ECOLOGICAL AND MOLECULAR FACTORS INVOLVED IN FUNGAL ENDOPHYTISM AND PATHOGENESIS

Group leader: María Soledad Sacristán Benayas - Associate Professor
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Personnel:

 

Fungal endophytes (FEs) are a diverse group of fungi that colonize internal plant tissues without causing disease symptoms. Many FEs are beneficial to the plant, with functions such as plant growth promotion (PGP) or the increase of plant tolerance to biotic and abiotic stresses. Thus, FEs are promising tools to develop novel microbial biostimulants. However, some of the FEs are related to pathogens and may behave as such under certain circumstances that can involve environmental factors or genetic host-fungal determinants.

 

There is a great lack of studies that explain how do FEs really interact with the plant. For an optimal and reliable application of these promising tools, it is essential to attain a good understanding of the mechanisms that govern their interaction with the plant, the conditions that maximize or reduce the benefit, the plant and fungal genes that optimize the outcome, or the molecules that could determine it. A deep knowledge of the principles that regulate the endophytic lifestyle can also provide clues for better understanding both mutualism and pathogenesis, and to identify common points and switches between both extremes that can be used for a better disease management.

 

The aims of our group are

  1. to study the environmental and molecular factors that affect fungal endophytism and its relationship with mutualistic and pathogenic interactions with the plant.
  2. to achieve the application of FEs and derived molecules to increase crop yield.


For that, we use as model of study the FEs of natural populations of the model plant Arabidopsis thaliana. During several years of surveys in ecologically distinct populations at Central Spain, we have isolated a high diverse number of fungal species from asymptomatic Arabidopsis plants, gathering a collection of more than 400 endophytic isolates (Figure 1. García et al., 2013). This was a pioneer work that described, for the first time, the fungal endophytic assemblages of this model plant. The screening of our collection of FE in the interaction with Arabidopsis plants under different controlled conditions has yielded interesting model systems to generate and test new hypothesis, taking advantage of the molecular tools and the abundant knowledge accessible from the host plant.




Figure 1. Fungal endophytes naturally infecting A. thaliana. A. Endophytic intercellular mycelium in an Arabidopsis leaf from a wild population. B. Emerging mycelium from a sillique after incubation in a humid chamber.

 


An important milestone of these analyses has been the discovering of the mutualistic interaction between Colletotrichum tofieldiae (Ct) and A. thaliana. We showed that Ct increases seed production of Arabidopsis plants (Priority Spanish Patent n. P201331839; International PCT application PCT/ES2014/070930; Divisional Application n. 2018274842). Further analysis carried out in collaboration with of Paul Schulze-Lefert (Max Planck Institute of Plant Breeding Research, Germany), showed that root infection by Ct promotes Arabidopsis shoot and root growth under phosphate (Pi) limiting conditions (Figure 2. Hiruma et al., 2016). Comparative genomics of Ct with related pathogens of the same genus indicated that the transition of Ct from parasitism to mutualism is relatively recent (Hacquard et al., 2016). Mutualistic behaviour was revealed by a narrowed repertoire of secreted effector proteins and a limited activation of pathogenicity-related genes in planta. Transcriptomic analyses indicated that beneficial responses are prioritized in Ct-colonized Arabidopsis roots under phosphate-deficient conditions, whereas plant defence responses were activated under phosphate sufficient conditions.



Figure 2. GFP labelled Colletotrichum tofieldiae hyphae penetrating PIP2A-mCherry-labeled Arabidopsis roots. Hiruma et al. (2016) Cell 165: 464–474

 


More recently, we have demonstrated the plant growth promotion of Ct on crops (tomato and maize, among others) (Figure 3, Díaz-González et al., 2020), expanding the possibilities of studying this fungal endophyte in very different hosts, and opening the door for its use in agriculture. We are currently deepening the understanding of the wide ability of Ct to interact with different hosts by an integrative approach including physiological, metabolic and transcriptomic data obtained under optimal and different stress conditions (AEI Project PID2021-123697OB-I00). In collaboration with Marcel Bucher from CEPLAS Cologne University., we are investigating the molecular exchange and feedback mechanisms of Ct in crops (SO EoI-CSPINT08-MOLEXBPI).



Figure 3. Representative image of maize (A) and tomato (B) seedlings from seeds inoculated with Ct or water for control and grown in MS medium for six days. Díaz-González et al. (2020) Agronomy 10: 1493.

 

 

We are also currently collaborating with the group of Carlos del Pozo at CBGP to study the role of other FE in plant adaptation to nutrient scarcity, heat and other stresses through changes in root physiology and development. For that, we are screening the FEs collection and have selected several beneficial isolates that are being further studied (SO projects EOI-TSP3-03 and μNUTRI-HEAT).

 

Extending our ultimate goal of achieving the application of FE and derived molecules to increase crop yield, we have got involved in the CBGP-TRADECORP Joint Research Unit BIOS4SUSTAIN, where we are working on the screening of our FE collection for positive interactors and further development as biostimulants. We are also involved in the project TED2021-130317B-I00, together with Antonio Molina and Carlos del Pozo groups, for the development of biosolutions for crop yield improvement derived from plant and fungal extracts.

 


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".