VIRUS-FUNGUS-PLANT INTERACTION: MYCOVIRUS OF BOTRYTIS CINEREA, MECHANISMS OF PATHOGENESIS AND VIRAL INFECTION EFFECT AT MOLECULAR LEVEL


Group leader: María Ángeles Ayllón Talavera - Associate Professor
This email address is being protected from spambots. You need JavaScript enabled to view it. 910679146 Ext:79146 / 910679132 Ext:79132 ( Lab 227-229)

 

Personnel:

 

Our research is adressed to elucidate phytopathogenic fungi-virus interactions focusing the studies on Botrytis cinerea.

The grey mold fungus Botrytis cinerea (teleomorph Botryotinia fuckeliana) is a necrotrophic plant pathogenic fungus that causes enormous economic losses worldwide in pre- and postharvest crops as important as horticultural, ornamental and fruit trees, so it has turned into model of study of necrotrophic fungi with a very wide host range. Fungal viruses or mycoviruses are widespread in all major groups of phytopathogenic fungi and, in general, are associated with non symptomatic infections of their hosts but some of them decrease the virulence of the infected fungus. The discovery of mycoviruses and its use as a tool to increase the knowledge about fungi biology, as well as its possible application in biocontrol strategies, has stimulated its study in B. cinerea. The main goal of our reseach is to gain insight in the molecular mechanisms of the interaction between mycoviruses and B. cinerea, and in the implications of this interaction with the plant, in order to develop future more efficient control strategies. We are interested in the biological and molecular characterization of mycoviruses that infect B. cinerea field isolates,  in their effects on fungal gene expression and virulence, in the RNA silencing function as an antiviral defense mechanism in B. cinerea, and also in the origin and evolution of mycoviruses.

We have analyzed two colletions of B. cinerea strains, one isolated from horticultural crops and other isolated from grapevine from the South and Center Spain, respectively, and found mycoviruses in most of them. We have performed the biological and molecular characterization of different novel mycoviruses infecting several Botrytis species and we have observed that some of them are related to plant viruses. We have also determined the effect of these viruses on the virulence and phenotype of the fungus. Now, we are analyzing the viral small RNAs populations in Botrytis species infected with different mycoviruses. In our new project we are very interested in the study of the origin and the evolution of mycoviruses, since some of them are related to plant viruses.

 


 Phylogenetic tree obtained by Maximum Likelihood method with the RdRp sequences of mycoviruses and plant ourmiaviruses.


Microconidia of B.cinerea.


Electron micrograph of a long flexuous rod shaped virus like particle in partially purified preparations from mycelium of a B. cinerea isolate.


Virulence of different isolates of B. cinerea infected with mycoviruses.

 

Projects:

  1. Virome NGS analysis of pests and pathogens for plant protection. H2020-SFS-17, 2018-2021. PI: M.A. Ayllón
    1. https://www.viroplant.eu/
    2. https://www.instagram.com/viroplant/?hl=es
    3. https://www.youtube.com/channel/UCTTQ45Ay9Th-vpaEqp_r7OQ
    4. https://twitter.com/viroplanth2020
  2. A virological approach to biocontrol Botrytis cinerea, a significant plant pathogenic fungus also relevant to human health. 2018-2021. PI: M.A. Ayllón
  3. Origen y evolución de micovirus. Proyecto Explora Ciencia-MINECO (AGL2014-62178-EXP), 2015-2018. PI: M.A. Ayllón
  4. Interacción virus-hongo-planta: virus de Botrytis cinerea, mecanismos de patogénesis y silenciamiento del RNA. MICINN (AGL2009-11778), 2010-2013. PI: M.A. Ayllón

 


Representative Publications

Wagemans, J., Holtappels, D., Vainio, E., Rabiey, M., Marzachì, C., Herrero, S., Ravanbakhsh, M., Tebbe, C.C., Ogliastro, M., Ayllón, M.A., Turina, M. 2022. Going Viral: Virus-Based Biological Control Agents for Plant Protection. Annual Review of Phytopathology 60, 21–42. DOI: 10.1146/annurev-phyto-021621-114208


Jiāng, D., Ayllón, M.A., Marzano, S.-Y.L., Kondō, H., Turina, M., ICTV Report ConsortiumYR 2022 2022. ICTV Virus Taxonomy Profile: Mymonaviridae 2022. Journal of General Virology 103, 001787. DOI: 10.1099/jgv.0.001787


