Tobamoviruses have probably co-diverged with their eudicotyledonous hosts for at least 110 million years

Abstract

A phylogeny has been calculated by maximum likelihood comparisons of the concatenated consensus protein sequences of 29 tobamoviruses shown to be non-recombinant. This phylogeny has statistically significant support throughout, including its basal branches. The viruses form eight lineages that are congruent with the taxonomy of the hosts from which each was first isolated and, with the exception of three of the twenty-nine species, all fall into three clusters that have either asterid or rosid or caryophyllid hosts (i.e. the major subdivisions of eudicotyledonous plants). A modified Mantel permutation test showed that the patristic distances of virus and host phylogenies are significantly correlated, especially when the three anomalously placed viruses are removed. When the internal branches of the virus phylogeny were collapsed the congruence decreased. The simplest explanation of this congruence of the virus and host phylogenies is that most tobamovirus lineages have co-diverged with their primary plant hosts for more than 110 million years, and only the brassica-infecting lineage originated from a major host switch from asterids to rosids. Their co-divergence seems to have been 'fuzzy' rather than 'strict', permitting viruses to switch hosts within major host clades. Our conclusions support those of a coalesence analysis of tobamovirus sequences, that used proxy node dating, but not a similar analysis of nucleotide sequences from dated samples, which concluded that the tobamoviruses originated only 100 thousand years ago.

Keywords: co-divergence; phylogenetic congruence; plant evolution; tobamovirus evolution.

Figure 1.

The phylogeny of the primary eudicotyledonous hosts of non-recombinant tobamoviruses. The name of each plant order is given with (in parentheses) the plant taxon which is minimally inclusive of the known primary host species. Asterid orders have red branches, rosid blue, and caryophyllid green. Redrawn from Fig. 1 of Magallón and Castillo (2009).

Figure 2.

Graph showing the statistical support for ML trees calculated from the aligned twenty-nine concat amino acid sequences obtained using different levels of consensus from 177 tobamovirus genomes.

Figure 3.

ML phylogeny of twenty-nine tobamoviruses calculated from 100 percent consensus concatenated amino acid sequences of their three main proteins; replicase, MP and CPs. The tree was calculated by PhyML (Guindon and Gascuel 2003) with the LG model (Le and Gascuel 2008). Branches are arranged radially, and are coloured blue, red, or black to show those linked only to rosid, or asterid, or mixed hosts, respectively. The SH-support measure for individual branches is shown, and the branches that have statistically significant support through the base of the tree are bold. The ‘ORSV-REP’ is where the consensus replicase gene of ORSV diverged, and ‘ORSV-MP/CP’ is where its consensus MP/CP concat diverged (see text). Acronyms for the viruses are: BmMtV, Brugmansia mild mottle virus; BPMtV, bell pepper mottle virus; CFMtMV, cucumber fruit mottle mosaic virus; CGMtMV, cucumber green mottle mosaic virus; CmMtV, cactus mild mottle virus; CMtV, cucumber mottle virus; CYMtV, Clitoria yellow mottle virus; FMV, frangipani mosaic virus; HLFtPV, Hibiscus latent Fort Pierce virus; HLSV, Hibiscus latent Singapore virus; KGMtMV, kyuri green mottle mosaic virus; MMV, maracuja mosaic virus; OPV, Obuda pepper virus; PapmMtV, paprika mild mottle virus; PFMV, passion fruit mosaic virus; PmMtV, pepper mild mottle virus; RCNaV, rattail cactus necrosis associated virus; RehMV, Rehmannia mosaic virus; RMV, ribgrass mosaic virus; SHMV, sunn-hemp mosaic virus, StFBV, Streptocarpus flower break virus; TmGMV, tobacco mild green mosaic virus; TMV, tobacco mosaic virus; ToMtV, tomato mottle virus; ToMV, tomato mosaic virus; TVCV, turnip vein-clearing virus; YMV, youcai mosaic virus; YTmMtV, yellow tailflower mild mottle virus; ZGMtMV, zucchini green mottle mosaic virus.

Figure 4.

The phylogeny of twenty-nine tobamovirus shown in Fig. 2 with a grey broken circle indicating the basal regions of the tree where part or all of every branch was shortened first to give a branch length corresponding to 0.0001 s/s. The grey disks indicate the positions to which all the basal branches were shortened for a more stringent test of congruence. For an explanation see text.

Figure 5.

Patristic distance diagrams comparing NJ trees calculated from the S codons and NS codons of sixty-seven TMV concat genomic sequences with NJ trees of the amino acid sequences that the complete sequences encoded.