Plant virus movement proteins originated from jelly-roll capsid proteins.

Numerous, diverse plant viruses encode movement proteins (MPs) that aid the virus movement through plasmodesmata, the plant intercellular channels. MPs are essential for virus spread and propagation in distal tissues, and several unrelated MPs have been identified. The 30K superfamily of MPs (named...

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Main Authors: Anamarija Butkovic, Valerian V Dolja, Eugene V Koonin, Mart Krupovic
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-06-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3002157
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author Anamarija Butkovic
Valerian V Dolja
Eugene V Koonin
Mart Krupovic
author_facet Anamarija Butkovic
Valerian V Dolja
Eugene V Koonin
Mart Krupovic
author_sort Anamarija Butkovic
collection DOAJ
description Numerous, diverse plant viruses encode movement proteins (MPs) that aid the virus movement through plasmodesmata, the plant intercellular channels. MPs are essential for virus spread and propagation in distal tissues, and several unrelated MPs have been identified. The 30K superfamily of MPs (named after the molecular mass of tobacco mosaic virus MP, the classical model of plant virology) is the largest and most diverse MP variety, represented in 16 virus families, but its evolutionary origin remained obscure. Here, we show that the core structural domain of the 30K MPs is homologous to the jelly-roll domain of the capsid proteins (CPs) of small RNA and DNA viruses, in particular, those infecting plants. The closest similarity was observed between the 30K MPs and the CPs of the viruses in the families Bromoviridae and Geminiviridae. We hypothesize that the MPs evolved via duplication or horizontal acquisition of the CP gene in a virus that infected an ancestor of vascular plants, followed by neofunctionalization of one of the paralogous CPs, potentially through the acquisition of unique N- and C-terminal regions. During the subsequent coevolution of viruses with diversifying vascular plants, the 30K MP genes underwent explosive horizontal spread among emergent RNA and DNA viruses, likely permitting viruses of insects and fungi that coinfected plants to expand their host ranges, molding the contemporary plant virome.
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spelling doaj.art-71715731f5974abba99d3b08f20f131d2023-07-04T05:31:06ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852023-06-01216e300215710.1371/journal.pbio.3002157Plant virus movement proteins originated from jelly-roll capsid proteins.Anamarija ButkovicValerian V DoljaEugene V KooninMart KrupovicNumerous, diverse plant viruses encode movement proteins (MPs) that aid the virus movement through plasmodesmata, the plant intercellular channels. MPs are essential for virus spread and propagation in distal tissues, and several unrelated MPs have been identified. The 30K superfamily of MPs (named after the molecular mass of tobacco mosaic virus MP, the classical model of plant virology) is the largest and most diverse MP variety, represented in 16 virus families, but its evolutionary origin remained obscure. Here, we show that the core structural domain of the 30K MPs is homologous to the jelly-roll domain of the capsid proteins (CPs) of small RNA and DNA viruses, in particular, those infecting plants. The closest similarity was observed between the 30K MPs and the CPs of the viruses in the families Bromoviridae and Geminiviridae. We hypothesize that the MPs evolved via duplication or horizontal acquisition of the CP gene in a virus that infected an ancestor of vascular plants, followed by neofunctionalization of one of the paralogous CPs, potentially through the acquisition of unique N- and C-terminal regions. During the subsequent coevolution of viruses with diversifying vascular plants, the 30K MP genes underwent explosive horizontal spread among emergent RNA and DNA viruses, likely permitting viruses of insects and fungi that coinfected plants to expand their host ranges, molding the contemporary plant virome.https://doi.org/10.1371/journal.pbio.3002157
spellingShingle Anamarija Butkovic
Valerian V Dolja
Eugene V Koonin
Mart Krupovic
Plant virus movement proteins originated from jelly-roll capsid proteins.
PLoS Biology
title Plant virus movement proteins originated from jelly-roll capsid proteins.
title_full Plant virus movement proteins originated from jelly-roll capsid proteins.
title_fullStr Plant virus movement proteins originated from jelly-roll capsid proteins.
title_full_unstemmed Plant virus movement proteins originated from jelly-roll capsid proteins.
title_short Plant virus movement proteins originated from jelly-roll capsid proteins.
title_sort plant virus movement proteins originated from jelly roll capsid proteins
url https://doi.org/10.1371/journal.pbio.3002157
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