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.

Keywords: evolution; metagenomes; phylogenetics; population genetics; potyvirids; potyviruses; recombination; speciation.

Figure 1

The phylogeny of the RdRps of selected potyvirids, and of the other most closely related viral RdRps (redrawn from [24]).

Figure 2

A maximum likelihood (ML) phylogeny of 166 potyvirids, calculated using the same methods as [29,30,31], from the protein sequences encoded by the RdRp regions of all genomes with GenBank Reference Sequence Accession Codes (July 2019), together with any others that had unique names. The most closely related non-potyvirid, bufivirus UC1, is included as an outlier. Branch colors indicate the major angiosperm “Order” from which each virus was isolated (i.e., its “primary host”); eudicotyledon rosid (red), asterid (blue), or caryophyllid (yellow) and monocotyledon (green) alismatid “A”, lilioid “L”, or commelinid “C”. The RdRps of potyviruses branching most closely to the rymoviruses are shown, and the phylogeny of the other 103 is collapsed. The nodes with a red disk have >0.9 SH support.

Figure 3

An ML phylogeny of 149 potyvirus ORF sequences with three rymovirus ORFs as outgroup using the same methods as [29,30,31]. The ORFs are from all 126 potyviruses represented in GenBank in mid-2019 by Reference Sequences, together with single representative sequences of all 23 other potyviruses in GenBank with unique names. Note that (a) shows the three rymoviruses and Lineages 1–4, whereas (b) shows Lineages 5–9. The “Order” of the primary host, namely the plant from which each was first isolated, and often given in the name of the virus, is shown by the branch color (and letter), eudicotyledonous rosid (red), asterid (blue), or caryophyllid (yellow) and monocotyledonous alismatid “A”, lilioid “L”, or commelinid “C”.

Figure 3

An ML phylogeny of 149 potyvirus ORF sequences with three rymovirus ORFs as outgroup using the same methods as [29,30,31]. The ORFs are from all 126 potyviruses represented in GenBank in mid-2019 by Reference Sequences, together with single representative sequences of all 23 other potyviruses in GenBank with unique names. Note that (a) shows the three rymoviruses and Lineages 1–4, whereas (b) shows Lineages 5–9. The “Order” of the primary host, namely the plant from which each was first isolated, and often given in the name of the virus, is shown by the branch color (and letter), eudicotyledonous rosid (red), asterid (blue), or caryophyllid (yellow) and monocotyledonous alismatid “A”, lilioid “L”, or commelinid “C”.

Figure 4

A graph comparing the patristic distances of the ML tree of ORFs in Figure 3a,b and the ML tree of the protein sequences encoded by these ORFs; 149 potyviruses and three rymoviruses are included.

Figure 5

The ML phylogenetic tree (collapsed) of the non-recombinant (n-rec) ORFs of five potyvirus populations. The number of ORF sequences for each virus (N), their average pairwise nt diversity (π) and, for each, the ratio of nonsynonymous nt diversity to synonymous nt diversity ω (dN/dS); also the slope (b) of the linear regression in a graph comparing the pairwise patristic distances in ML trees of the ORF sequences (y axis) and encoded polyproteins (x axis), and the maximum patristic distance (max ORF-dist) in the patristic distance graph.

Figure 6

The ML phylogenetic trees (collapsed) of the phylogroups/groups/strains of the non-recombinant (n-rec) ORFs of five potyviruses. The number of ORF sequences for each grouping (N), their average pairwise nt diversity (π), and, for each, the ratio of nonsynonymous nt diversity to synonymous nt diversity ω (dN/dS), and the statistical significance of Tajima’s D coefficient for the group.

Figure 7

A stacked column chart of the ω (dN/dS) values of the genes of populations of different potyvirus phylogroups/groups/strains. The N-terminal protein (P1) is at the base of each column.