Virus–Plant Co‐evolution

Abstract

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.

close

References

Agrawal AF and Lively CM (2002) Infection genetics: gene‐for‐gene versus matching‐alleles models and all points in between. Evolutionary Ecology Research 4: 79–90.

Albar L, Ndjiondjop MN, Esshak Z et al. (2003) Fine genetic mapping of a gene required for Rice yellow mottle virus cell‐to‐cell movement. Theoretical and Applied Genetics 107: 371–378.

Anderson RM and May RM (1982) Coevolution of hosts and parasites. Parasitology 85: 411–426.

Andrade M, Abe Y, Nakahara KS and Uyeda I (2009) The cyv‐2 resistance to Clover yellow vein virus in pea is controlled by the eukaryotic initiation factor 4E. Journal of General Plant Pathology 75: 241–249.

Ayme V, Petit‐Pierre J, Souche S, Palloix A and Moury B (2007) Molecular dissection of the potato virus Y VPg virulence factor reveals complex adaptations to the pvr2 resistance allelic series in pepper. Journal of General Virology 88: 1594–1601.

Ben Khalifa M, Simon V, Fakhfakh H and Moury B (2011) Tunisian potato virus Y isolates with unnecessary pathogenicity towards pepper: support for the matching allele model in eIF4E resistance–potyvirus interactions. Plant Pathology DOI: 10.1111/j.1365‐3059.2011.02540.x.

Bendahmane A, Kanyuka KV and Baulcombe DC (1997) High resolution and physical mapping of the Rx gene for extreme resistance to potato virus X in tetraploid potato. Theoretical and Applied Genetics 95: 153–162.

Bendahmane A, Kanyuka KV and Baulcombe DC (1999) The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11: 781–792.

Bendahmane A, Quercy M, Kanyuka KV and Baulcombe DC (2000) Agrobacterium transient expression system as a tool for the isolation of disease resistant genes: application to the Rx2 locus in potato. Plant Journal 21: 73–81.

Berzal‐Herranz A, de la Cruz A, Tenllado F et al. (1995) The Capsicum L3 gene‐mediated resistance against the tobamoviruses is elicited by the coat protein. Virology 209: 498–505.

Brommonschenkel SH, Frary A and Tanksley SD (2000) The broad‐spectrum tospovirus resistance gene Sw‐5 of tomato is a homolog of the root‐knot nematode resistance gene Mi. Molecular Plant–Microbe Interactions 13: 1130–1138.

Bruun‐Rasmussen M, Moller IS, Tulinius G et al. (2007) The same allele of translation initiation factor 4E mediates resistance against two Potyvirus spp. in Pisum sativum. Molecular Plant–Microbe Interactions 20: 1075–1082.

Caranta C, Palloix A, GebreSelassie K et al. (1996) A complementation of two genes originating from susceptible Capsicum annuum lines confers a new and complete resistance to pepper veinal mottle virus. Phytopathology 86: 739–743.

Charron C, Nicolaï M, Gallois J‐L et al. (2008) Natural variation and functional analyses provide evidence for co‐evolution between plant eIF4E and potyviral VPg. Plant Journal 54: 56–68.

Chisholm ST, Mahajan SK, Whitham SA, Yamamoto ML and Carrington JC (2000) Cloning of the Arabidopsis RTM1 gene, which controls restriction of long‐distance movement of tobacco etch virus. Proceedings of the National Academy of Sciences of the USA 97: 489–494.

Clarke DD (1986) Tolerance of parasites and disease in plants and its significance in host–parasite interactions. Advances in Plant Pathology 5: 161–198.

Cooley MB, Pathirana S, Wu HJ, Kachroo P and Klessig DF (2000) Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. Plant Cell 12: 663–676.

Cosson P, Sofer L, Le QH et al. (2010) RTM3, which controls long‐distance movement of potyviruses, is a member of a new plant gene family encoding a meprin and TRAF homology domain‐containing protein. Plant Physiology 154: 222–232.

