PLANT-VIRUS INTERACTION AND CO-EVOLUTION

Personnel:


The long term research of the group focuses on understanding the emergence of new viral diseases. Plant viral diseases have a high socio-economic impact, as they affect crop and forest productivity as well as the composition and dynamics of natural ecosystems. The highest impact of diseases in host populations is often caused by emerging diseases, defined as those whose incidence in a host population is increasing as a result of long-term changes in their underlying epidemiology. Major factors favouring disease emergence are genetic change in pathogen and host populations, and changes in host ecology and environment. Hence, the research interests of the group are organised around the evolutionary ecology of plant-virus interactions.

The focus of our research is on plant virus evolution and plant-virus co-evolution, and the specific questions addressed include: i) the analysis of across-host fitness trade-offs as related to virus adaptation to new hosts species or genotypes, and of the underlying mechanisms, ii) the evolution of dominant and recessive resistance factors, iii) the mechanisms of tolerance of plants to viruses, and their relation with phenotypic plasticity, iv) the role of tolerance in plant-virus co-evolution. Last, and with the final goal of developing explanatory and/or predictive models of plant-virus-co-evolution, a significant effort is devoted to the analysis and estimation of relevant evolutionary parameters.

Model for Cucumber mosaic virus evolution in a two-host systems. Plants can be infected by virus genotypes Y, A and N that compete in mixed infections (M)

 

These questions are approached using different host-virus pathosystems, including both crops and wild plants in natural ecosystems. For instance, the evolution of pathogenicity and resistance is analysed both in viruses infecting pepper crops, and in natural populations of pepper wild relatives. A major thrust in the recent past has been on developing Arabidopsis thaliana as a model plant for the study of plant-virus co-evolution, both in its ecological an in its mechanistic aspects, because of the obvious advantages of this species for populational and molecular studies in plant biology.

Relevant results

The analysis of across-host fitness trade-offs has mostly focused on two systems. The first is pepper-infecting tobamoviruses, examples of specialist parasites. Long-term analysis of the genetic composition of the tobamovirus populations infecting pepper crops in SE Spain, jointly with molecular analyses of pathotype diversification and experimental estimates of relative fitnesses of different pathotypes, have provided sound evidence of fitness penalties associated to resistance-breaking and on how such penalties drive pathogenicity evolution in the virus (Fraile et al., 2011). Currently we analyse the possible role of antagonistic pleiotropy and epistasis in generating the observed trade-offs. Also, we are extending the analysis of pathogenicity-associated penalties to fitness components unrelated to the within host-multiplication component of the virus. Last, we have characterized the parameters and mechanisms of contact transmission of tobamoviruses, (Sacristán et al., 2011), an issue highly relevant for modelling their evolution in pepper crops.

 

The second system is Cucumber mosaic virus (CMV), an example of a generalist parasite with a broad host range. We have estimated the levels of within-host multiplication, virulence, transmissibility and within-host competition in mixed infections of different genotypes of this virus in melon, and compared the values of these parameters in melon and tomato, the two major hosts of the virus (Betancourt et al., 2011). These analyses are at the base for the development of a model describing and predicting the evolution of CMV virulence in a heterogeneous host system, a highly relevant approach to understand virulence evolution in generalist viruses.

On the plant-virus co-evolution side the most relevant results pertain to the analysis of the interaction of viruses with A. thaliana and wild peppers (Capsicum annuum var aviculare). Field surveys of six wild populations of A. thaliana in central Spain are being carried out since 2005 to monitor for the incidence of five brassica-infecting viruses, including CMV, in relation to host plant demography and environment. Partial results of this study have already been published (Pagán et al., 2010) showing, among other results, that CMV was the most prevalent virus. In parallel, the polymorphisms for resistance and tolerance, and the genetic structure for these defence traits, are being analysed in wild Arabidopsis populations of different sites in Spain. The analysis of tolerance mechanisms had shown that tolerance is due to plasticity in life-history traits, specifically, to altered resource allocation from vegetative growth to reproduction upon infection (Pagán et al., 2008). Presently, research focuses on how environmental conditions modulates tolerance to CMV in different Arabidopsis accessions, and on the possible involvement of genes regulating the flowering transition in tolerance.

