HOST ADAPTATION IN FUNGAL PLANT PATHOGENS

Group leader: Andrea Sánchez Vallet - Ramón y Cajal fellow
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Personnel:

 

Our vision

   Disease damage in crops leads to high yield reductions and challenges food security. Thus, the development of novel and durable strategies for crop protection is a fundamental task for plant pathologists and requires substantial advances in our understanding of plant pathosystems and pathogen evolution. Our group aims to determine the mechanisms enabling pathogens to adapt to their host.

  


Our approach

   Research in the group of Andrea Sanchez Vallet integrates population genomics, functional studies, greenhouse assays, and microbiology approaches. Our research focuses on diseases that challenge food production systems to provide applied tools to design novel and more environmentally friendly and durable control strategies. We use the model system wheat - Zymoseptoria tritici. This pathogen causes very high yield losses in all the production areas of wheat and has a very strong evolutionary potential.

   Our research focuses on deciphering the processes that underpin the colonization of fungi as pathogens on plant hosts. One of the first contacts between pathogens and plant cells is through the plant apoplast. The apoplast is not only a source of nutrients for colonizing organisms, but also a hostile environment where pathogens are recognized and where host antimicrobials counteract the progression of pathogens. Additionally, the apoplast accommodates endophytic microorganisms, which compete with pathogens for space and nutrients.

  Our research aims to investigate the dynamic processes that occur between plants and pathogens and to reveal the mechanisms by which pathogens adapt to their hosts at the molecular, evolutionary, and population levels.


Research lines

1- Nonhost resistance and pathogen adaptation

  The emergence of new diseases is a threat to food security. However, the mechanisms that determine pathogen adaptation to certain plant hosts remain elusive. Plants have a very robust immune response that prevents potential pathogens from colonizing a host. Nonhost resistance is defined as the resistance of a plant towards all the individuals of a pathogenic species. This type of resistance largely determines a pathogen’s host range and is the reason why pathogens cannot infect most potential hosts. The mechanisms mediating nonhost resistance remain largely unknown. Recent work of my research team has demonstrated that effector recognition is key for controlling infection of pathogenic and non-pathogenic species. In this project, we aim to decipher the contribution of effector-triggered immunity to nonhost resistance.

 

Figure 1. Avr3D1 homologs from Zymoseptoria ardabiliae and Zymoseptoria pseudotritici are recognized by wheat in a cultivar-dependent manner.

 

  

 2- Contribution of host microbiota to pathogen adaptation

The apoplast harbours a variety of endophytic microorganisms. Pathogens need to interfere with these endophytes to colonize a host. The mechanisms underlying intrahost competition between microorganisms and the contribution of resident microbiota to pathogen colonization remain largely unknown. We have recently generated a collection of 400 fungal endophytes from wheat plants and 300 strains of Z. tritici. We have demonstrated that around 15% of the isolated endophytes inhibit the growth of the pathogen. These results highlight the potential of fungal endophytes to prevent pathogen colonization. In this project, we aim to decipher the contribution of endophytes to pathogen adaptation and the mechanisms adopted by pathogens to interfere with fungal antagonists. With this aim, we combine population genomics approaches, microbiome analysis, transcriptomics, and functional characterization.

 

 

Figure 2. Transcriptome analysis of wheat indicates that the virulent strain of Zymoseptoria tritici controls avirulence factor-triggered plant resistance.

 

 

 

3- The role of plant cell wall in the dialogue between plants and pathogens

A very important component of the host apoplast with which plant pathogens tightly interact is the plant cell wall. It is a defensive barrier and a source of nutrients for pathogens. To break down the cell wall, pathogens employ a plethora of cell wall degrading enzymes, which hydrolyse plant cell wall polysaccharides. To counter this attack, plants can detect the derived cell wall degradation products and induce a resistance response that prevents pathogen progression. We hypothesize that pathogens have evolved to balance nutrient acquisition and prevent host recognition. We have recently identified several Z. tritici cell wall degrading enzymes that release oligosaccharides that are recognized by wheat and trigger an immune response that hinders Z. tritici infection. Remarkably, Z. tritici evolved to tightly regulate these enzymes to only be produced at late stages of the infection and, this way, prevent early recognition by the host. This project will aim to characterize these cell wall degrading enzymes and their contribution to infection and host evasion. We also aim to identify cell wall-derived oligosaccharides that trigger resistance in wheat that can potentially be used to control diseases in the fields.




Figure 3. Cell wall degrading enzymes (CWDEs) secreted by bacterial and fungal pathogens hydrolyse cell wall polysaccharides (e.g. cellulose in blue, hemicelluloses in orange and homogalacturonans (HG) in yellow) during host colonisation. This hydrolysis releases glycans that are used by pathogens as nutrients. Cell wall breakage creates chemotaxis gradients of oligosaccharides/monosaccharides that are perceived by chemoreceptors of bacterial pathogens to identify the entry points on the surface of plant cells. Some of the released glycans, can be perceived as Damage Associated Molecular Patterns (DAMPs) by the host Pattern Recognition Receptors (PRRs)

 


4- 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 are poorly understood and only a few resistance genes have been associated with markers, which hinders the 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 potential future diseases. This project is a collaboration with the Polytechnic University of Madrid, University of Seville, Agrovegetal S.L. and CSIC.

 

Funding

CHARACTERIZATION OF HISTONE DEMETHYLASES INVOLVED IN THE REGULATION OF FUNGAL PATHOGEN EFFECTOR GENES DURING WHEAT COLONIZATION. Ministerio de Ciencia e Innovación. PID2023-150977NB-I00, .

