MOLECULAR MECHANISMS OF VIRULENCE OF FUNGAL WHEAT PATHOGENS
- Álvarez Aragón, Rocío - Postdoctoral Fellow
- De Francesco, Agustina - Postdoctoral María Zambrano
- Maestre Guillen, Alejandro - Technician
- Oberti Rivarola, Héctor - Student
- Ostermann, Cécile - Student
- Praz, Coraline - Otros postdoctorales de programas oficiales
- Suárez Fernández, Marta - Postdoctoral Margarita Salas
- Tirado Conejo, Rocío - Technician
Fungal pathogens, such as Zymoseptoria tritici, the causal agent of Septoria tritici blotch in wheat, have an intimate interaction with their hosts. Not only do they have to acquire nutrients from them, but they also have to protect themselves against the host immune system. The molecular mechanisms by which plant pathogenic fungi infect their hosts have been studied for years. However, the molecular components that determine specificity between the plant and the host remain enigmatic. In our group, we are interested in analyzing the molecular mechanisms by which Z. tritici infects host plants. Specifically, we are interested in analyzing how this fungal pathogen is able to cope with the host immune system and how it eventually kills the cells. The aim of my research is to gain knowledge into the molecular basis of infection of Z. tritici.
Z. tritici pathogenicity
Z. triticiis a highly specialized pathogen that only infects wheat and no other plants. In this project, we aim to understand the molecular mechanisms by which Z. tritici infects wheat and adapt to its host. One of our main goals is to identify the key molecular components involved in the interaction between both microorganisms by using population genetics approaches. We recently identified a new avirulence factor which is specifically recognized by certain wheat cultivars hindering the infection progression. The gene is highly polymorphic and specifically expressed during host colonization. To understand the molecular basis of recognition and the molecular targets of effectors, we functionally characterize candidate genes and perform biochemical analyses.
Figure 1: leaves of the wheat cultivar Runal spray‐infected with Zymoseptoria tritici strains 3D1 and 3D7 and harvested at different days post‐inoculation (dpi). (b) Fully necrotised leaves with pycnidia of cv Runal infected by 3D1 and 3D7 at 21 dpi.
Chromatin remodeling and expression of effector genes
Tight gene expression regulation of virulence factors is required for successful colonization of the host. Although it is frequently assumed that chromatin remodeling is required for induction of expression of effectors, we still do not understand the molecular components involved in this process. We recently demonstrated that host-triggered chromatin remodeling is involved in cell-specific expression profiles of effector genes (Meile et al. 2018). In this project, we aim to elucidate how stress related genes are activated during infection and what is the contribution of chromatin remodeling in gene expression regulation.
Figure 2: The effector gene AvrStb6 is silenced under axenic conditions and on hyphae growing on the leaf surface, but de-repressed during apoplast colonization. Fluorescence of mCherry and mTurquoise2 of Z. tritici strain 3D7 during infection of wheat leaves. His1-mCherry fusion protein is under the control of the AvrStb6 promoter and mTurquoise2 under the control of the constitutive α-tubulin promoter.
Identification of new sources of broad-spectrum resistance to septoria tritici blotch and leaf rust in durum wheat
Wheat is the third-most produced global cereal and is grown on more land than any other crop in the world. Durum wheat (Triticum turgidum spp. durum) production is concentrated in the Mediterranean Basin and in Spain, the production reaches 1 million tonnes. Durum wheat production is highly affected by several diseases and the two most problematic ones are septoria tritici blotch, caused by Zymoseptoria tritici, and leaf rust caused by several species of the genus Puccinia, including Puccinia triticina, the fungus causing the wheat leaf rust disease. The genetics of septoria tritici blotch and rust resistance in durum wheat is poorly understood and only a few resistance genes have been associated with markers, which hinders breeding of durum wheat resistant cultivars. In this project we aim to optimize the use of durum wheat genetic resources and design new prediction models to anticipate disease outbreaks, thereby providing sustainable control methods against two of the most damaging wheat pathogens in the world (Zymoseptoria tritici and Puccinia triticina) and against potential future diseases.
