Plant virus movement proteins originated from jelly-roll capsid proteins

• Published in: PLoS biology Vol. 21; no. 6; p. e3002157
• Main Authors: Butkovic, Anamarija, Dolja, Valerian V., Koonin, Eugene V., Krupovic, Mart
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 15.06.2023; Public Library of Science (PLoS)
• Subjects: Biology and life sciences; Capsid Proteins - genetics; Coevolution; CP gene; Deoxyribonucleic acid; DNA; DNA viruses; Evolution; Flowers & plants; Genes; Genomes; Identification and classification; Insects; Life Sciences; Medicine and Health Sciences; Microbiology and Parasitology; Natural history; Nicotiana - genetics; Origin; Phylogenetics; Physiological aspects; Plant Viral Movement Proteins - chemistry; Plant Viral Movement Proteins - genetics; Plant Viral Movement Proteins - metabolism; Plant viruses; Plant Viruses - genetics; Plant Viruses - metabolism; Plants; Plants - genetics; Plasmodesmata; Propagation; Proteins; Ribonucleic acid; RNA; RNA viruses; Tobacco; Tobacco Mosaic Virus - genetics; Tobacco Mosaic Virus - metabolism; Viral proteins; Virology; Virus diseases of plants; Viruses; France
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.3002157

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.