Virus–Plant Co‐evolution


Virus infection and plant defences may, respectively, reduce the fitness of plants and viruses, which could result in virus–plant co‐evolution. It is commonly assumed that viruses and plants co‐evolve, but evidence supporting this hypothesis is scant, refers mostly to the virus partner, and almost totally derives from the study of highly virulent viruses in agricultural systems, in which host genetic structure is manipulated leading to genetic changes in the virus population. Research has focussed on processes driven by qualitative resistance, either dominant or recessive, which conform, respectively, to the gene‐for‐gene and matching‐alleles models of host–pathogen co‐evolution. A serious limitation is the limited information available for systems in which the host might also evolve in response to virus infection, that is, wild hosts in natural ecosystems, an area of research that should be encouraged.

Key Concepts:

  • Requirements for co‐evolution have not been yet shown to be fully met for any virus–plant system.

  • Infection of plants by viruses does not necessarily decrease plant fitness.

  • Virus–plant interactions determined by single, dominant resistance genes conform to the gene‐for‐gene model of host–pathogen interaction.

  • Most dominant resistance genes of plants to viruses encode NB‐LRR proteins (R proteins).

  • There is no current evidence for diversifying selection of R proteins targeting viruses.

  • The product of any virus gene can be an avirulence determinant eliciting the defence determined by resistance genes.

  • Virus–plant interactions determined by single, recessive resistance genes conform to the matching‐alleles model of host–pathogen interaction.

  • Pathogenicity on dominant resistance genes may have important fitness costs.

  • Pathogenicity on recessive resistance genes may have fitness costs depending on the virus and host genotypes.

  • Constraints to virus evolution may determine the durability of resistance factors bred into crops.

Keywords: plant viruses; resistance; susceptibility; gene‐for‐gene interactions; matching‐alleles interactions; costs of pathogenicity; durability of resistance

Figure 1.

Two loci gene‐for‐gene model of host–pathogen co‐evolution for a diploid host and a haploid pathogen species. The product of the dominant resistance allele at either of two loci A and B, RA and RB, in the host allows recognition of the product of avirulence genes, AVRA and AVRB, respectively, in the pathogen, triggering defences and limiting infection, that is the interaction is incompatible (−). If the plant genotype is homozygous for the recessive susceptibility alleles rA or rB, or the pathogen genotype has the virulence alleles avrA or avrB, the pathogen is not recognised, defences are not triggered and infection occurs, the interaction is a compatible one (+). In the host genotypes with the dominant resistance alleles (RA/− and/or RB/−), the relative fitness of the avirulent pathogen genotypes (alleles AVRA or AVRB) is near zero, whereas that of the virulent ones (avrA or avrB) is considered as 1. In the host genotype rArA, rBrB the virulent pathogen genotype has a lower relative fitness than the avirulent genotype (cost of pathogenicity). The panel at the lower right shows that costs of pathogenicity may also differ according to the number of virulence factors and the host genotype.

Figure 2.

Two loci matching‐alleles model of host–pathogen co‐evolution for a diploid host and a haploid pathogen species. The product of alleles A and B at two loci in the host genotype interact with the products of the virulence alleles VA and VB at two loci in the pathogen genotype, allowing infection (+). This interaction does not occur with the product of alleles va or vb, resulting in a lack of susceptibility (−) or resistance. Similarly, the product of alleles a and b in the host interact with the products of alleles va and vb in the pathogen, allowing infection, but not with the products of allele VA or VB. For infection, the right interaction must occur with the products of both loci. In a pure matching‐alleles model, the relative fitness of the pathogen is 1 if infection occurs, and is 0 in the incompatible interaction, and there are no fitness penalties for pathogenicity. Here alleles A, B and a, b are represented as dominant and recessive, respectively, but this is not a requirement of the model.



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Further Reading

Bergelson J, Dwyer G and Emerson JJ (2001) Models and data on plant–enemy coevolution. Annual Review of Genetics 35: 469–499.

Caranta C, Aranda MA, Tepfer M and López‐Moya JJ (eds) (2011) Recent Advances in Plant Virology, 470 pp. Norfolk, UK: Caister Academic Press.

Desbiez C, Moury B and Lecoq H (2011) The hallmarks of “green” viruses: do plant viruses evolve differently from the others? Infection Genetics and Evolution 11: 812–824.

Eitas TK and Dangl JL (2010) NB‐LRR proteins: pairs, pieces, perception, partners and pathways. Current Opinion in Plant Biology 13: 472–477.

Elena SF, Badhomme S, Carrasco P et al. (2011) The evolutionary genetics of emerging plant RNA viruses. Molecular Plant–Microbe Interactions 24: 287–293.

Elena SF, Carrera J and Rodrigo G (2011) A systems biology approach to the evolution of plant virus interactions. Current Opinion in Plant Biology 14: 372–377.

Maule AJ, Caranta C and Boulton MI (2007) Sources of natural resistance to plant viruses: status and prospects. Molecular Plant Pathology 8: 223–231.

McDowell JM and Simon SA (2006) Recent insights into R gene evolution. Molecular Plant Pathology 7: 437–448.

Sacristán S and García‐Arenal F (2008) The evolution of virulence and pathogenicity in plant pathogen populations. Molecular Plant Pathology 9: 369–384.

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Fraile, Aurora, and García‐Arenal, Fernando(Feb 2012) Virus–Plant Co‐evolution. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0023723]