ECOLOGICAL AND MOLECULAR FACTORS INVOLVED IN FUNGAL ENDOPHYTISM AND PATHOGENESIS

Group leader: María Soledad Sacristán Benayas - Associate Professor
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Endophytes are fungi that grow inside the plant without causing apparent symptoms of disease. The vast majority of plants of natural ecosystems are colonized by endophytes, and this situation can be beneficial for the plant in many cases. However, some of the endophytic fungi are related to latent pathogens and saprotrophs that cause severe pre and post-harvest losses. The endophytic lifestyle of fungi is poorly characterized, particularly concerning the molecular interactions established during penetration, infection and colonization of plant tissues. A deep knowledge of the principles that regulate the endophytic lifestyle can provide clues for better understanding mutualism and pathogenesis and to identify common points and switches between both extremes that can be used for a better disease management.

 

The aim of this research line is to study the endophytes of natural populations of Arabidopsis thaliana in order to establish a model system to generate and test hypothesis about the general principles underlying the endophytic lifestyle. A. thaliana is the best studied plant model, so there is a large amount of available information about its functional genetics and genomics and a variety of tools to deepen in the knowledge of plant biology. Furthermore, A. thaliana is not just a lab model plant: the knowledge generated in the lab is being applied to the study of its wild populations, so it has become a model, as well, for the study of plant ecology, adaptation and evolution. The availability of endophytic isolates naturally infecting A. thaliana offers a great opportunity for an integral approach to better understand the principles of the endophytic lifestyle, taking advantage of the molecular tools and the abundant knowledge accessible from the host plant.


A. Endophytic intercellular mycelium in an Arabidopsis leaf from a wild population.

B. Emerging mycelium from a sillique after incubation in a humid chamber. 


During four years of surveys, we have isolated a high diverse number of fungal species from asymptomatic plants, gathering a collection of more than 1000 endophytic isolates (García et al., 2013). Isolates of the most abundant genera were chosen in order to test them on A. thaliana plants under controlled conditions and to investigate the outcome of the interactions. An important milestone of these analyses has been the discovering of the mutualistic interaction between Colletotrichum tofieldiae (Ct) and A. thaliana. We have shown that Ct increases seed production when applied to leaves of A. thaliana plants (Sacristán et al. 2014, Patent ES-2439393). The interaction between Ct and A. thaliana has been further characterized at the cellular and molecular level in collaboration with the research group of Paul Schulze-Lefert (Max Planck Institute of Plant Breeding Research, Germany), showing that root infection by Ct increases the growth of At roots and shoots under phosphate (P) limiting conditions (Hiruma et al., 2016). Comparative genomics of Ct with related pathogens of the same genus indicates that the transition of Ct from parasitism to mutualism is relatively recent (Hacquard et al., 2016). Mutualistic behaviour is revealed by a narrowed repertoire of secreted effector proteins and a limited activation of pathogenicity-related genes in planta. Transcriptomic analyses indicate that beneficial responses are prioritized in Ct-colonized A. thaliana roots under phosphate-deficient conditions, whereas defence responses are activated under phosphate sufficient conditions.


GFP labelled Colletotrichum tofieldiae hyphae penetrating PIP2A-mCherry-labeled A. thaliana roots. Hiruma et al. (2016) Cell 165: 464–474             


Further interesting endophytes isolated in our surveys are closely related to the species Plectosphaerella cucumerina. The species P. cucumerina is well known as a plant pathogenic fungus that naturally infects A. thaliana and has been deeply studied as model for necrotrophic interactions by the “Plant Innate Immunity and Resistance against Necrotrophic Fungi” group at the CBGP. Within this group, Soledad Sacristán is responsible of the phenotypic and genomic comparison of endophytic, pathogenic and non pathogenic isolates of P. cucumerina. This study will bring more information about the genomic and functional signatures that determine the endophytic or pathogenic lifestyles.

