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A fungal pathogen secretes plant alkalinizing peptides to increase infection

Nature Microbiology volume 1, Article number: 16043 (2016) Cite this article

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A Corrigendum to this article was published on 09 May 2016

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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Figure 1: High extracellular pH promotes invasive growth, plant infection and phosphorylation of the pathogenicity-associated MAPK Fmk1 in F. oxysporum.
Figure 2: Fusarium oxysporum encodes a functional RALF peptide.
Figure 3: F-RALF promotes fungal virulence and suppresses plant immune responses.
Figure 4: F-RALF targets the plant RLK FERONIA.

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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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Author notes

  1. Sara Masachis and David Segorbe: †These authors contributed equally to this work.

Authors and Affiliations

  1. Departamento de Genética, Campus de Excelencia Internacional Agroalimentario ceiA3, Universidad de Córdoba, Córdoba, Spain

    Sara Masachis, David Segorbe, David Turrà, Mercedes Leon-Ruiz, Mennat El Ghalid, Manuel S. López-Berges & Antonio Di Pietro

  2. Zentrum für Molekularbiologie der Pflanzen, University Tübingen, 72076 Tübingen, Germany

    Ursula Fürst & Georg Felix

  3. Biosciences, University of Exeter, Exeter, EX4 4QD, UK

    Guy Leonard & Thomas A. Richards

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Contributions

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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Correspondence to Antonio Di Pietro.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

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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