PLANT-VIRUS INTERACTION AND CO-EVOLUTION

Group leader: Fernando García-Arenal Rodríguez - Professor Emeritus
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Personnel:

 

The long term research goal of the group is understanding the emergence of new viral diseases, viruses being the major group of emergent pathogens of animals and plants.
  Plant viral diseases affect food security, crop and forest productivity, and the structure and functions of ecosystems. The highest socio-economic impact of infectious diseases is often caused by emerging diseases, i.e., those whose incidence is increasing in a new host population. Emergence is a complex eco-evolutionary process, requiring new host-virus encounters and virus adaptation to the new host. Understanding emergence is central to its anticipation and prevention.
  Hence, the research in the group is organised around the evolutionary ecology of plant-virus interactions. We focus on plant-virus co-evolution and on the factors that disrupt co-evolutionary dynamics. Specific questions currently addressed include:

  1. Assessing the role of ecosystem functional diversity in infection risk and virus host range
  2. Estimating the effect of virus infection in wild plant communities
  3. Identifying across-host fitness trade-offs that may condition host-range evolution, and disentangling the underlying mechanisms
  4. Understanding the factors that modulate virus virulence and plant defence
  5. Dissecting the molecular genetics of plant tolerance to virus infection


These questions are approached using different host-virus systems, including crops, model species and wild plants in natural ecosystems.

Relevant results

Virulence and tolerance as determinants of disease

A goal of our group is to understand which factors modulate virulence, i.e., the harmful effect on host fitness of pathogen infection. The effect of infection on hosts is jointly determined by pathogen and host factors. We focus on tolerance, a defence that specifically reduces virulence. We analyse tolerance in the Cucumber mosaic virus (CMV)-Arabidopsis thaliana interaction. We have shown that according to conditions of the abiotic environment this plant-virus interactions can be antagonistic or mutualistic. This relevant result introduces important uncertainties about the nature of CMV infection under field conditions, and about its effect on Arabidopsis populations. We have shown that Arabidopsis wild genotypes differ in tolerance to CMV, and that CMV field isolates differ in virulence to Arabidopsis, a condition for plant-virus co-evolution (Figure 1). Through the analysis of wild ecotypes and local populations of Arabidopsis in the Iberian Peninsula we have further shown that tolerance to CMV (as is the case for resistance) is under uniform selection, again a result compatible with a negative effect of infection in the plant fitness. These analyses are complemented by field experiments in which Arabidopsis genotypes are rated for tolerance and resistance to CMV, to be compared with results under controlled conditions. Moreover, demographic analyses of wild Arabidopsis populations in relation to virus infection are being performed, which will show, and allow to quantify, any effect of virus infection on the host fitness.

Figure 1. Wild genotypes of A. thaliana assayed for tolerance to CMV (left), which is a quantitative trait (rigth).

 

   In the recent past we have shown that tolerance of Arabidopsis to CMV is effected by developmental plasticity resulting in resource reallocation from growth to reproduction. Analyses of recombinant inbred lines derived from a cross between a tolerant and a non-tolerant genotype identified QTLs for tolerance that co-mapped with genes with a well-known role in flowering time regulation. Analyses of mutant and introgression lines have shown the role to floral regulator genes in tolerance. This research line, which merges infection and developmental genetics, is being pursued by characterising the role of these genes in the host plant response to CMV infection, and the underlying molecular mechanisms, which we hypothesise will involve their altered expression upon virus infection. This research line is developed in collaboration with Dr. Pedro Crevillén at CBGP.

Host range evolution and the overcoming of host resistance

Overcoming host resistance in gene-for-gene plant-virus interactions is an instance of host range expansion, which can be hindered by across-host fitness trade-offs. Identifying such trade-offs and their causes is relevant, as the use of genetic resistance is a major strategy for controlling viral diseases in crops. We have shown that overcoming of L-gene resistance in pepper by tobamoviruses was associated with severe within-host multiplication penalties. Results also showed that resistance-breaking (RB) mutations had pleiotropic effects on virus multiplication that were antagonistic or positive depending on the specific mutation, the host genotype, and the type of infection, single or mixed with other virus genotypes. Thus, the emergence of RB mutants will depend on the genetic structure of the host population and on the frequency of mixed infections. L-gene RB mutations occur in the virus coat protein, and we showed RB mutations affect particle stability and virus survival in the environment. These results showed the possibility of trade-offs between different virus life-history traits (reproduction and survival), and how plant resistance can select for altered survival, which may condition RB evolution. We are currently exploring how the interactions among genetic (pleiotropic effects of host-range mutations) and environmental factors (survival in the environment, mixed infections and other) modulate the genetic structure of tobamoviruses in pepper crops and in their wild reservoirs (Figure 2).