Decroocq V, Salvado B, Sicard O et al. (2009) The determinant of Potyvirus ability to overcome the RTM resistance of Arabidopsis thaliana maps to the N‐terminal region of the coat protein. Molecular Plant–Microbe Interactions 22: 1302–1311.

Díaz JA, Nieto C, Moriones E, Truniger V and Aranda MA (2004) Molecular characterization of a Melon necrotic spot virus strain that overcomes the resistance in melon and non‐host plants. Molecular Plant–Microbe Interactions 17: 668–675.

Drake JW, Charlesworth B, Charlesworth D and Crow JF (1998) Rates of spontaneous mutation. Genetics 148: 1667–1686.

Elena SF, Carrasco P, Darós JA and Sanjuan R (2006) Mechanisms of genetic robustness in RNA viruses. EMBO Reports 7: 168–173.

Escriu F, Fraile A and García‐Arenal F (2007) Constraints to genetic exchange support gene coadaptation in a tripartite RNA virus. PLoS Pathogens 3: e8.

Farnham G and Baulcombe DC (2006) Artificial evolution extends the spectrum of viruses that are targeted by a disease‐resistance gene from potato. Proceedings of the National Academy of Sciences of the USA 103: 18828–18833.

Fraile A and García‐Arenal F (2010) The coevolution of plants and viruses: resistance and pathogenicity. Advances in Virus Research 76: 1–32.

Fraile A, Pagán I, Anastasio G, Saez E and García‐Arenal F (2011) Rapid genetic diversification and high fitness penalties associated with increased pathogenicity in a plant virus. Molecular Biology and Evolution 28: 1425–1437.

Frank SA (1996) Models of parasite virulence. Quarterly Review of Biology 71: 37–78.

Friedman AR and Baker BJ (2007) The evolution of resistance genes in multi‐protein plant resistance systems. Current Opinion in Genetics & Development 17: 493–499.

Gallois J‐L, Charron C, Sanchez F et al. (2010) Single amino acid changes in the turnip mosaic virus viral genome‐linked protein (VPg) confer virulence towards Arabidopsis thaliana mutants knocked out for eukaryotic initiation factors eIF(iso)4E and elF(iso)4G. Journal of General Virology 91: 288–293.

Gao ZH, Johansen E, Eyers S et al. (2004) The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell‐to‐cell trafficking. Plant Journal 40: 376–385.

García‐Arenal F and McDonald BA (2003) An analysis of the durability of resistance to plant viruses. Phytopathology 93: 941–952.

Garrido‐Ramírez ER, Sudarshana MR, Lucas WJ and Gilbertson RL (2000) Bean dwarf mosaic virus BV1 protein is a determinant of the hypersensitive response and avirulence in Phaseolus vulgaris. Molecular Plant–Microbe Interactions 13: 1184–1194.

Gibbs AJ (1980) A plant virus that partially protects its wild legume host against herbivores. Intervirology 13: 42–47.

Gómez P, Rodríguez‐Hernández AM, Moury B and Aranda MA (2009) Genetic resistance for the sustainable control of plant virus diseases: breeding, mechanisms and durability. European Journal of Plant Pathology 125: 1–22.

Hajimorad MR, Eggenberger AL and Hill JH (2005) Loss and gain of elicitor function of Soybean mosaic virus G7 provoking Rsv1‐mediated lethal systemic hypersensitive response maps to P3. Journal of Virology 79: 1215–1222.

Hamada H, Tomita R, Iwadate Y et al. (2007) Cooperative effect of two amino acid mutations in the coat protein of Pepper mild mottle virus overcomes L3‐mediated resistance in Capsicum plants. Virus Genes 34: 205–214.

Hanada K and Harrison BD (1977) Effects of virus genotype and temperature on seed transmission of nepoviruses. Annals of Applied Biology 85: 79–92.

