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  • Review Article
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Symbiosis versus competition in plant virus evolution

Nature Reviews Microbiology volume 3, pages 917–924 (2005)Cite this article

Key Points

  • Darwinian natural selection is a gradual process of change produced by random mutations followed by competitive selection. However, extant species indicate that some evolutionary changes have been more rapid than could occur by Darwinian evolution, and the theory of symbiogenesis, or evolution by the merging of dissimilar symbiotic entities, has gained support in recent years.

  • Plant RNA viruses were shown to compete in early studies on cross-protection, in which mild strains of a virus could protect plants from subsequent infection by more virulent strains. The requirement of this type of competition is that the strains are similar. Symbiosis involves a different paradigm from competition.

  • In mixed infections of plant viruses, there is a potential for symbiotic associations. The definition of symbiosis requires that the entities are dissimilar. Some well described examples of plant viruses that are symbiotic include potyviruses, which are often synergistic with other viruses; luteoviruses, which often require other viruses for dissemination; and satellites, which establish parasitic symbiosis with their helper viruses.

  • The effect of symbiosis on plant virus evolution can be seen in the modular nature of plant virus genes, which show evidence of recombination and reassortment in their evolutionary history when phylogenetic trees for different genes or genome components are analysed.

  • Symbiogenesis is probably a major component of plant virus evolution, allowing evolutionary leaps that could accommodate changing environments and host ranges. However, the gradual process of natural selection undoubtedly fine-tunes the resulting new species through random mutation and selection.

Abstract

Darwin's theory of evolution by natural selection has been supported by molecular evidence and by experimental evolution of viruses. However, it might not account for the evolution of all life, and an alternative model of evolution through symbiotic relationships also has gained support. In this review, the evolution of plant viruses has been reinterpreted in light of these two seemingly opposing theories by using evidence from the earliest days of plant virology to the present. Both models of evolution probably apply in different circumstances, but evolution by symbiotic association (symbiogenesis) is the most likely model for many evolutionary events that have resulted in rapid changes or the formation of new species. In viruses, symbiogenesis results in genomic reassortment or recombination events among disparate species. These are most noticeable by phylogenetic comparisons of extant viruses from different taxonomic groups.

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Figure 1: Life cycle and reassortment of a segmented positive-sense RNA plant virus.
Figure 2: A proposed model for the emergence of a new taxonomic group of viruses following a symbiotic relationship.
Figure 3: Comparison of hypothetical phylogenetic trees for different proteins of viruses undergoing modular evolution.
Figure 4: Cladograms of the phylogenetic relationships among species in the genus Cucumovirus.

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Acknowledgements

The author wishes to thank E. Blancaflor, D. Brooks, A. Elmer, L. Marquez, G. May, J. Pita, M. Taylor and P. Xu for thoughtful discussions and editorial comments, B. Falk for unpublished data and L. Villarreal and F. Ryan for inspiration for this line of thinking. The author is also grateful to the S.R. Noble Foundation for financial support.

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Authors and Affiliations

  1. Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, 73401, Oklahoma, USA

    Marilyn J. Roossinck

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DATABASES

Entrez

bean distortion mosaic virus

cucumber mosaic virus

maize chlorotic mottle virus

pea early browning virus

pea enation mosaic virus

peanut stunt virus

pepper mottle virus

pepper veinal mottle virus

potato virus X

potato virus Y

rice tungro bacilliform virus

rice tungro spherical virus

southern bean mosaic virus

southern cowpea mosaic virus

sugarcane yellow leaf virus

sunn-hemp mosaic virus

tobacco mild green mosaic virus

tobacco mosaic virus

tobacco rattle virus

tomato aspermy virus

vaccinia virus

wheat streak mosaic virus

FURTHER INFORMATION

Marilyn J. Roossinck's homepage

Glossary

SALTATION

A rapid evolutionary event that changes a species into another species.

SYMBIOGENESIS

The fusion of symbiotic organisms to form a new species. According to Ryan's definition, this can result from endosymbiosis, which involves genes and/or genomes, and exosymbiosis, in which the interaction involves behaviour or shared metabolites.

POSITIVE-SENSE RNA VIRUS

A virus with a single-stranded RNA genome that can serve as a messenger RNA without further transcription.

ISOGENIC

Genetically identical; derived from the same inbred line.

SUPERINFECTION

Infection of a cell by a virus when it is already infected by another virus.

SATELLITE RNA

A parasitic RNA associated with some plant RNA viruses. Satellite RNAs are completely dependent on their helper virus for replication and dissemination, but do not provide any essential function to the helper virus.

PARARETROVIRUS

A virus that packages an RNA pre-genome that is converted to DNA in the virion. Retroviruses and pararetroviruses behave like RNA viruses in their evolutionary capacity because their replication machinery is highly error prone.

CO-EVOLUTION

The evolution of two symbiotic species in which each change by one partner is compensated by a change in the other partner.

CONGRUENT TREES

A set of phylogenetic trees using different genes that show the same patterns of evolution for each gene. Incongruent trees show markedly different topologies when different genes from the same set of taxa are analysed.

CLADISTIC TREE

A tree depicting the phylogenetic relationships of a group of organisms. In a cladogram, only the branching order is significant, the branch lengths are not significant.

SPECIATION

The formation of a new species. By classic definition, a new species is sexually incompatible with its parental species, although the definition for viruses, and many other organisms such as plants, is less clear.

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Roossinck, M. Symbiosis versus competition in plant virus evolution. Nat Rev Microbiol 3, 917–924 (2005). https://doi.org/10.1038/nrmicro1285

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