Abstract
Plant infections caused by fungi are often associated with an increase in the pH of the surrounding host tissue1. Extracellular alkalinization is thought to contribute to fungal pathogenesis, but the underlying mechanisms are poorly understood. Here, we show that the root-infecting fungus Fusarium oxysporum uses a functional homologue of the plant regulatory peptide RALF (rapid alkalinization factor)2,3 to induce alkalinization and cause disease in plants. An upshift in extracellular pH promotes infectious growth of Fusarium by stimulating phosphorylation of a conserved mitogen-activated protein kinase essential for pathogenicity4,5. Fungal mutants lacking a functional Fusarium (F)-RALF peptide failed to induce host alkalinization and showed markedly reduced virulence in tomato plants, while eliciting a strong host immune response. Arabidopsis plants lacking the receptor-like kinase FERONIA, which mediates the RALF-triggered alkalinization response6, displayed enhanced resistance against Fusarium. RALF homologues are found across a number of phylogenetically distant groups of fungi, many of which infect plants. We propose that fungal pathogens use functional homologues of alkalinizing peptides found in their host plants to increase their infectious potential and suppress host immunity.
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Acknowledgements
The authors thank E. Martínez Aguilera for technical assistance and A. Ramiro for help with Arabidopsis experiments. This work was supported by grant no. BIO2013-47870-R from the Spanish Ministerio de Innovación y Competitividad (MINECO) to A.D.P. S.M. has received an undergraduate student fellowship from MINECO. D.S. was supported by project BIO2008-04479 from MINECO/ERA-NET PathoGenoMics. M.L.R. was supported by project BIO296 from the Junta de Andalucia. M.E.G. was supported by a Marie Curie Initial Training Network (ITN) ARIADNE (FP7-PEOPLE-ITN-237936) grant from the European Commission. U.F. was supported by the German Federal Ministry of Education and Research–Knowledge-Based Bio-Economy in Europe (BMBF–KBBE) project 031A328 and G.F. was funded by the Deutsche Forschungsgemeinschaft through CRC 1101.
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A.D.P., D.T., T.A.R. and G.F. designed the experiments. S.M., D.S., D.T., M.L.R., U.F., M.E.G., G.L. and T.A.R. carried out the experiments and analysed the data. A.D.P., G.F. and T.A.R. wrote the manuscript.
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Supplementary Figures 1–8 and Supplementary Table 3. (PDF 9961 kb)
Supplementary Table 1
Genomes searched (XLSX 34 kb)
Supplementary Table 2
Results of JackHMMEr searches (XLS 267 kb)
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Masachis, S., Segorbe, D., Turrà, D. et al. A fungal pathogen secretes plant alkalinizing peptides to increase infection. Nat Microbiol 1, 16043 (2016). https://doi.org/10.1038/nmicrobiol.2016.43
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DOI: https://doi.org/10.1038/nmicrobiol.2016.43
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