Forgia, M., Chiapello, M., Daghino, S., Pacifico, D., Crucitti, D., Oliva, D., Ayllon, M., Turina, M., Turina, M. 2022. Three new clades of putative viral RNA-dependent RNA polymerases with rare or unique catalytic triads discovered in libraries of ORFans from powdery mildews and the yeast of oenological interest Starmerella bacillaris. Virus Evolution 8, veac038. DOI: 10.1093/ve/veac038


Galán-Cubero, R., Córdoba, L., Rodríguez-Romero, J., Chiapello, M., Turina, M., Ayllón, M.A. 2022. Molecular Data of a Novel Penoulivirus Associated with the Plant-Pathogenic Fungus Erysiphe necator. Phytopathology® PHYTO-12-21-0536-A. DOI: 10.1094/PHYTO-12-21-0536-A


Córdoba, L., Ruiz-Padilla, A., Rodríguez-Romero, J., Ayllón, M.A. 2022. Construction and Characterization of a Botrytis Virus F Infectious Clone. Journal of Fungi 8, 459. DOI: 10.3390/jof8050459


Kuhn, J.H., Adkins, S., Agwanda, B.R., Al Kubrusli, R., Alkhovsky, S.V., Amarasinghe, G.K., Avšič-Županc, T., Ayllón, M.A. 2021. Correction to: 2021 Taxonomic update of phylum Negarnaviricota (Riboviria: Orthornavirae), including the large orders Bunyavirales and Mononegavirales. Archives of Virology 166, 3567–3579. DOI: 10.1007/s00705-021-05266-w


Kuhn, J.H., Adkins, S., Agwanda, B.R., Al Kubrusli, R., Alkhovsky, S.V., Amarasinghe, G.K., Avšič-Županc, T., Ayllón, M.A. 2021. 2021 Taxonomic update of phylum Negarnaviricota (Riboviria: Orthornavirae), including the large orders Bunyavirales and Mononegavirales. Archives of Virology 166, 3513–3566. DOI: 10.1007/s00705-021-05143-6


Ruiz-Padilla, A., Rodríguez-Romero, J., Gómez-Cid, I., Pacifico, D., Ayllón, M.A. 2021. Novel Mycoviruses Discovered in the Mycovirome of a Necrotrophic Fungus. mBio 12. DOI: 10.1128/mBio.03705-20


Chiapello, M., Rodríguez-Romero, J., Ayllón, M.A., Turina, M. 2020. Analysis of the virome associated to grapevine downy mildew lesions reveals new mycovirus lineages. Virus Evolution 6. DOI: 10.1093/ve/veaa058