Harrison BD (2002) Virus variation in relation to resistance breaking plants. Euphytica 124: 181–192.

Hayes AJ, Jeong SC, Gore MA et al. (2004) Recombination within a nucleotide‐binding site/leucine‐rich‐repeat gene cluster produces new variants conditioning resistance to soybean mosaic virus in soybeans. Genetics 166: 493–503.

Hebrard E, Poulicard N, Gerard C et al. (2010) Direct interaction between the Rice yellow mottle virus (RYMV) VPg and the central domain of the rice eIF(iso)4G1 factor correlates with rice susceptibility and RYMV virulence. Molecular Plant–Microbe Interactions 23: 1506–1513.

Hofinger BJ, Russell JR, Bass CG et al. (2011) An exceptionally high nucleotide and haplotype diversity and a signature of positive selection for the eIF4E resistance gene in barley are revealed by allele mining and phylogenetic analyses of natural populations. Molecular Ecology 20: 3653–3668.

Ishibashi K, Masuda K, Naito S, Meshi T and Ishikawa M (2007) An inhibitor of viral RNA replication is encoded by a plant resistance gene. Proceedings of the National Academy of Sciences of the USA 104: 13833–13838.

Janzac B, Fabre F, Palloix A and Moury B (2009) Constraints on evolution of virus avirulence factors predict the durability of corresponding plant resistances. Molecular Plant Pathology 10: 599–610.

Janzac B, Montarry J, Palloix A, Navaud O and Moury B (2010) A point mutation in the polymerase of potato virus y confers virulence toward the Pvr4 resistance of pepper and a high competitiveness cost in susceptible cultivar. Molecular Plant–Microbe Interactions 23: 823–830.

Jarozs AM and Davelos AI (1995) Effects of disease in wild plant populations and the evolution of pathogen aggressiveness. New Phytologist 129: 371–387.

Jeger MJ, Seal SE and Van den Bosch F (2006) Evolutionary epidemiology of plant virus disease. Advances in Virus Research 67: 163–203.

Jenner CE, Wang X, Ponz F and Walsh JA (2002) A fitness cost for Turnip mosaic virus to overcome host resistance. Virus Research 86: 1–6.

Kang BC, Yeam I and Jahn MM (2005a) Genetics of virus resistance. Annual Review of Phytopathology 43: 581–621.

Kang BC, Yeam I, Frantz JD, Murphy JF and Jahn MM (2005b) The pvr1 locus in pepper encodes a translation initiation factor eIF4E that interacts with Tobacco etch virus VPg. Plant Journal 41: 392–405.

Kanyuka K, McGrann G, Alhudaib K, Hariri D and Adams MJ (2004) Biological and sequence analysis of a novel European isolate of Barley mild mosaic virus that overcomes the barley rym5 resistance gene. Archives of Virology 149: 1469–1480.

Lanfermeijer FC, Dijkhuis J, Sturre MJ, de Haan P and Hille J (2003) Cloning and characterization of the durable tomato mosaic virus resistance gene Tm‐22 from Lycopersicon esculentum. Plant Molecular Biology 52: 1037–1049.

Lanfermeijer FC, Warmink J and Hille J (2005) The products of the broken Tm‐2 and the durable Tm‐22 resistance genes from tomato differ in four amino acids. Journal of Experimental Botany 56: 2925–1933.

Lee J‐H, Muhsin M, Atienza GA et al. (2009) Single nucleotide polymorphisms in a gene for translation initiation factor (eIF4G) of rice (Oryza sativa) associated with resistance to Rice tungro spherical virus. Molecular Plant–Microbe Interactions 23: 29–38.

Lefeuvre P, Lett JM, Reynaud B and Martin DP (2007) Avoidance of protein fold disruption in natural virus recombinants. PLoS Pathogens 3: e181.

Malmstrom CM, Stoner CJ, Brandenburg S and Newton LA (2006) Virus infection and grazing exert counteracting influences on survivorship of native bunchgrass seedlings competing with invasive exotics. Journal of Ecology 94: 264–275.

