Tobamovirus infection aggravates gray mold disease caused by Botrytis cinerea by manipulating the salicylic acid pathway in tomato

Botrytis cinerea is the causative agent of gray mold disease, and infects more than 1400 plant species, including important crop plants. In tomato, B. cinerea causes severe damage in greenhouses and post-harvest storage and transport. Plant viruses of the Tobamovirus genus cause significant damage t...

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Main Authors: Rupali Gupta, Meirav Leibman-Markus, Daniela Weiss, Ziv Spiegelman, Maya Bar
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-06-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1196456/full
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author Rupali Gupta
Meirav Leibman-Markus
Daniela Weiss
Ziv Spiegelman
Maya Bar
author_facet Rupali Gupta
Meirav Leibman-Markus
Daniela Weiss
Ziv Spiegelman
Maya Bar
author_sort Rupali Gupta
collection DOAJ
description Botrytis cinerea is the causative agent of gray mold disease, and infects more than 1400 plant species, including important crop plants. In tomato, B. cinerea causes severe damage in greenhouses and post-harvest storage and transport. Plant viruses of the Tobamovirus genus cause significant damage to various crop species. In recent years, the tobamovirus tomato brown rugose fruit virus (ToBRFV) has significantly affected the global tomato industry. Most studies of plant-microbe interactions focus on the interaction between the plant host and a single pathogen, however, in agricultural or natural environments, plants are routinely exposed to multiple pathogens. Here, we examined how preceding tobamovirus infection affects the response of tomato to subsequent infection by B. cinerea. We found that infection with the tobamoviruses tomato mosaic virus (ToMV) or ToBRFV resulted in increased susceptibility to B. cinerea. Analysis of the immune response of tobamovirus-infected plants revealed hyper-accumulation of endogenous salicylic acid (SA), upregulation of SA-responsive transcripts, and activation of SA-mediated immunity. Deficiency in SA biosynthesis decreased tobamovirus-mediated susceptibility to B. cinerea, while exogenous application of SA enhanced B. cinerea symptoms. These results suggest that tobamovirus-mediated accumulation of SA increases the plants’ susceptibility to B. cinerea, and provide evidence for a new risk caused by tobamovirus infection in agriculture.
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spelling doaj.art-c248063e3d014d7f873bee52b44f03282023-06-12T04:35:00ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-06-011410.3389/fpls.2023.11964561196456Tobamovirus infection aggravates gray mold disease caused by Botrytis cinerea by manipulating the salicylic acid pathway in tomatoRupali GuptaMeirav Leibman-MarkusDaniela WeissZiv SpiegelmanMaya BarBotrytis cinerea is the causative agent of gray mold disease, and infects more than 1400 plant species, including important crop plants. In tomato, B. cinerea causes severe damage in greenhouses and post-harvest storage and transport. Plant viruses of the Tobamovirus genus cause significant damage to various crop species. In recent years, the tobamovirus tomato brown rugose fruit virus (ToBRFV) has significantly affected the global tomato industry. Most studies of plant-microbe interactions focus on the interaction between the plant host and a single pathogen, however, in agricultural or natural environments, plants are routinely exposed to multiple pathogens. Here, we examined how preceding tobamovirus infection affects the response of tomato to subsequent infection by B. cinerea. We found that infection with the tobamoviruses tomato mosaic virus (ToMV) or ToBRFV resulted in increased susceptibility to B. cinerea. Analysis of the immune response of tobamovirus-infected plants revealed hyper-accumulation of endogenous salicylic acid (SA), upregulation of SA-responsive transcripts, and activation of SA-mediated immunity. Deficiency in SA biosynthesis decreased tobamovirus-mediated susceptibility to B. cinerea, while exogenous application of SA enhanced B. cinerea symptoms. These results suggest that tobamovirus-mediated accumulation of SA increases the plants’ susceptibility to B. cinerea, and provide evidence for a new risk caused by tobamovirus infection in agriculture.https://www.frontiersin.org/articles/10.3389/fpls.2023.1196456/fullBotrytis cinereatobamovirusToMVToBRFVsalicylic acidimmunity
spellingShingle Rupali Gupta
Meirav Leibman-Markus
Daniela Weiss
Ziv Spiegelman
Maya Bar
Tobamovirus infection aggravates gray mold disease caused by Botrytis cinerea by manipulating the salicylic acid pathway in tomato
Frontiers in Plant Science
Botrytis cinerea
tobamovirus
ToMV
ToBRFV
salicylic acid
immunity
title Tobamovirus infection aggravates gray mold disease caused by Botrytis cinerea by manipulating the salicylic acid pathway in tomato
title_full Tobamovirus infection aggravates gray mold disease caused by Botrytis cinerea by manipulating the salicylic acid pathway in tomato
title_fullStr Tobamovirus infection aggravates gray mold disease caused by Botrytis cinerea by manipulating the salicylic acid pathway in tomato
title_full_unstemmed Tobamovirus infection aggravates gray mold disease caused by Botrytis cinerea by manipulating the salicylic acid pathway in tomato
title_short Tobamovirus infection aggravates gray mold disease caused by Botrytis cinerea by manipulating the salicylic acid pathway in tomato
title_sort tobamovirus infection aggravates gray mold disease caused by botrytis cinerea by manipulating the salicylic acid pathway in tomato
topic Botrytis cinerea
tobamovirus
ToMV
ToBRFV
salicylic acid
immunity
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1196456/full
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