Kuhn, J.H., Adkins, S., Alioto, D., Alkhovsky, S.V., Amarasinghe, G.K., Anthony, S.J., Avšič-Županc, T., Ayllón, M.A., Bahl, J., Balkema-Buschmann, A., Ballinger, M.J., Bartonička, T., Basler, C., Bavari, S., Beer, M., Bente, D.A., Bergeron, É., Bird, B.H., Blair, C., Blasdell, K.R., Bradfute, S.B., Breyta, R., Briese, T., Brown, P.A., Buchholz, U.J., Buchmeier, M.J., Bukreyev, A., Burt, F., Buzkan, N., Calisher, C.H., Cao, M., Casas, I., Chamberlain, J., Chandran, K., Charrel, R.N., Chen, B., Chiumenti, M., Choi, I.-R., Clegg, J.C.S., Crozier, I., da Graça, J.V., Dal Bó, E., Dávila, A.M.R., de la Torre, J.C., de Lamballerie, X., de Swart, R.L., Di Bello, P.L., Di Paola, N., Di Serio, F., Dietzgen, R.G., Digiaro, M., Dolja, V.V., Dolnik, O., Drebot, M.A., Drexler, J.F., Dürrwald, R., Dufkova, L., Dundon, W.G., Duprex, W.P., Dye, J.M., Easton, A.J., Ebihara, H., Elbeaino, T., Ergünay, K., Fernandes, J., Fooks, A.R., Formenty, P.B.H., Forth, L.F., Fouchier, R.A.M., Freitas-Astúa, J., Gago-Zachert, S., Gāo, G.F., García, M.L., García-Sastre, A., Garrison, A.R., Gbakima, A., Goldstein, T., Gonzalez, J.-P.J., Griffiths, A., Groschup, M.H., Günther, S., Guterres, A., Hall, R.A., Hammond, J., Hassan, M., Hepojoki, J., Hepojoki, S., Hetzel, U., Hewson, R., Hoffmann, B., Hongo, S., Höper, D., Horie, M., Hughes, H.R., Hyndman, T.H., Jambai, A., Jardim, R., Jiāng, D., Jin, Q., Jonson, G.B., Junglen, S., Karadağ, S., Keller, K.E., Klempa, B., Klingström, J., Kobinger, G., Kondō, H., Koonin, E.V., Krupovic, M., Kurath, G., Kuzmin, I.V., Laenen, L., Lamb, R.A., Lambert, A.J., Langevin, S.L., Lee, B., Lemos, E.R.S., Leroy, E.M., Li, D., Lǐ, J., Liang, M., Liú, W., Liú, Y., Lukashevich, I.S., Maes, P., Marciel de Souza, W., Marklewitz, M., Marshall, S.H., Martelli, G.P., Martin, R.R., Marzano, S.-Y.L., Massart, S., McCauley, J.W., Mielke-Ehret, N., Minafra, A., Minutolo, M., Mirazimi, A., Mühlbach, H.-P., Mühlberger, E., Naidu, R., Natsuaki, T., Navarro, B., Navarro, J.A., Netesov, S.V., Neumann, G., Nowotny, N., Nunes, M.R.T., Nylund, A., Økland, A.L., Oliveira, R.C., Palacios, G., Pallas, V., Pályi, B., Papa, A., Parrish, C.R., Pauvolid-Corrêa, A., Pawęska, J.T., Payne, S., Pérez, D.R., Pfaff, F., Radoshitzky, S.R., Rahman, A., Ramos-González, P.L., Resende, R.O., Reyes, C.A., Rima, B.K., Romanowski, V., Robles Luna, G., Rota, P., Rubbenstroth, D., Runstadler, J.A., Ruzek, D., Sabanadzovic, S., Salát, J., Sall, A.A., Salvato, M.S., Sarpkaya, K., Sasaya, T., Schwemmle, M., Shabbir, M.Z., Shí, X., Shí, Z., Shirako, Y., Simmonds, P., Širmarová, J., Sironi, M., Smither, S., Smura, T., Song, J.-W., Spann, K.M., Spengler, J.R., Stenglein, M.D., Stone, D.M., Straková, P., Takada, A., Tesh, R.B., Thornburg, N.J., Tomonaga, K., Tordo, N., Towner, J.S., Turina, M., Tzanetakis, I., Ulrich, R.G., Vaira, A.M., van den Hoogen, B., Varsani, A., Vasilakis, N., Verbeek, M., Wahl, V., Walker, P.J., Wang, H., Wang, J., Wang, X., Wang, L.-F., Wèi, T., Wells, H., Whitfield, A.E., Williams, J.V., Wolf, Y.I., Wú, Z., Yang, X., Yáng, X., Yu, X., Yutin, N., Zerbini, F.M., Zhang, T., Zhang, Y.-Z., Zhou, G., Zhou, X. 2020. 2020 taxonomic update for phylum Negarnaviricota (Riboviria: Orthornavirae), including the large orders Bunyavirales and Mononegavirales. Archives of Virology. DOI: 10.1007/s00705-020-04731-2


Ayllón, M.A., Turina, M., Xie, J., Nerva, L., Marzano, S.-Y.L., Donaire, L., Jiang, D., Consortium, I.R. 2020. ICTV Virus Taxonomy Profile: Botourmiaviridae. Journal of General Virology. DOI: 10.1099/jgv.0.001409


Chiapello, M., Rodríguez‐Romero, J., Nerva, L., Forgia, M., Chitarra, W., Ayllón, M.A., Turina, M. 2020. Putative new plant viruses associated with Plasmopara viticola-infected grapevine samples. Annals of Applied Biology. DOI: 10.1111/aab.12563


Jiāng (姜道宏), D., Ayllón, M.A., Marzano, S.-Y.L., ICTV Report Consortium 2019. ICTV Virus Taxonomy Profile: Mymonaviridae. Journal of General Virology. DOI: 10.1099/jgv.0.001301