Figure 2. Tobbaco mild green mosaic virus (TMGMV) is an important pathogen of pepper with a wild reservoir in Nicotiana glauca (left). Host range mutations show pleiotropic effects and epistatic interactions (right).


 

Functional diversity and plant virus interactions

Ecosystem simplification due to human activities has been linked to virus emergence. To address this important question we have studied virus infection in the wild pepper or chiltepin, which grows in Mexico in different habitats, from wild to managed or cultivated populations. We have shown in the past that human management of the chiltepin habitat results in increased infection risk by two begomoviruses. We have more recently analysed the relationship between habitat anthropisation and genetic diversity, mutation fixation and recombination in these viruses. Further, we have shown by genetic and phenotypic characterization of the alleles of major dominant and recessive resistance genes, that anthropisation results in altered selection for resistance of chiltepin to potyviruses.


Even if information on the evolution of plant-virus interactions in the chiltepin system is highly relevant, it has the limitation, common to most studies, of focussing on single host –single pathogen systems. However, a full understanding of transmission pathways, disease risk, host-range evolution and, ultimately, emergence, requires the analysis of multi-host / multi-pathogen systems at the landscape scale. We have undertaken this ambitious goal focussing on four a priori habitats under different levels of human interventions, and characterised by different plant communities, in a heterogeneous agricultural landscape in Central Spain. Initial results from a set of 11 viruses on 83 plant species show unexpected relations that would have not been apparent in analyses of one virus or one habitat (Figure 3). Three important results are: i) virus host range depend on host community structure, viruses behaving as facultative generalists that specialise locally, ii) biodiversity-disease risk relations depend on community structure and on spatial scale, and iii) co-infections are capital determinants of infection network structure. This research is currently pursued at a finer detail, including a broader range of habitats, and a deeper analysis of viromes by means of deep sequencing techniques and by the development of new computational tools in collaboration with Dr. Sergi Valverde (Institute of Evolutionary Biology, CSIC, Barcelona, Spain).


Figure 3. Network of interactions among 11 gneralist viruses and 83 host plant species. Link coloir denotes the habitat where the interaction occurs, and node size proportional to the number of links.

 


In addition, the role of co-infecting communities at the single host level in plant-virus interactions is being analysed in a larger context by including the interaction of viruses and bacteria, and its possible role in pathogen virulence and evolution. This research line is developed in collaboration with Dr. Emila López-Solanilla at CBGP.


 


Representative Publications

Schönegger, D., Marais, A., Garcia Arenal, F., Malmstrom, C.M., Martinez Jimenez, M., McLeish, M., Lefebvre, M., Faure, C., Svanella-Dumas, L., Candresse, T. 2024. Sympatric populations of crop and wild carrots (Daucus carota ssp.) have distinct viromes, with shared core species more prevalent in farm-grown populations. Phytobiomes Journal. DOI: 10.1094/PBIOMES-06-24-0062-R

McLeish, M., Peláez, A., Pagán, I., Gavilán, R.G., Fraile, A., García-Arenal, F. 2024. Plant virus community structuring is shaped by habitat heterogeneity and traits for host plant resource utilisation. New Phytologist. DOI: 10.1111/nph.20054

Cuevas, B., Fraile, A., Garcia-Arenal, F. 2024. An Agent Based Model Shows How Mixed Infections Drive Multi-Year Pathotype Dynamics in a Plant-Virus System. Phytopathology®. DOI: 10.1094/PHYTO-06-23-0214-R

de Andrés-Torán, R., Guidoum, L., Zamfir, A.D., Mora, M.Á., Moreno-Vázquez, S., García-Arenal, F. 2023. Tobacco Mild Green Mosaic Virus (TMGMV) Isolates from Different Plant Families Show No Evidence of Differential Adaptation to Their Host of Origin. Viruses 15, 2384. DOI: 10.3390/v15122384

