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Metabolic priming by a secreted fungal effector

Nature volume 478, pages 395–398 (2011)Cite this article

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Abstract

Maize smut caused by the fungus Ustilago maydis is a widespread disease characterized by the development of large plant tumours. U. maydis is a biotrophic pathogen that requires living plant tissue for its development and establishes an intimate interaction zone between fungal hyphae and the plant plasma membrane. U. maydis actively suppresses plant defence responses by secreted protein effectors1,2. Its effector repertoire comprises at least 386 genes mostly encoding proteins of unknown function1,3,4 and expressed exclusively during the biotrophic stage3. The U. maydis secretome also contains about 150 proteins with probable roles in fungal nutrition, fungal cell wall modification and host penetration as well as proteins unlikely to act in the fungal-host interface4 like a chorismate mutase. Chorismate mutases are key enzymes of the shikimate pathway and catalyse the conversion of chorismate to prephenate, the precursor for tyrosine and phenylalanine synthesis. Root-knot nematodes inject a secreted chorismate mutase into plant cells likely to affect development5,6. Here we show that the chorismate mutase Cmu1 secreted by U. maydis is a virulence factor. The enzyme is taken up by plant cells, can spread to neighbouring cells and changes the metabolic status of these cells through metabolic priming. Secreted chorismate mutases are found in many plant-associated microbes and might serve as general tools for host manipulation.

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Figure 1: Cmu1 has chorismate mutase activity, affects virulence and salicylic acid levels.
Figure 2: Cmu1 is translocated to plant cells and spreads to neighbouring tissue.
Figure 3: Model of Cmu1-mediated metabolic priming in infected maize tissue.

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Acknowledgements

We are thankful to N. Amrhein and H.-U. Mösch for their comments on the manuscript. We thank B. Valent and C. H. Khang for alerting us to the fact that Magnaporthe grisea possesses a secreted chorismate mutase, and are grateful to M. Dickman for allowing us to cite his unpublished results. We thank T. Brefort, E. Mörschel, A. Kaever and M. Landesfeind for experimental support. We acknowledge advice by P. Kast, thank P. Schulze-Lefert for the Gateway-compatible plant transformation vectors, and D. Sicker for providing DIBOA and DIMBOA standards. We acknowledge technical assistance by R. Wissel, S. Löser, D. Vogel, F. Raths, G. Sowa, K. Bolte, M. Johannsen and P. Meyer. Our work was supported through DFG project DJ64/1-1, the collaborative research Center SFB593, and the LOEWE program of the State of Hesse.

Author information

Author notes

  1. Kerstin Schipper & Boris Macek

    Present address: Present addresses: Heinrich-Heine-Universität, Abteilung Mikrobiologie, Gebäude 26.12, Ebene 01, Universitätsstrasse 1, D-40225 Düsseldorf, Germany (K.S.); Proteome Center Tuebingen, Auf der Morgenstelle 15, D-72076 Tübingen, Germany (B.M.).,

  2. Armin Djamei and Kerstin Schipper: These authors contributed equally to this work.

Authors and Affiliations

  1. Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Straße 10, D-35043 Marburg, Germany

    Armin Djamei, Kerstin Schipper, Franziska Rabe, Anupama Ghosh, Volker Vincon, Jörg Kahnt & Regine Kahmann

  2. Zentrum Synthetische Mikrobiologie, Philipps-Universität Marburg, D-35032 Marburg, Germany

    Kerstin Schipper

  3. Max Planck Institute of Molecular Plant Physiology, Wissenschaftspark Golm, Am Mühlenberg 1, D-14476 Potsdam-Golm, Germany

    Sonia Osorio, Takayuki Tohge & Alisdair R. Fernie

  4. Georg-August-University, Albrecht-von-Haller Institute, Justus-von-Liebig Weg 11, D-37077 Göttingen, Germany

    Ivo Feussner

  5. Georg-August-University, Institute for Microbiology and Genetics, Grisebachstraße 8, D-37077 Göttingen, Germany

    Kirstin Feussner & Peter Meinicke

  6. Center for Plant Molecular Biology, University of Tübingen, Auf der Morgenstelle 5, D-72076 Tübingen, Germany

    York-Dieter Stierhof

  7. Max Planck Institute for Developmental Biology, Spemannstraße 35, D-72076 Tübingen, Germany

    Heinz Schwarz

  8. Max Planck Institute for Biochemistry, Am Klopferspitz 18, D-82152 Martinsried, Germany

    Boris Macek & Matthias Mann

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Contributions

A.D., K.S., F.R., V.V., J.K., S.O., T.T., K.F., P.M., Y.-D.S., H.S., A.G. and B.M. designed and performed the wet bench experiments. All authors contributed to data analysis. R.K., A.D. and K.S. wrote the manuscript with input from all co-authors. R.K. directed the project.

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Correspondence to Regine Kahmann.

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Supplementary information

Supplementary Information

This file contains Supplementary Figures 1- 24 with legends, Supplementary References and Supplementary Tables 1 and 3-8 (see separate file for Supplementary Table 2). (PDF 3189 kb)

Supplementary Table 2

This table shows the data matrix of 810 high quality marker candidates (ANOVA pVal<1x10-5) identified by metabolite fingerprinting by UPLC-ESI TOF-MS analysis in leaves of Zea maize 8 days post U. maydis infection. (XLS 632 kb)

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Djamei, A., Schipper, K., Rabe, F. et al. Metabolic priming by a secreted fungal effector. Nature 478, 395–398 (2011). https://doi.org/10.1038/nature10454

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