The existence of numerous virus groups that include related viruses infecting animals and plants demands an evolutionary explanation. From general principles, there appear to be three major scenarios ():
- Evolution of related plant and animal viruses from a common ancestral virus that predates the divergence of plants and animals;
- Horizontal virus transfer (HVT) between plants and animals;
- Parallel evolution of related viruses from related ancestral genetic elements.
The three scenarios for the origin of related viruses in plants and animals: Common ancestry, horizontal virus transfer and parallel evolution.
The principal criteria for distinguishing between these routes of evolution include the host range of a virus group, in particular whether it contains viruses infecting unicellular eukaryotes, in addition to those infecting plants and animals; phylogenies of conserved genes – whether or not plant and animal viruses cluster together; the comparative diversity of the virus group in plants and animals; and the level of similarity between the sequences and genome organizations of members of the groups infecting plants and animals. Application of these criteria to the diverse groups of viruses suggests that all three routes have been important, their relative contributions varying between groups of viruses.
Common ancestry of plant and animal viruses is linked to the current view of the early stages in the evolution of eukaryotes. Although animals and plants are the most complex multicellular eukaryotes, there is no evidence that they are monophyletic. On the contrary, animals and plants form distinct branches within two of the five (or possibly six) supergroups of eukaryotes, and all recent attempts to root the eukaryote tree place the root between the supergroups that include, respectively, animals and plants. Thus, the common origin scenario would imply that the common ancestors of virus groups shared by animals and plants already existed at the stage of the Last Eukaryotic Common Ancestor (LECA), perhaps evolving concomitantly with eukaryogenesis.
The primary showcases for common ancestry come from the opposite poles of the virus world: some of the simplest viruses, the picornavirus-like superfamily of positive-strand RNA viruses () [11
], and the most complex viruses, the NCLDV [31
]. Indeed, among the viruses of diverse unicellular eukaryotes discovered by both traditional and metagenomic methods, the picornavirus-like viruses and the NCLDV are by far the most abundant groups among the RNA and DNA viruses, respectively [5
]. There is a many to many mapping of the major branches of the respective viruses onto the supergroups of eukaryotes: viruses of the same branch infect hosts from different supergroups, and conversely, each supergroup hosts viruses from different branches. This pattern suggests early radiation of the major branches within the picornavirus-like superfamily and within the NCLDV, with subsequent assortment of viruses from pre-existing ancestral pools to the emerging supergroups of eukaryotes () [11
]. Thus, within the picornavirus-like superfamily, four of the six major branches include both plant and animal viruses, and viruses of unicellular eukaryotes, the implication being that ancestors of these groups of viruses have already diverged at the stage of LECA. Similar conclusions have been reached in the phylogenomic study of the NCLDV that probably were represented by several ancestral viruses at the stage of LECA. At the divergence of the supergroups, the animal lineage inherited the iridoviruses and the common ancestors of poxviruses and asfarviruses, whereas green algae were infected by phycodnaviruses, later excluded from the land plant lineage.
The case for a likely transfer of viruses between plants and animals is presented by the negative strand RNA viruses such as rhabdoviruses and bunyaviruses (). There is no evidence that any negative strand RNA viruses infect unicellular eukaryotes, so origin of related plant and animal viruses from a common ancestor antedating LECA is unlikely. Evolution via HVT is compatible with the high similarity between the protein sequences and genome architectures of plant and animal viruses in these families (). Furthermore, vehicles for transfer are available: invertebrate parasites of animals and plants. Strikingly, viruses of the order Mononegavirales
and the family Bunyaviridae
that infect plants and vertebrates can also reproduce in their arthropod vectors [48
]. The discovery of negative strand RNA viruses, some of which are related to animal and others to plant viruses, in plant parasitic nematodes, the most abundant animals on earth, suggests that HVT could be even more opportune than currently appreciated [50
]. Furthermore, the direction of HVT can be inferred with considerable confidence: from animals to plants, given the much greater diversity of negative strand RNA viruses in animals and the fact that all suspected vectors are animals.
The ssDNA viruses of plants and animals present a story of apparent parallel evolution from related prokaryotic genetic elements that replicate via the RCR mechanism () [27
]. Although animal circoviruses and plant geminiviruses show similar organizations of the replication and CP modules (), sequence similarity between the respective proteins is low, and virion architectures are different, a single and a ‘siamese twins’ icosahedra, respectively [51
]. A handful of known ssDNA viruses from unicellular eukaryotes, diatoms, have distinct genome organization and share little sequence similarity with either circoviruses or geminiviruses [53
]. In contrast, a close evolutionary relationship appears to exist between replication proteins of geminiviruses and ssDNA plasmids from phythopathogenic bacteria both of which reproduce within plant phloem cells [54
]. Given that at least some geminiviruses can replicate in bacteria [55
], the origin of this plant virus family could involve horizontal transfer of the replicase gene module from a bacterial plasmid with concomitant acquisition of the CP and MP genes from pre-existing plant virus(es) [54
]. Although with less certainty, a potential circovirus ancestor was also proposed to be a bacterial ssDNA plasmid [54
]. Thus, it appears likely that geminiviruses and circoviruses evolved in parallel and via similar scenarios, namely recombination between a plasmid from a bacterial parasite and a plant or animal virus, respectively. Certainly, conclusions on the routes of virus evolution have to be taken cautiously because new discoveries of ecological genomics have the potential to change the scenarios. A case in point is the single-cell genomic study of picobiliphytes, a group of marine picoeukaryotes distantly related to green algae and plants, in which a putative virus related to plant nanoviruses has been discovered [57
]. Numerous homologs of this novel virus are detectable in marine metagenomic samples, suggesting the existence of abundant nanovirus-like agents in unicellular eukaryotes and implying an ancient origin of this family of ssDNA viruses. Similar discoveries on other virus groups by no means can be ruled out.