Poulicard, N., Pagán, I., González-Jara, P., Mora, M.Á., Hily, J.-M., Fraile, A., Piñero, D., García-Arenal, F. 2023. Repeated loss of the ability of a wild pepper disease resistance gene to function at high temperatures suggests that thermoresistance is a costly trait. New Phytologist. DOI: 10.1111/nph.19371

Babalola, B., Fraile, A., García-Arenal, F., McLeish, M. 2023. Ecological Strategies for Resource Use by Three Bromoviruses in Anthropic and Wild Plant Communities. Viruses 15, 1779. DOI: 10.3390/v15081779

Zamfir, A.D., Babalola, B.M., Fraile, A., McLeish, M., Garcia-Arenal, F. 2023. Tobamoviruses show broad host ranges and little genetic diversity among four habitat types of a heterogeneous ecosystem. Phytopathology®. DOI: 10.1094/PHYTO-11-22-0439-V

Elena, S.F., García-Arenal, F. 2023. Plant Virus Adaptation to New Hosts: A Multi-scale Approach, in: Domingo, E., Schuster, P., Elena, S.F., Perales, C. (Eds.), Viral Fitness and Evolution: Population Dynamics and Adaptive Mechanisms, Current Topics in Microbiology and Immunology. Springer International Publishing, Cham, pp. 167–196. DOI: 10.1007/978-3-031-15640-3_5

Pagán, I., García-Arenal, F. 2022. Cucumber Mosaic Virus-Induced Systemic Necrosis in Arabidopsis thaliana: Determinants and Role in Plant Defense. Viruses 14, 2790. DOI: 10.3390/v14122790

McLeish, M.J., Zamfir, A.D., Babalola, B.M., Peláez, A., Fraile, A., García-Arenal, F. 2022. Metagenomics show high spatiotemporal virus diversity and ecological compartmentalisation: Virus infections of melon, Cucumis melo, crops, and adjacent wild communities. Virus Evolution 8, veac095. DOI: 10.1093/ve/veac095

Moreno-Pérez, M.G., Bera, S., McLeish, M., Fraile, A., García-Arenal, F. 2022. Reversion of a resistance-breaking mutation shows reversion costs and high virus diversity at necrotic local lesions. Molecular Plant Pathology. DOI: 10.1111/mpp.13281

Babalola, B.M., Faure, C., Marais, A., Fraile, A., Garcia-Arenal, F., Candresse, T. 2022. First report of carrot torrado virus 1 (CaTV1) naturally infecting carrots in Spain. Journal of Plant Pathology. DOI: 10.1007/s42161-022-01196-x

Babalola, B.M., Schönegger, D., Faure, C., Marais, A., Fraile, A., Garcia-Arenal, F., Candresse, T. 2022. Identification of two novel putative satellite RNAs with hammerhead structures in the virome of French and Spanish carrot samples. Archives of Virology. DOI: 10.1007/s00705-022-05538-z

Babalola, B.M., Faure, C., Marais, A., Fraile, A., Garcia-Arenal, F., Candresse, T. 2022. First report of Apium virus Y in wild carrot (Daucus carota ssp. carota) in Spain. New Disease Reports 45, e12097. DOI: 10.1002/ndr2.12097

Shukla, A., Pagán, I., Crevillén, P., Alonso-Blanco, C., García-Arenal, F. 2021. A role of flowering genes in the tolerance of Arabidopsis thaliana to cucumber mosaic virus. Molecular Plant Pathology. DOI: 10.1111/mpp.13151

McLeish, M., Peláez, A., Pagán, I., Gavilán, R., Fraile, A., García-Arenal, F. 2021. Structuring of plant communities across agricultural landscape mosaics: the importance of connectivity and the scale of effect. BMC Ecology and Evolution 21, 173. DOI: 10.1186/s12862-021-01903-9

McLeish, M., Fraile, A., Garcia-Arenal, F. 2020. Population genomics of plant viruses: the ecology and evolution of virus emergence. Phytopathology®. DOI: 10.1094/PHYTO-08-20-0355-FI

Peláez, A., McLeish, M.J., Paswan, R.R., Dubai, B., Fraile, A., García‐Arenal, F. 2020. Ecological fitting is the forerunner to diversification in a plant virus with broad host range. Journal of Evolutionary Biology. DOI: 10.1111/jeb.13672

Pagán, I., García-Arenal, F. 2020. Tolerance of Plants to Pathogens: A Unifying View. Annual Review of Phytopathology. DOI: 10.1146/annurev-phyto-010820-012749

