Molecular mechanisms of virulence of fungal wheat pathogens
- Olmo Montoro, Iván del - Postdoctoral Fellow
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 still 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.
1. Z. tritici pathogenicity
Z. tritici is 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.
2. 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. 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.
3. 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, 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.
Figure 3: Co-infecting hyphae of different strains co-exist in wheat. Confocal microscopy analysis of cultivar Drifter infected with one strain of Z. tritici expressing cytosolic eGFP and the other strain expressing cytosolic mCherry.
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