DETERMINANTS OF PLANT VIRUS SEED TRANSMISSION AND SPECIATION

Group leader: Jesús Israel Pagán Muñoz - Assistant Professor
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Personnel:


The FAO estimates that, in the next 35 years, global agricultural production will need to increase by 60% to achieve acceptable levels of food safety for a human population that would reach nine billion. One of the most serious challenges to achieve this goal is to reduce the impact of emerging infectious diseases in crop production. Emerging diseases in plants are mainly caused by RNA viruses, which affect negatively sustainable food production by reducing crop quality and yield. The main focus of our research is to understand the processes of plant virus emergence, with the ultimate goal of contributing to control emerging diseases.



Evergreen oak and riparian forest in the Iberian Peninsula

 

A key feature of RNA viruses, which is often associated with disease emergence, is their high potential to generate genetic diversity. This characteristic provides RNA viruses with a high capacity for adaptation to new environments, including new hosts. Adaptation to new host genotypes or species may lead to diversification of the virus population, which may result in the emergence of new diseases caused by the appearance of new viral lineages or species: that is, by ‘speciation’ events. Although virus speciation is central to understand disease emergence, its determinants are still poorly understood. One of the major research goals of our group is characterizing the ecological and genetic factors that drive speciation processes of RNA virus populations. We are especially interested in understanding how ecosystem biodiversity influences virus speciation and emergence. To address this subject, we analyze how changes in biodiversity and other ecological traits of evergreen oak forests and riparian forests of the Iberian Peninsula affect the population genetic diversity and prevalence of plant RNA viruses of the genus Potyvirus, which makes 25% of all known plant viruses. These two ecosystems are frequently adjacent to crop lands, and are therefore a source of economically important pathogens such as potyviruses. We complement our epidemiological and molecular studies with bioinformatics approaches aimed at building mathematical models that predict the conditions favoring virus speciation according to ecosystem ecological conditions.


Schematic representation of the direct and indirect routes of virus seed invasion.

 

Another characteristic of plant viruses that facilitates disease emergence is their great potential to spread rapidly. About 25% of all known plant viruses are vertically transmitted from parent to offspring through the seeds, and this is surely an underestimate as more viruses are reported to be seed transmitted every year. Given that approximately 90% of the food crops grown worldwide are propagated from seeds, seed transmitted viruses are an important threat for crop production. Seed infection provides the virus with a mean to persist for long periods of time when hosts or vectors are not available, allows for long distance dissemination of the virus via infected seeds, and represents an important source of primary inoculum for many viruses, which are disseminated afterwards via insect vectors. Current strategies to reduce the impact of seed transmitted viruses mostly involve routine seed health testing for seed certification and plant quarantine. However, the efficacy of these methods is limited. The second major research focus of our group is the characterization of the plant and virus genes that control seed transmission. To attain this goal, we use the model system formed by the plant Arabidopsis thaliana and two viruses that infect natural populations of this host and are seed-transmitted: Cucumber mosaic virus and Turnip mosaic virus. Our aim is using this knowledge with biotechnological purposes to obtain plant varieties immune to seed transmission. Thus, we work with seed and biotechnology companies to transfer our findings into economically important crops.


Phylogenetic differentiation of Rabies virus isolates according to the host of origin   

 

Our research interests are not only limited to plant viruses. We also collaborate with different national and international groups in the study of clinical and ecological determinants of the evolution and emergence of animal and human RNA viruses through comparative genomics approaches. For instance, we have contributed to understand the clinical determinants of between-host evolution in HIV infected children, and we have identified the ecological determinants of Rabies virus population genetic diversity.


Funding

  1. Ministerio de Economía y Competitividad. BIO2016-79165-R
  2. Marie Curie Actions. Carreer Integration Grant. PCIG11-GA-2012-322100

 


Representative Publications

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

Sáez, C., Pagán, I. 2022. When plants are Trojan horses for viruses. New Phytologist. DOI: 10.1111/nph.18571

Sáez, C., Pagán, I. 2022. When plants are Trojan horses for viruses. New Phytologist. DOI: 10.1111/nph.18571

Pagán, I. 2022. Transmission through seeds: The unknown life of plant viruses. PLOS Pathogens 18, e1010707. DOI: 10.1371/journal.ppat.1010707

Martín-Hernández, I., Pagán, I. 2022. Gene Overlapping as a Modulator of Begomovirus Evolution. Microorganisms 10, 366. DOI: 10.3390/microorganisms10020366

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

Montes, N., Vijayan, V., Pagán, I. 2021. Host population structure for tolerance determines the evolution of plant-virus interactions. New Phytologist. DOI: https://doi.org/10.1111/nph.17466

