The Potyviruses: An Evolutionary Synthesis Is Emerging

Abstract

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.

Doubling of the known set of RNA viruses by metagenomic analysis of an aquatic virome

“…Although these and previously recognized dicistroviruses share the same genome organization, they form sister groups in the RdRP phylogeny (for example, OV.9 and OV. 13 47,48 . Because the marine virome appears to be ancestral to the terrestrial plant virome 49 , these aquatic relatives of the potyviruses probably resemble the common ancestor, and were accordingly dubbed Protopotyviruses (Fig.…”

“…The fourth clade (101 members) of the Yangshan virome RdRPs within Pisuviricota (including OV.16 and OV.23; Supplementary Datasets 1 and 2 ) is a sister group to Potyviridae , the largest family of plant viruses 47 , 48 . Because the marine virome appears to be ancestral to the terrestrial plant virome 49 , these aquatic relatives of the potyviruses probably resemble the common ancestor, and were accordingly dubbed Protopotyviruses (Fig.…”

Aphid Transmission of Potyvirus: The Largest Plant-Infecting RNA Virus Genus

“…The generic features include (i) the precise delivery of virus particles (virions) through a needle-like stylet into a host cell, (ii) parthenogenetic mode of reproduction efficiently producing abundant progeny within a short span of time, (iii) diverse modes of feeding allowing access to host plants across several families and (iv) unique adaptations such as overwintering egg stage facilitating survival in adverse conditions and wing formation allowing aphids and viruses to disseminate over long distances [ 2 , 3 ]. The specific features of aphids that enable the transmission of certain plant viruses over the others are a result of co-evolution of aphids and viruses over thousands of years [ 4 , 5 ]. For instance, aphid-transmitted non-persistent viruses have unique binding sites and strategies, transmission mechanisms, and context specific effects on aphid biology, virus epidemics depending on specific virus and aphid species involved [ 2 ].…”

The cis‐expression of the coat protein of turnip mosaic virus is essential for viral intercellular movement in plants

“…Potyviruses represent the largest group of known plant RNA viruses, including many agriculturally important viruses such as Turnip mosaic virus (TuMV), Plum pox virus (PPV), Soybean mosaic virus (SMV), and Potato virus Y (PVY) (Revers and García, 2015;Wylie et al, 2017;Cui and Wang, 2019;Gibbs et al, 2020). Potyviruses have a positive-sense, single-stranded RNA genome of approximately 10,000 nucleotides that encodes a long open reading frame (ORF) and additional small ORFs resulting from RNA polymerase slippage during viral genome replication (Olspert et al, 2015;Revers and García, 2015;Rodamilans et al, 2015;Hagiwara-Komoda et al, 2016;Cui and Wang, 2019).…”