The role of plant cell wall in plant-microbe interactions
Plant cell walls are dynamic barriers that pathogens must overcome for within-host colonization and between-host transmission. Alterations of the plant cell wall integrity (CWI) during pathogen colonization (e.g. by the activity of Cell Wall Degrading Enzymes (CWDEs) secreted by pathogens) result in the release of wall-derived glycans, which can potentially be perceived by pathogens to activate virulence mechanisms for colonization and by the host to induce a resistance response. In the frame of this project, we will investigate how the balance between glycan perception by plants and pathogens contribute to the infection outcome. This proposal aims to identify plant CWI alterations and cell wall derived glycans released during plant-pathogen interactions to further characterize the molecular bases of glycan perception by plants/pathogens and their impact in balancing microbial colonization/transmission.
Dialogue between strains in genetically diverse infections
Natural infections are often caused by mixtures of genetically different pathogen strains (mixed-infections). Most research projects aim to understand the interactions of individual hosts with single pathogen strains. In mixed infections, pathogens not only have to overcome the host resistance response, but they also have to compete with other pathogenic strains to achieve successful infection. Mixed infections have strong consequences for the progress of the infection, for the evolution of virulence and for the epidemiology. Until now, the molecular components involved in interactions between co-infecting strains remain to be elucidated, but effectors have been proposed to be involved. The aim of this research project is to gain understanding of the molecular components involved in the interaction between fungal strains and the impact of the host on the outcome of mixed infections.
REGULACION EPIGENETICA DE GENES EFECTORES DE HONGOS PATOGENOS DE PLANTAS. Ministerio de Ciencia e Innovación. Proyectos de I+D+i, Programa Estatal de Generación de Conocimiento y Fortalecimiento Científico y Tecnológico del Sistema de I+D+i y del Programa Estatal de I+D+i Orientada a los Retos de la Sociedad, del Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020. Proyecto PID2019-108693RA-I00 financiado por AEI/10.13039/501100011033
IDENTIFICACIÓN DE NUEVAS FUENTES DE RESISTENCIA HORIZONTAL A SEPTORIA Y ROYA EN TRIGO DURO. Ministerio de Ciencia e Innovación. Proyecto de Líneas Estratégicas de la Colaboración Público-Privada (2021). Plan de Recuperación, Transformación y Resiliencia. Proyecto PLEC2021-007930 financiado por MCIN/ AEI/10.13039/501100011033/ y la Unión Europea “NextGenerationEU”/PRTR.
WALLADAPT (Deciphering the function of plant cell wall integrity and wall derived glycans in plant-microbe interactions for enhancing sustainable crop disease resistance). EoI-MCBGP21 Code: PLANTADAPT_03_WALLADAPT. Programa Severo Ochoa. Ayuda CEX2020-000999-S financiada por MCIN/AEI /10.13039/501100011033
DES OUTLIS MOLÉCULAIRES POUR LA SÉLECTION DE RÉSISTANCES DIVERSIFIÉES et EFFICACES CONTRE LA SEPTORIOSE DU BLÉ (DivR). Fonds de Soutien à l’Obtention Végétale (FSOV)
Cadot, S., Gfeller, V., Hu, L., Singh, N., Sánchez-Vallet, A., Glauser, G., Croll, D., Erb, M., van der Heijden, M.G.A., Schlaeppi, K. 2021. Soil composition and plant genotype determine benzoxazinoid-mediated plant–soil feedbacks in cereals. Plant, Cell & Environment. DOI: 10.1111/pce.14184
Barrett, L.G., Zala, M., Mikaberidze, A., Alassimone, J., Ahmad, M., McDonald, B.A., Sánchez‐Vallet, A. 2021. Mixed infections alter transmission potential in a fungal plant pathogen. Environmental Microbiology. DOI: https://doi.org/10.1111/1462-2920.15417