Amarasinghe, G.K., Ayllón, M.A., Bào, Y., Basler, C.F., Bavari, S., Blasdell, K.R., Briese, T., Brown, P.A., Bukreyev, A., Balkema-Buschmann, A., Buchholz, U.J., Chabi-Jesus, C., Chandran, K., Chiapponi, C., Crozier, I., de Swart, R.L., Dietzgen, R.G., Dolnik, O., Drexler, J.F., Dürrwald, R., Dundon, W.G., Duprex, W.P., Dye, J.M., Easton, A.J., Fooks, A.R., Formenty, P.B.H., Fouchier, R.A.M., Freitas-Astúa, J., Griffiths, A., Hewson, R., Horie, M., Hyndman, T.H., Jiāng, D., Kitajima, E.W., Kobinger, G.P., Kondō, H., Kurath, G., Kuzmin, I.V., Lamb, R.A., Lavazza, A., Lee, B., Lelli, D., Leroy, E.M., Lǐ, J., Maes, P., Marzano, S.-Y.L., Moreno, A., Mühlberger, E., Netesov, S.V., Nowotny, N., Nylund, A., Økland, A.L., Palacios, G., Pályi, B., Pawęska, J.T., Payne, S.L., Prosperi, A., Ramos-González, P.L., Rima, B.K., Rota, P., Rubbenstroth, D., Shī, M., Simmonds, P., Smither, S.J., Sozzi, E., Spann, K., Stenglein, M.D., Stone, D.M., Takada, A., Tesh, R.B., Tomonaga, K., Tordo, N., Towner, J.S., van den Hoogen, B., Vasilakis, N., Wahl, V., Walker, P.J., Wang, L.-F., Whitfield, A.E., Williams, J.V., Zerbini, F.M., Zhāng, T., Zhang, Y.-Z., Kuhn, J.H. 2019. Taxonomy of the order Mononegavirales: update 2019. Archives of Virology. DOI: 10.1007/s00705-019-04247-4


Maes, P., Amarasinghe, G.K., Ayllón, M.A., Basler, C.F., Bavari, S., Blasdell, K.R., Briese, T., Brown, P.A., Bukreyev, A., Balkema-Buschmann, A., Buchholz, U.J., Chandran, K., Crozier, I., de Swart, R.L., Dietzgen, R.G., Dolnik, O., Domier, L.L., Drexler, J.F., Dürrwald, R., Dundon, W.G., Duprex, W.P., Dye, J.M., Easton, A.J., Fooks, A.R., Formenty, P.B.H., Fouchier, R.A.M., Freitas-Astúa, J., Ghedin, E., Griffiths, A., Hewson, R., Horie, M., Hurwitz, J.L., Hyndman, T.H., Jiāng, D., Kobinger, G.P., Kondō, H., Kurath, G., Kuzmin, I.V., Lamb, R.A., Lee, B., Leroy, E.M., Lǐ, J., Marzano, S.-Y.L., Mühlberger, E., Netesov, S.V., Nowotny, N., Palacios, G., Pályi, B., Pawęska, J.T., Payne, S.L., Rima, B.K., Rota, P., Rubbenstroth, D., Simmonds, P., Smither, S.J., Song, Q., Song, T., Spann, K., Stenglein, M.D., Stone, D.M., Takada, A., Tesh, R.B., Tomonaga, K., Tordo, N., Towner, J.S., van den Hoogen, B., Vasilakis, N., Wahl, V., Walker, P.J., Wang, D., Wang, L.-F., Whitfield, A.E., Williams, J.V., Yè, G., Zerbini, F.M., Zhang, Y.-Z., Kuhn, J.H. 2019. Taxonomy of the order Mononegavirales: second update 2018. Archives of Virology. DOI: 10.1007/s00705-018-04126-4


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".


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".


Illana, A; Marconi, M; Rodríguez-Romero, J; Xu, P; Dalmay, T; Wilkinson, MD; Ayllón, MÁ; Sesma, A. 2017. "Molecular characterization of a novel ssRNA ourmia-like virus from the rice blast fungus Magnaporthe oryzae". Archives of Virology. DOI: 10.1007/s00705-016-3144-9".


Donaire, L; Ayllón, MA. 2017. "Deep sequencing of mycovirus-derived small RNAs from Botrytis species". Molecular Plant Pathology. 18(8): 1127-1137. DOI: 10.1111/mpp.12466".


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".


Donaire, L; Rozas, J; Ayllón, MA. 2016. "Molecular characterization of Botrytis ourmia-like virus, a mycovirus close to the plant pathogenic genus Ourmiavirus". Virology. DOI: 10.1016/j.virol.2015.11.027".


Rodríguez-García, C; Medina, V; Alonso, A; Ayllón, MA. 2014. "Mycoviruses of Botrytis cinerea isolates from different hosts". Annals of Applied Biology. DOI: 10.1111/aab.12073".


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".