 

 

ROLE OF EFFECTOR RECOGNITION IN NONHOST RESISTANCE. MICIU/AEI /10.13039/ 501100011033 y por la Unión Europea NextGenerationEU/PRTR. . CNS2023-144037


 

 

DESIGN OF SUSTAINABLE BIOCONTROL STRATEGIES AGAINST SEPTORIA TRITICI BLOTCH OF WHEAT. Funded by MCIN/AEI /10.13039/501100011033 and European Union NextGenerationEU PRTR 2022. TED2021-132093B-I00

 

 

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)

 


Representative Publications

Oberti, H., Sessa, L., Oliveira-Rizzo, C., Di Paolo, A., Sanchez-Vallet, A., Seidl, M.F., Abreo, E. 2024. Novel genomic features in entomopathogenic fungus : accessory genomic regions and putative virulence genes involved in the infection process of soybean pest. Pest Management Science. DOI: 10.1002/ps.8631

Meile, L., Carrasco-López, C., Lorrain, C., Kema, G.H.J., Saintenac, C., Sanchez-Vallet, A. 2024. The molecular dialogue between Zymoseptoria tritici and wheat. Molecular Plant-Microbe Interactions®. DOI: 10.1094/MPMI-08-24-0091-IRW

Molina, A., Sánchez-Vallet, A., Jordá, L., Carrasco-López, C., Rodríguez-Herva, J.J., López-Solanilla, E. 2024. Plant cell walls: source of carbohydrate-based signals in plant-pathogen interactions. Current Opinion in Plant Biology 82, 102630. DOI: 10.1016/j.pbi.2024.102630

Fuertes-Rabanal, M., Largo-Gosens, A., Fischer, A., Munzert, K.S., Carrasco-López, C., Sánchez-Vallet, A., Engelsdorf, T., Mélida, H. 2024. Linear β-1,2-glucans trigger immune hallmarks and enhance disease resistance in plants. Journal of Experimental Botany erae368. DOI: 10.1093/jxb/erae368

Battache, M., Suarez-Fernandez, M., Klooster, M.V., Cambon, F., Sánchez-Vallet, A., Lebrun, M.-H., Langin, T., Saintenac, C. 2024. Stomatal penetration: the cornerstone of plant resistance to the fungal pathogen Zymoseptoria tritici. BMC Plant Biology 24, 736. DOI: 10.1186/s12870-024-05426-5

Alassimone, J., Praz, C., Lorrain, C., De Francesco, A., Carrasco-López, C., Faino, L., Shen, Z., Meile, L., Sánchez-Vallet, A. 2024. The Zymoseptoria tritici Avirulence Factor AvrStb6 Accumulates in Hyphae Close to Stomata and Triggers a Wheat Defense Response Hindering Fungal Penetration. Molecular Plant-Microbe Interactions® 37, 432–444. DOI: 10.1094/MPMI-11-23-0181-R

Yugueros, S.I., Peláez, J., Stajich, J.E., Fuertes-Rabanal, M., Sánchez-Vallet, A., Largo-Gosens, A., Mélida, H. 2024. Study of fungal cell wall evolution through its monosaccharide composition: An insight into fungal species interacting with plants. The Cell Surface 11, 100127. DOI: 10.1016/j.tcsw.2024.100127

Fernández-Calvo, P., López, G., Martín-Dacal, M., Aitouguinane, M., Carrasco-López, C., González-Bodí, S., Bacete, L., Mélida, H., Sánchez-Vallet, A., Molina, A. 2024. Leucine rich repeat-malectin receptor kinases IGP1/CORK1, IGP3 and IGP4 are required for arabidopsis immune responses triggered by β-1,4-D-Xylo-oligosaccharides from plant cell walls. The Cell Surface 11, 100124. DOI: 10.1016/j.tcsw.2024.100124

Amezrou, R., Ducasse, A., Compain, J., Lapalu, N., Pitarch, A., Dupont, L., Confais, J., Goyeau, H., Kema, G.H.J., Croll, D., Amselem, J., Sanchez-Vallet, A., Marcel, T.C. 2024. Quantitative pathogenicity and host adaptation in a fungal plant pathogen revealed by whole-genome sequencing. Nature Communications 15, 1933. DOI: 10.1038/s41467-024-46191-1

Bernasconi, A., Lorrain, C., Flury, P., Alassimone, J., McDonald, B.A., Sánchez-Vallet, A. 2023. Virulent strains of Zymoseptoria tritici suppress the host immune response and facilitate the success of avirulent strains in mixed infections. PLOS Pathogens 19, e1011767. DOI: 10.1371/journal.ppat.1011767

Suarez-Fernandez, M., Álvarez-Aragón, R., Pastor-Mediavilla, A., Maestre-Guillén, A., del Olmo, I., De Francesco, A., Meile, L., Sánchez-Vallet, A. 2023. Sas3-mediated histone acetylation regulates effector gene activation in a fungal plant pathogen. mBio e01386-23. DOI: 10.1128/mbio.01386-23

Meile, L., Garrido-Arandia, M., Bernasconi, Z., Peter, J., Schneller, A., Bernasconi, A., Alassimone, J., McDonald, B.A., Sánchez-Vallet, A. 2022. Natural variation in Avr3D1 from Zymoseptoria sp. contributes to quantitative gene-for-gene resistance and to host specificity. New Phytologist. DOI: 10.1111/nph.18690

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