Martin DP, van der Walt E, Posada D and Rybicki EP (2005) The evolutionary value of recombination is constrained by genome modularity. PLoS Genetics 1: 475–479.

Meshi T, Motoyoshi F, Adachi A et al. (1988) Two concomitant base substitutions in the putative replicase genes of tobacco mosaic virus confer the ability to overcome the effects of tomato resistance gene, Tm‐1. EMBO Journal 7: 1575–1581.

Moffett P (2009) Mechanisms of recognition in R gene mediated resistance. Advances in Virus Research 75: 1–33.

Moury B, Morel C, Johansen E et al. (2004) Mutations in Potato virus Y genome‐linked protein determine virulence toward recessive resistances in Capsicum annuum and Lycopersicon hirsutum. Molecular Plant–Microbe Interactions 17: 322–329.

Naderpour M, Lund OS, Larsen R and Johansen E (2010) Potyviral resistance derived from cultivars of Phaseolus vulgaris carrying bc‐3 is associated with the homozygotic presence of a mutated eIF4E allele. Molecular Plant Pathology 11: 255–263.

Nicaise V, German‐Retana S, Sanjuan R et al. (2003) The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the potyvirus Lettuce mosaic virus. Plant Physiology 132: 1272–1282.

Nieto C, Morales M, Orjeda G et al. (2006) An eIF4E allele confers resistance to an uncapped and non‐polyadenylated RNA virus in melon. Plant Journal 48: 452–462.

Padgett HS, Watanabe Y and Beachy RN (1997) Identification of the TMV replicase sequence that activates the N gene mediated hypersensitive response. Molecular Plant–Microbe Interactions 10: 709–715.

Pagán I, Alonso‐Blanco C and García‐Arenal F (2008) Host responses in life‐history traits and tolerance to virus infection in Arabidopsis thaliana. PLoS Pathogens 4: e1000124.

Pagán I, Alonso‐Blanco C and García‐Arenal F (2009) Differential tolerance to direct and indirect density‐dependent costs of viral infection in Arabidopsis thaliana. PLoS Pathogens 5: e1000531.

Palloix A, Ayme V and Moury B (2009) Durability of plant major resistance genes to pathogens depends on the genetic background, experimental evidence and consequences for breeding strategies. New Phytologist 18: 190–199.

Poulicard N, Pinel‐Galzi A, Hebrard E and Fargette D (2010) Why Rice yellow mottle virus, a rapidly evolving RNA plant virus, is not efficient at breaking rymv1–2 resistance. Molecular Plant Pathology 11: 145–154.

Power AG and Mitchell CE (2004) Pathogen spillover in disease epidemics. American Naturalist 164: S79–S89.

Roossinck MJ (2011) The good viruses: viral mutualistic symbioses. Nature Reviews Microbiology 9: 99–108.

Roudet‐Tavert G, Michon T, Walter J, Redondo E and Le Gall O (2007) Central domain of a Potyvirus VPg is involved in the interaction with the host translation initiation factor eIF4E and the viral protein HcPro. Journal of General Virology 88: 1029–1033.

Ruffel S, Dussault MH, Palloix A and Caranta C (2002) A natural recessive resistance gene against potato virus Y in pepper corresponds to the eukaryotic initiation factor 4E (eIF4E). Plant Journal 32: 1067–1075.

Ruffel S, Gallois JL, Lesage M et al. (2005) The recessive potyvirus resistance gene pot‐1 is the tomato orthologue of the pepper pvr2‐eIF4E gene. Molecular Genetics & Genomics 274: 346–353.

Ruffel S, Gallois JL, Moury B et al. (2006) Simultaneous mutations in translation initiation factors eIF4E and eIF(iso)4E are required to prevent pepper veinal mottle virus infection of pepper. Journal of General Virology 87: 2089–2098.