Rebaque, D., Hierro, I. del, López, G., Bacete, L., Vilaplana, F., Dallabernardina, P., Pfrengle, F., Jordá, L., Sánchez‐Vallet, A., Pérez, R., Brunner, F., Molina, A., Mélida, H. 2021. Cell wall-derived mixed-linked β-1,3/1,4-glucans trigger immune responses and disease resistance in plants. The Plant Journal. DOI: https://doi.org/10.1111/tpj.15185
Meile, L., Peter, J., Puccetti, G., Alassimone, J., McDonald, B.A., Sánchez-Vallet, A. 2020. Chromatin Dynamics Contribute to the Spatiotemporal Expression Pattern of Virulence Genes in a Fungal Plant Pathogen. mBio 11. DOI: 10.1128/mBio.02343-20
Sánchez-Vallet, A., Tian, H., Rodriguez-Moreno, L., Valkenburg, D.-J., Saleem-Batcha, R., Wawra, S., Kombrink, A., Verhage, L., Jonge, R. de, Esse, H.P. van, Zuccaro, A., Croll, D., Mesters, J.R., Thomma, B.P.H.J. 2020. A secreted LysM effector protects fungal hyphae through chitin-dependent homodimer polymerization. PLOS Pathogens 16, e1008652. DOI: 10.1371/journal.ppat.1008652
Poretti, M., Praz, C.R., Meile, L., Kälin, C., Schaefer, L.K., Schläfli, M., Widrig, V., Sanchez-Vallet, A., Wicker, T., Bourras, S. 2020. Domestication of High-Copy Transposons Underlays the Wheat Small RNA Response to an Obligate Pathogen. Molecular Biology and Evolution 37, 839–848. DOI: 10.1093/molbev/msz272
Sánchez-Vallet, A., Tian, H., Rodriguez-Moreno, L., Valkenburg, D.-J., Saleem-Batcha, R., Wawra, S., Kombrink, A., Verhage, L., Jonge, R. de, Esse, H.P. van, Zuccaro, A., Croll, D., Mesters, J.R., Thomma, B.P.H.J. 2019. A secreted LysM effector protects fungal hyphae through chitin-dependent homodimer polymerization. bioRxiv 787820. DOI: 10.1101/787820
Fiorin, G.L., Sanchéz-Vallet, A., Thomazella, D.P. de T., do Prado, P.F.V., do Nascimento, L.C., Figueira, A.V. de O., Thomma, B.P.H.J., Pereira, G.A.G., Teixeira, P.J.P.L. 2018. Suppression of Plant Immunity by Fungal Chitinase-like Effectors. Current Biology 28, 3023-3030.e5. DOI: 10.1016/j.cub.2018.07.055
Krishnan, P., Meile, L., Plissonneau, C., Ma, X., Hartmann, F.E., Croll, D., McDonald, B.A., Sánchez-Vallet, A. 2018. Transposable element insertions shape gene regulation and melanin production in a fungal pathogen of wheat. BMC Biology 16, 78. DOI: 10.1186/s12915-018-0543-2
Meile, L., Croll, D., Brunner, P.C., Plissonneau, C., Hartmann, F.E., McDonald, B.A., Sánchez‐Vallet, A. 2018. A fungal avirulence factor encoded in a highly plastic genomic region triggers partial resistance to septoria tritici blotch. New Phytologist 219, 1048–1061. DOI: 10.1111/nph.15180
Sánchez-Vallet, A., Fouché, S., Fudal, I., Hartmann, F.E., Soyer, J.L., Tellier, A., Croll, D. 2018. The Genome Biology of Effector Gene Evolution in Filamentous Plant Pathogens. Annual Review of Phytopathology 56, 21–40. DOI: 10.1146/annurev-phyto-080516-035303
Piślewska-Bednarek, M., Nakano, R.T., Hiruma, K., Pastorczyk, M., Sanchez-Vallet, A., Singkaravanit-Ogawa, S., Ciesiołka, D., Takano, Y., Molina, A., Schulze-Lefert, P., Bednarek, P. 2018. Glutathione Transferase U13 Functions in Pathogen-Triggered Glucosinolate Metabolism. Plant Physiology 176, 538–551. DOI: 10.1104/pp.17.01455
Sánchez‐Vallet, A., Hartmann, F.E., Marcel, T.C., Croll, D. 2017. Nature’s genetic screens: using genome‐wide association studies for effector discovery. Molecular Plant Pathology 19, 3–6. DOI: 10.1111/mpp.12592
Hartmann, F.E., Sánchez-Vallet, A., McDonald, B.A., Croll, D. 2017. A fungal wheat pathogen evolved host specialization by extensive chromosomal rearrangements. The ISME Journal 11, 1189–1204. DOI: 10.1038/ismej.2016.196
Sánchez-Vallet, A., Mesters, J.R., Thomma, B.P.H.J. 2015. The battle for chitin recognition in plant-microbe interactions. FEMS Microbiology Reviews 39, 171–183. DOI: 10.1093/femsre/fuu003
Sánchez-Vallet, A., Saleem-Batcha, R., Kombrink, A., Hansen, G., Valkenburg, D.-J., Thomma, B.P., Mesters, J.R. 2013. Fungal effector Ecp6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization. eLife 2, e00790. DOI: 10.7554/eLife.00790