Valverde, S., Vidiella, B., Montañez, R., Fraile, A., Sacristán, S., García-Arenal, F. 2020. Coexistence of nestedness and modularity in host–pathogen infection networks. Nature Ecology & Evolution. DOI: 10.1038/s41559-020-1130-9

McLeish, M.J., Fraile, A., García‐Arenal, F. 2019. Trends and gaps in forecasting plant virus disease risk. Annals of Applied Biology 1–7. DOI: 10.1111/aab.12553

García-Arenal, F., Zerbini, F.M. 2019. Life on the Edge: Geminiviruses at the Interface Between Crops and Wild Plant Hosts. Annual Review of Virology 6, 411–433. DOI: 10.1146/annurev-virology-092818-015536

Montes, N., Pagán, I. 2019. Light Intensity Modulates the Efficiency of Virus Seed Transmission through Modifications of Plant Tolerance. Plants 8, 304. DOI: 10.3390/plants8090304

Bujarski, J., Gallitelli, D., García-Arenal, F., Pallás, V., Palukaitis, P., Reddy, M.K., Wang, A., ICTV Report Consortium 2019. ICTV Virus Taxonomy Profile: Bromoviridae. Journal of General Virology 100, 1206–1207. DOI: 10.1099/jgv.0.001282

Montes, N., Alonso-Blanco, C., García-Arenal, F. 2019. Cucumber mosaic virus infection as a potential selective pressure on Arabidopsis thaliana populations. PLOS Pathogens 15, e1007810. DOI: 10.1371/journal.ppat.1007810

McLeish, M.J., Fraile, A., García-Arenal, F. 2019. Evolution of plant–virus interactions: host range and virus emergence. Current Opinion in Virology, Emerging viruses: intraspecies transmission • Viral Immunology 34, 50–55. DOI: 10.1016/j.coviro.2018.12.003

McLeish, M., Sacristán, S., Fraile, A., Garcia-Arenal, F. 2018. Co-infection organises epidemiological networks of viruses and hosts and reveals hubs of transmission. Phytopathology. DOI: 10.1094/PHYTO-08-18-0293-R

Bera, S., Fraile, A., García-Arenal, F. 2018. Analysis of Fitness Trade-Offs in the Host Range Expansion of an RNA Virus, Tobacco Mild Green Mosaic Virus. Journal of Virology 92, e01268-18. DOI: 10.1128/JVI.01268-18

Fraile, A; García-Arenal, F. 2018. "Tobamoviruses as models for the study of virus evolution", Advances in Virus Research. Academic Press. DOI: 10.1016/bs.aivir.2018.06.006".

Parizad, S; Dizadji, A; Koohi Habibi, M; Winter, S; Kalantari, S; Movi, S; García-Arenal, F; Ayllón, MA. 2018. "Description and genetic variation of a distinct species of Potyvirus infecting saffron (Crocus sativus L.) plants in major production regions in Iran". Annals of Applied Biology 2018 v.173 no.3 pp. 233-242. DOI: 10.1111/aab.12456".

McLeish, MJ; Fraile, A; García-Arenal, F. "Ecological complexity in plant virus host range evolution", Advances in Virus Research. Academic Press. DOI: 10.1016/bs.aivir.2018.02.009".

Pagán, I; García-Arenal, F. 2018. "Tolerance to plant pathogens: theory and experimental Evidence". International Journal of Molecular Sciences. DOI: 10.3390/ijms19030810".

McLeish, M; Sacristán, S; Fraile, A; García-Arenal, F. 2017. "Scale dependencies and generalism in host use shape virus prevalence". Proceedings of the Royal Society Biological Sciences Series B. DOI: 10.1098/rspb.2017.2066".

Pagán, I; García-Arenal, F. "Population Genomics of Plant Viruses", p. 1-33. Springer International Publishing, Cham. DOI: 10.1007/13836_2018_15".

Fernández-Tabanera, E; Fraile, A; Lunello, P; Garcia-Arenal, F; Ayllon, MA. 2018. "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".

Parizad, S; Dizadji, A; Koohi Habibi, M; Winter, S; Kalantari, S; Garcia-Arenal, F; Ayllón, MA. 2017. "Prevalence of saffron latent virus (saLV), a new Potyvirus species, in saffron fields of Iran". Journal of Plant Pathology. DOI: 10.4454/jpp.v99i3.3963".

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".

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.