Montes, N., Cobos, A., Gil-Valle, M., Caro, E., Pagán, I. 2021. Arabidopsis thaliana Genes Associated with Cucumber mosaic virus Virulence and Their Link to Virus Seed Transmission. Microorganisms 9, 692. DOI: 10.3390/microorganisms9040692

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

Montes, N., Vijayan, V., Pagán, I. 2020. Trade-offs between host tolerances to different pathogens in plant–virus interactions. Virus Evolution 6. DOI: 10.1093/ve/veaa019

Rodríguez-Nevado, C., G. Gavilán, R., Pagán, I. 2019. Host Abundance and Identity Determine the Epidemiology and Evolution of a Generalist Plant Virus in a Wild Ecosystem. Phytopathology™ 110, 94–105. DOI: 10.1094/PHYTO-07-19-0271-FI

Cobos, A., Montes, N., López-Herranz, M., Gil-Valle, M., Pagán, I. 2019. Within-host multiplication and speed of colonization as infection traits associated with plant virus vertical transmission. Journal of Virology JVI.01078-19. DOI: 10.1128/JVI.01078-19

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

Pagán, I. 2018. "The diversity, evolution and epidemiology of plant viruses: A phylogenetic view". Infection, Genetics and Evolution. DOI: 10.1016/j.meegid.2018.07.033".

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

Rodríguez-Nevado, C; Lam, TTY; Holmes, EC; Pagán, I. 2018. "The impact of host genetic diversity on virus evolution and emergence". Ecology Letters. DOI: 10.1111/ele.12890".

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

Domínguez-Rodríguez, S; Rojas, P; Fernández McPhee, C; Pagán, I; Navarro, ML; Ramos, JT; Holguín, Á. 2018. "Effect of HIV/HCV Co-Infection on the Protease Evolution of HIV-1B: A Pilot Study in a Pediatric Population". Scientific Reports. DOI: 10.1038/s41598-018-19312-2".

Rodríguez-Nevado, C; Montes, N; Pagán, I. 2017. "Ecological factors affecting infection risk and population genetic diversity of a novel potyvirus in its native wild ecosystem". Frontiers in Plant Science. DOI: 10.3389/fpls.2017.01958".

Rojas Sánchez, P; Cobos, A; Navaro, M; Ramos, JT; Pagán, I; Holguín, Á. 2017. "Impact of clinical parameters in the intrahost evolution of HIV-1 subtype B in pediatric patients: A machine learning approach". Genome Biology and Evolution. DOI: 10.1093/gbe/evx193".

Vijayan, V; López-González, S; Sánchez, F; Ponz, F; Pagán, I. 2017. "Virulence evolution of a sterilizing plant virus: Tuning multiplication and resource exploitation". Virus Evolution. DOI: 10.1093/ve/vex033".

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".

Donaire, L; Pagán, I; Ayllón, MA. 2016. "Characterization of Botrytis cinerea negative-stranded RNA virus 1, a new mycovirus related to plant viruses, and a reconstruction of host pattern evolution in negative-sense ssRNA viruses". Virology. DOI: http://dx.doi.org/10.1016/j.virol.2016.09.017".

Pagán, I; Rojas, P; Ramos, JT; Holguín, A. 2016. "Clinical determinants of HIV-1B between-host evolution and their association with drug resistance in pediatric patients". PLoS One. DOI: 10.1371/journal.pone.0167383".

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".

Franco, L; Pagán, I; Serre Del Cor, N; Schunk, M; Neumayr, A; Molero, F; Potente, A; Hatz, C; Wilder-Smith, A; Sánchez-Seco, MP; Tenorio, A. 2015. "Molecular epidemiology suggests Venezuela as the origin of the dengue outbreak in Madeira, Portugal in 2012-2013". Clinical Microbiology and Infection. DOI: 10.1016/j.cmi.2015.03.016".

Muñoz-Alía, MÁ; Fernández-Muñoz, R; Casasnovas, JM; Porras-Mansilla, R; Serrano-Pardo, Á; Pagán, I; Ordobás, M; Ramírez, R; Celma, ML. 2015. "Measles virus genetic evolution throughout an imported epidemic outbreak in a highly vaccinated population". Virus Research. DOI: 10.1016/j.virusres.2014.11.015".

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".

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".

Pagán, I; Holguín, A. 2013. "Reconstructing the timing and dispersion routes of HIV-1 subtype B epidemics in the Caribbean and Central America: a phylogenetic story". PLoS One. DOI: 10.1371/journal.pone.0069218".

Simon-Loriere, E; Holmes, EC; Pagán, I. 2013. "The effect of gene overlapping on the rate of RNA virus evolution". Molecular Biology and Evolution. DOI: mst094 [pii] 10.1093/molbev/mst094".

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.