that glutathione can act as a key signaling factor in not only susceptible rbohD reaction but also the resistance reaction presented by rbohF and rbohD/F mutants during TuMV interaction. Furthermore, by actively reducing the pool of glutathione in the apoplast, GGT and GR enzymes acted as a cell first line in the Arabidopsis-TuMV pathosystem response, protecting the cell from oxidative stress in resistant interactions. These dynamically changed signal transductions involved symplast and apoplast in mediated response to TuMV.

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A binary interaction map between turnip mosaic virus and Arabidopsis thaliana proteomes.

Publications

A binary interaction map between turnip mosaic virus and Arabidopsis thaliana proteomes.

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