 

The analysis of populations of the wild pepper, or chiltepín, in different bioeographical provinces of Mexico has allowed to analyse the spatial genetic structure of this plant species, and on how it is affected by human intervention, as this species is currently undergoing a process of domestication (González-Jara et al., 2011). On the same populations, the allelic variation at the L locus, determining dominant resistance to tobamoviruses, and at the pvr2 locus, determining recessive resistance to potyviruses, is being analysed.

On the same populations, the allelic variation at the L locus, determining dominant resistance to tobamoviruses, and at the pvr2 locus, determining recessive resistance to potyviruses, is being analysed. Data will allow to test the hypothesis of host-virus coevolution, and to analyse if the evolution of dominant and recessive resistance systems, that correspond to gene-for-gene and to matching-alleles models of host-pathogen interaction, evolve in nature. The analysis of chiltepin populations has also allowed to address the question of whether infection and disease risk are positively correlated with the degree of human modification of the host plant habitat, and on what are the key ecological factors behind. Results have shown that infection and disease risk are higher the higher the level of anthropisation of the habitat, and that species richness of the habitat is the major ecological factor (negatively) correlated with disease risk. These results, highly relevant to understand virus emergence, have been recently published (Pagán et al., 2012). These results also prompted the analysis of how landscape heterogeneity determines the population structure of chiltepin-infecting viruses, resulting in apparent co-evolution (Rodelo-Urrego et al., 2013) a subject that, again, is relevant to understand virus emergence.

 

Within the above framework, Dr. Israel Pagán is leading a new project on the modes of speciation in plant RNA viruses. This research is aimed at studying the processes and ecological determinants involved in the generation of new plant virus variants in natural ecosystems. This is a long-standing goal in the research areas of virology and evolution, as knowledge on this topic is central to understand the emergence of new viral diseases. Specifically, the project is focused on exploring the population genetic structure and epidemiology of species of the genus Potyvirus that infect plant communities in evergreen oak forests of the Iberian Peninsula, and on understanding how host ecological traits determine the genetic diversity of the virus populations.

 

Representative Publications

Shukla, A; Pagán, I; García-Arenal, F. 2017. "Effective tolerance based on resource reallocation is a virus-specific defence in Arabidopsis thaliana". Molecular Plant Pathology. DOI: 10.1111/mpp.12629".

Fernández-Tabanera, E; Fraile, A; Lunello, P; Garcia-Arenal, F; Ayllon, MA. 2017. "First Report of Onion Yellow Dwarf Virus in Leek (Allium ampeloprasum var. porrum) in Spain". Plant Disease. DOI: 10.1094/PDIS-06-17-0892-PDN".

Bera, S; Moreno-Pérez, MG; García-Figuera, S; Pagán, I; Fraile, A; Pacios, LF; García-Arenal, F. 2017. "Pleiotropic effects of resistance-breaking mutations on particle stability provide insight on life history evolution in a plant RNA virus". Journal of Virology. DOI: 10.1128/jvi.00435-17".

Parizad, S; Dizadji, A; Habibi, MK; Mohammadi, GHM; Kalantari, S; Izadpanah, F; García-Arenal, F; Winter, S. 2017. "Identification and partial characterization of the virus infecting saffron (Crocus sativus) in Iran". Iranian Journal of Plant Protection Science. DOI: 10.22059/ijpps.2017.215361.1006735".

Moreno-Pérez, MG; García-Luque, I; Fraile, A; García-Arenal, F. 2016. "Mutations determining resistance-breaking in a plant RNA virus have pleiotropic effects on its fitness that depend on the host environment and on the type, single or mixed, of infection". Journal of Virology. DOI: 10.1128/jvi.00737-16".