 


Representative Publications

Fiallo-Olivé, E., Palacio-Bielsa, A., Sacristán, S. 2023. Plant Pathogenic Microorganisms: State-of-the-Art Research in Spain. Microorganisms 11, 816. DOI: 10.3390/microorganisms11030816

Poveda, J., Baptista, P., Sacristán, S., Velasco, P. 2022. Editorial: Beneficial effects of fungal endophytes in major agricultural crops. Frontiers in Plant Science 13. DOI: 10.3389/fpls.2022.1061112

Poveda, J., Díaz-González, S., Díaz-Urbano, M., Velasco, P., Sacristán, S. 2022. Fungal endophytes of Brassicaceae: Molecular interactions and crop benefits. Frontiers in Plant Science 13. DOI: 10.3389/fpls.2022.932288

Sacristán, S., Goss, E.M., Eves-van den Akker, S. 2021. How Do Pathogens Evolve Novel Virulence Activities?. Molecular Plant-Microbe Interactions® MPMI-09-20-0258-IA. DOI: 10.1094/MPMI-09-20-0258-IA

Díaz-González, S., Marín, P., Sánchez, R., Arribas, C., Kruse, J., González-Melendi, P., Brunner, F., Sacristán, S. 2020. Mutualistic Fungal Endophyte Colletotrichum tofieldiae Ct0861 Colonizes and Increases Growth and Yield of Maize and Tomato Plants. Agronomy 10, 1493. DOI: 10.3390/agronomy10101493

Muñoz-Barrios, A., Sopeña-Torres, S., Ramos, B., López, G., Del Hierro García, I., Díaz-González, S., González-Melendi, P., Mélida, H., Fernández-Calleja, V., Mixão, V., Martín Dacal, M., Marcet-Houben, M., Gabaldón, T., Sacristan, S., Molina, A. 2020. Differential expression of fungal genes determines the lifestyle of Plectosphaerella strains during Arabidopsis thaliana colonization. Molecular Plant-Microbe Interactions®. DOI: 10.1094/MPMI-03-20-0057-R

Valverde, S., Vidiella, B., Montañez, R., Fraile, A., Sacristán, S., García-Arenal, F. 2020. Coexistence of nestedness and modularity in host–pathogen infection networks. Nature Ecology & Evolution. DOI: 10.1038/s41559-020-1130-9

Conesa, C.M., Saez, A., Navarro-Neila, S., de Lorenzo, L., Hunt, A.G., Sepúlveda, E.B., Baigorri, R., Garcia-Mina, J.M., Zamarreño, A.M., Sacristán, S., del Pozo, J.C. 2020. Alternative Polyadenylation and Salicylic Acid Modulate Root Responses to Low Nitrogen Availability. Plants 9, 251. DOI: 10.3390/plants9020251

McLeish, M., Sacristán, S., Fraile, A., Garcia-Arenal, F. 2018. Co-infection organises epidemiological networks of viruses and hosts and reveals hubs of transmission. Phytopathology. DOI: 10.1094/PHYTO-08-18-0293-R

McLeish, M; Sacristán, S; Fraile, A; García-Arenal, F. 2017. "Scale dependencies and generalism in host use shape virus prevalence". Proceedings of the Royal Society Biological Sciences Series B. DOI: 10.1098/rspb.2017.2066".

Hacquard, S; Kracher, B; Hiruma, K; Münch, PC; Garrido-Oter, R; Thon, MR; Weimann, A; Damm, U; Dallery, J-F; Hainaut, M; Henrissat, B; Lespinet, O; Sacristán, S; Ver Loren van Themaat, E; Kemen, E; McHardy, AC; Schulze-Lefert, P; O/'Connell, RJ. 2016. "Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi". Nature Communications. DOI: 10.1038/ncomms11362".

Hiruma, K; Gerlach, N; Sacristán, S; Nakano, Ryohei T; Hacquard, S; Kracher, B; Neumann, U; Ramírez, D; Bucher, M; O’Connell, Richard J; Schulze-Lefert, P. 2016. "Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent". Cell. DOI: 10.1016/j.cell.2016.02.028".

Amselem, J; Vigouroux, M; Oberhaensli, S; Brown, JK; Bindschedler, LV; Skamnioti, P; Wicker, T; Spanu, PD; Quesneville, H; Sacristan, S. 2015. "Evolution of the EKA family of powdery mildew avirulence-effector genes from the ORF 1 of a LINE retrotransposon". BMC Genomics. DOI: 10.1186/s12864-015-2185-x".

García, E; Alonso, Á; Platas, G; Sacristán, S. 2013. "The endophytic mycobiota of Arabidopsis thaliana". Fungal Diversity. DOI: 10.1007/s13225-012-0219-0".