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Host Range Evolution of Potyviruses: A Global Phylogenetic Analysis
Open AccessReview

The Potyviruses: An Evolutionary Synthesis Is Emerging

1
Emeritus Faculty, Australian National University, Canberra, ACT 2601, Australia
2
Department of Plant Protection, Faculty of Agriculture, University of Kurdistan, P.O. Box 416, Sanandaj, Iran
3
Laboratory of Plant Virology, Department of Applied Biological Sciences, Faculty of Agriculture, Saga University, 1-banchi, Honjo-machi, Saga 840-8502, Japan
4
The United Graduate School of Agricultural Sciences, Kagoshima University, 1-21-2410 Korimoto, Kagoshima 890-0065, Japan
5
Institute of Agriculture, University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia
*
Authors to whom correspondence should be addressed.
Viruses 2020, 12(2), 132; https://doi.org/10.3390/v12020132
Received: 31 December 2019 / Revised: 16 January 2020 / Accepted: 20 January 2020 / Published: 22 January 2020
(This article belongs to the Special Issue The Complexity of the Potyviral Interaction Network)
In this review, encouraged by the dictum of Theodosius Dobzhansky that “Nothing in biology makes sense except in the light of evolution”, we outline the likely evolutionary pathways that have resulted in the observed similarities and differences of the extant molecules, biology, distribution, etc. of the potyvirids and, especially, its largest genus, the potyviruses. The potyvirids are a family of plant-infecting RNA-genome viruses. They had a single polyphyletic origin, and all share at least three of their genes (i.e., the helicase region of their CI protein, the RdRp region of their NIb protein and their coat protein) with other viruses which are otherwise unrelated. Potyvirids fall into 11 genera of which the potyviruses, the largest, include more than 150 distinct viruses found worldwide. The first potyvirus probably originated 15,000–30,000 years ago, in a Eurasian grass host, by acquiring crucial changes to its coat protein and HC-Pro protein, which enabled it to be transmitted by migrating host-seeking aphids. All potyviruses are aphid-borne and, in nature, infect discreet sets of monocotyledonous or eudicotyledonous angiosperms. All potyvirus genomes are under negative selection; the HC-Pro, CP, Nia, and NIb genes are most strongly selected, and the PIPO gene least, but there are overriding virus specific differences; for example, all turnip mosaic virus genes are more strongly conserved than those of potato virus Y. Estimates of dN/dS (ω) indicate whether potyvirus populations have been evolving as one or more subpopulations and could be used to help define species boundaries. Recombinants are common in many potyvirus populations (20%–64% in five examined), but recombination seems to be an uncommon speciation mechanism as, of 149 distinct potyviruses, only two were clear recombinants. Human activities, especially trade and farming, have fostered and spread both potyviruses and their aphid vectors throughout the world, especially over the past five centuries. The world distribution of potyviruses, especially those found on islands, indicates that potyviruses may be more frequently or effectively transmitted by seed than experimental tests suggest. Only two meta-genomic potyviruses have been recorded from animal samples, and both are probably contaminants. View Full-Text
Keywords: potyviruses; potyvirids; phylogenetics; population genetics; evolution; recombination; speciation; metagenomes potyviruses; potyvirids; phylogenetics; population genetics; evolution; recombination; speciation; metagenomes
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Gibbs, A.J.; Hajizadeh, M.; Ohshima, K.; Jones, R.A. The Potyviruses: An Evolutionary Synthesis Is Emerging. Viruses 2020, 12, 132.

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