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DETERMINANTS OF PLANT VIRUS SEED TRANSMISSION AND SPECIATION

Group leader: Jesús Israel Pagán Muñoz - Associate Professor

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910679197 (Office 225 )

910679133 (Lab 227)

Personnel:

García Ordoñez, Lucía - PhD Student

Lewis Lewis, Tiene - Technician

Martín Castro, Laura - TFG Student

Rascón García, Cristina - TFG Student

Rodríguez Mello, Camila - TFG Student

Romero Azcondo, Pablo - Technician

Vázquez Sández, María - TFM Student

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

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

Representative Publications

Broncano-Lavado, A., Aguilera-Correa, J.J., Roquet-Banères, F., Kremer, L., Mediero, A., Seoane-Blanco, M., van Raaij, M.J., Pagán, I., Esteban, J., García-Quintanilla, M. 2025. P3MA: A Promising Mycobacteriophage Infecting Mycobacterium abscessus. Antibiotics 14, 801. DOI: 10.3390/antibiotics14080801

Jaime, C., Montes, N., Gil-Valle, M., Dunger, G., Pagán, I. 2025. The interplay between virus infection and water-related stress is mediated by the plant metabolism of ascorbic acid. New Phytologist. DOI: 10.1111/nph.70180

Santamaría-Corral, G., Pagán, I., Aguilera-Correa, J.J., Esteban, J., García-Quintanilla, M. 2024. A Novel Bacteriophage Infecting Multi-Drug- and Extended-Drug-Resistant Pseudomonas aeruginosa Strains. Antibiotics 13, 523. DOI: 10.3390/antibiotics13060523

García-Ordóñez, L., Pagán, I. 2024. Vertical and horizontal transmission of plant viruses: two extremes of a continuum?. npj Viruses 2, 1–10. DOI: 10.1038/s44298-024-00030-8

Sáez, C., Pagán, I. 2024. Plant viruses traveling without passport. PLOS Biology 22, e3002626. DOI: 10.1371/journal.pbio.3002626

Gil-Valle, M., Sáez, C., Montes, N., Pagán, I. 2024. Quantification of Plant Virus Seed Transmission Rate in Arabidopsis thaliana, in: Fontes, E.P.B., Mäkinen, K. (Eds.), Plant-Virus Interactions, Methods in Molecular Biology. Springer US, New York, NY, pp. 181–192. DOI: 10.1007/978-1-0716-3485-1_13

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

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

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