Poulicard, N; Pacios, LF; Gallois, J-L; Piñero, D; García-Arenal, F. 2016. "Human management of a wild plant modulates the evolutionary dynamics of a gene determining recessive resistance to virus infection". PLoS Genetics. DOI: 10.1371/journal.pgen.1006214".

Betancourt, M; Fraile, A; Milgroom, MG; García-Arenal, F. 2016. "Aphid vector population density determines the emergence of necrogenic satellite RNAs in populations of cucumber mosaic virus". Journal of General Virology. DOI: 10.1099/jgv.0.000435".

Donaire, L; Burgyan, J; Garcia-Arenal, F. 2016. "RNA silencing may play a role in but is not the only determinant of the multiplicity of infection". Journal of Virology. DOI: 10.1128/JVI.02345-15".

Fraile, A; García-Arenal, F. 2016. "Environment and evolution modulate plant virus pathogenesis". Current Opinion in Virology. DOI: 10.1016/j.coviro.2016.01.008".

Hily, J-M; Poulicard, N; Mora, M-Á; Pagán, I; García-Arenal, F. 2016. "Environment and host genotype determine the outcome of a plant–virus interaction: from antagonism to mutualism". New Phytologist. DOI: 10.1111/nph.13631".

Fraile, A; García-Arenal, F. 2015. "Modelling infection dynamics and evolution of viruses in plant populations", p. 89-93. In M. Corbera, J. M. Cors, J. Llibre, and A. Korobeinikov (eds.), Trends in Mathematics, vol. 4. Springer International Publishing, Switzerland. DOI: 10.1007/978-3-319-22129-8_16".

Gessain, A; García-Arenal, F. 2015. "Editorial overview: Emerging viruses: interspecies transmission". Current Opinion in Virology. DOI: http://dx.doi.org/10.1016/j.coviro.2015.02.001".

Tepfer, M; Jacquemond, M; García-Arenal, F. 2015. "A critical evaluation of whether recombination in virus-resistant transgenic plants will lead to the emergence of novel viral diseases". New Phytologist. DOI: 10.1111/nph.13358".

Roossinck, MJ; García-Arenal, F. 2015. "Ecosystem simplification, biodiversity loss and plant virus emergence". Current Opinion in Virology. DOI: 10.1016/j.coviro.2015.01.005".

Pagán, I; Montes, M; Milgroom, MG; García-Arenal, F. 2014. "Vertical transmission selects for reduced virulence in a plant virus and for increased resistance in the host". PLoS Pathogens. DOI: 10.1371/journal.ppat.1004293".

Fraile, A; Hily, J-M; Pagán, I; Pacios, LF; García-Arenal, F. 2014. "Host resistance selects for traits unrelated to resistance-breaking that affect fitness in a plant virus". Molecular Biology and Evolution. DOI: 10.1093/molbev/msu045".

Rodelo-Urrego, M; Pagán, I; González-Jara, P; Betancourt, M; Moreno-Letelier, A; Ayllón, MA; Fraile, A; Piñero, D; García-Arenal, F. 2013. "Landscape heterogeneity shapes host-parasite interactions and results in apparent plant-virus codivergence". Molecular Ecology. DOI: 10.1111/mec.12232".

Betancourt, M; Escriu, F; Fraile, A; García-Arenal, F. 2013. "Virulence evolution of a generalist plant virus in a heterogeneous host system". Evolutionary Applications. DOI: 10.1111/eva.12073".

Pagan, I.; Gonzalez-Jara, P.; Moreno-Letelier, A.; Rodelo-Urrego, M.; Fraile, A.; Pinero, D.; Garcia-Arenal, F. 2012. Effect of biodiversity changes in disease risk: exploring disease emergence in a plant-virus system. PLoS Pathog 8:e1002796.

Centro de Biotecnología y Genómica de Plantas UPM – INIA Parque Científico y Tecnológico de la U.P.M. Campus de Montegancedo
Autopista M-40, Km 38 - 28223 Pozuelo de Alarcón (Madrid) Tel.: +34 91 4524900 ext. 1806 / +34 91 3364539 Fax: +34 91 7157721. Contacto

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