Saito T, Meshi T, Takamatsu N and Okada Y (1987) Coat gene sequence of tobacco mosaic virus encodes host response determinant. Proceedings of the National Academy of Sciences of the USA 84: 6074–6077.

Sanjuán R, Moya A and Elena SF (2004) The contribution of epistasis to the architecture of fitness in an RNA virus. Proceedings of the National Academy of Sciences of the USA 101: 15376–15379.

Schaad MC, Anderberg RJ and Carrington JC (2000) Strain‐specific interaction of the tobacco etch virus NIa protein with the translation initiation factor eIF4E in the yeast two‐hybrid system. Virology 273: 300–306.

Seo Y‐S, Rojas MR, Lee J‐Y et al. (2006) A viral resistance gene from common bean functions across plant families and is up‐regulated in a non‐virus‐specific manner. Proceedings of the National Academy of Sciences of the USA 103: 11856–11861.

Seo Y‐S, Jeon JS, Rojas MR and Gilbertson RL (2007) Characterization of a novel Toll/interleukin‐1 receptor (TIR)‐TIR gene differentially expressed in common bean (Phaseolus vulgaris cv. Othello) undergoing a defence response to the geminivirus Bean dwarf mosaic virus. Molecular Plant Pathology 8: 151–162.

Stein N, Perovic D, Kumlehn J et al. (2005) The eukaryotic translation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare. Plant Journal 42: 912–922.

Takahashi H, Miller J, Nonaki Y et al. (2002) RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant Journal 32: 655–667.

Thiemele D, Boisnard A, Ndjiondjop MN et al. (2010) Identification of a second major resistance gene to Rice yellow mottle virus, RYMV2, in the African cultivated rice species, O. glaberrima. Theoretical and Applied Genetics 121: 169–179.

Tomita R, Murai J, Miura Y et al. (2008) Fine mapping and DNA fiber FISH analysis locates the tobamovirus resistance gene L3 of Capsicum chinense in a 400‐kb region of R‐like genes cluster embedded in highly repetitive sequences. Theoretical and Applied Genetics 117: 1107–1118.

Traoré O, Pinel‐Galzi A, Issaka S et al. (2010) The adaptation of Rice yellow mottle virus to the eIF(iso)4G‐mediated rice resistance. Virology 408: 103–108.

Truniger V and Aranda MA (2009) Recessive resistance to plant viruses. Advances in Virus Research 75: 119–159.

Vidal S, Cabrera H, Andersson RA, Fredriksson A and Valkonen JPT (2002) Potato gene Y‐1 is an N gene homolog that confers cell death upon infection with potato virus Y. Molecular Plant–Microbe Interactions 15: 717–727.

Weber H and Pfitzner AJP (1998) Tm22 resistance in tomato requires recognition of the carboxy terminus of the movement protein of tomato mosaic virus. Molecular Plant–Microbe Interactions 11: 498–503.

Weber H, Ohnesorge S, Silber MV and Pfitzner AJP (2004) The Tomato mosaic virus 30kDa movement protein interacts differentially with the resistance genes Tm‐2 and Tm‐22. Archives of Virology 149: 1499–1514.

Whitham SA, Anderberg RJ, Chisholm ST and Carrington JC (2000) Arabidopsis RTM2 gene is necessary for specific restriction of tobacco etch virus and encodes an unusual small heat shock‐like protein. Plant Cell 12: 569–582.

Whitham S, Dinesh‐Kumar SP, Choi D et al. (1994) The product of the tobacco mosaic virus resistance gene N: similarity to Toll and the interleukin‐1 receptor. Cell 78: 1101–1115.

Woolhouse MEJ, Webster JP, Domingo E, Charlesworth B and Levin BR (2002) Biological and biomedical implications of the co‐evolution of pathogens and their hosts. Nature Genetics 32: 569–577.

Xu P, Chen F, Mannas JP et al. (2008) Virus infection improves drought tolerance. New Phytologist 180: 911–921.

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.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

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