The role of secreted Ustilago maydis proteins during pathogenesis.

Prof. Dr. Regine Kahmann

Max Planck Institute for Terrestrial Microbiology
Karl-von-Frisch-Strasse
D-35043 Marburg
Tel. +49-(0)6421-178-501
Fax +49-(0)6421-178-509
kahmann@mpi-marburg.mpg

Project description

The fungus Ustilago maydis elicits smut disease in corn. The most prominent symptoms of the disease are large plant tumors in which the fungus proliferates and differentiates into spores. U. maydis establishes a biotrophic relationship with its host, i.e. plant cells stay alive. This is accomplished by an invagination of the host plasma membrane which surrounds the infecting hyphae like a sheath. Recent experiments have revealed that pathogenic development of U. maydis is governed by a large number of secreted proteins of unknown function. Many of the genes for these protein-effectors are organized in gene clusters which are upregulated during pathogenesis. Mutants in which individual clusters were deleted showed virulence phenotypes ranging from hypervirulence, attenuated virulence to the complete loss of virulence. In this project we wish to determine which genes are responsible for the observed phenotypes, where the secreted proteins localize (apoplast or plant host, see Figure 1), how compartmentalisation is achieved and which function the respective effectors exert in their respective compartment. In addition, we want to study whether non-conventional secretion mechanisms contribute to the fungal proteome in the apoplast and how this relates to disease development.

Figure 1: Schematic view of the early U. maydis infection process. The dikaryotic fungal hyphae enters a plant cells through a specialized infection structure (appressorium).The plant plasma membrane invaginates and encases the penetrating hyphae. Protein effectors are first secreted to the tight interface between fungal cell wall and host plasma membrane. Following secretion they are likely to bind plant targets either in the interface or after translocation to the cytoplasm of plant cells.

Staff

Dr. Armin Djamei (postdoc)
Dr. Jinsong Wu (postdoc)
Dr. Shigeyuki Tanaka (postdoc)
Dr. Stefanie Reissmann (postdoc)
Liang Liang (PhD student)
Nina Neidig (PhD student)
Nancy Gross (PhD student)
Nicole Rössel (technical assistance)
Karin Münch (technical assistance)
Volker Vincon (technical assistance)

Publications since 2007

Kahmann, R. & Schirawski, J. (2007) Mating in the smut fungi: from a and b to the downstream cascades.In Sex in Fungi, (J. Heitman et al., eds.) ASM Press, Washington, 377-388

Molina, L. & Kahmann, R. (2007) An Ustilago maydis gene involved in H2O2 detoxification is required for virulence. Plant Cell 19, 2293-2309.

Brefort, T., Schipper, K., Doehlemann, G. & Kahmann, R. (2008) The biotrophic phase of Ustilago maydis: novel determinants for compatibility. In Genomics of Disease, Stadler Genetics Symposia Series, (J.P.Gustafson, J. Taylor and G.Stacey, eds.), Springer, New York pp.173-179.

Doehlemann, G., Wahl, R., Vranes, M., de Vries, R.P., Kamper, J. &

Kahmann, R. (2008) Establishment of compatibility in the Ustilago maydis/maize pathosystem. J Plant Physiol. 165, 29-40.

Reineke, G., Heinze, B., Schirawski, J., Buettner, H., Kahmann, R. & Basse, C.W. (2008)

Indole-3-acetic acid formation by the smut fungus Ustilago maydis contributes to increased auxin levels in infected maize tissue but is not essential for host tumor formation. Mol. Plant Pathol. 9, 339-355.

Zarnack,K., Eichhorn, H., Kahmann, R., & Feldbrügge, M. (2008) Target genes of transcription factor Prf1 respond differentially to MAPK regulation during pheromone signalling in Ustilago maydis . Mol. Microbiol. 69, 1041-1053.

Doehlemann, G., Wahl, R., Horst, R., Voll, L., Usadel, B., Poiree, F., Stitt,

M.,Sonnewald, U.,Pons, J., Kahmann, R. & Kämper, J. (2008) The biotrophic fungus Ustilago maydis suppresses plant cell death and reprograms metabolism of its host. Plant Journal 56, 181-195.

Mueller, O., Kahmann, R., Aguilar, G., Trejo-Aguilar, B., Wu, A., & de Vries,

A.P. (2008) The secretome of the maize pathogen Ustilago maydis. Fungal Genetics & Biol. 45, Suppl. 1: S63-70.

Doehlemann, G., van der Linde, K., Assmann, D., Schwammbach, D., Hof,

A.,Mohanty, A., Jackson, D., & Kahmann, R.(2009) Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells.PLoS Pathog. Feb;5(2):e1000290. Epub 2009 Feb 6.PMID: 19197359

Mendoza-Mendoza, A., Berndt, P., Djamei, A., Weise, C., Linne, U., Marahiel,

M.,Vranes, M., Kämper, J., & Kahmann, R.(2009) Physical-chemical plant-derived signals induce differentiation in Ustilago maydis. Mol Microbiol.71, 895-911.

Di Stasio, M., Brefort, T., Mendoza-Mendoza, A., Münch, K., & Kahmann,

R.(2009) The dual specificity phosphatase Rok1 negatively regulates mating and pathogenicity in Ustilago maydis. Mol. Microbiol. 73,73-88.

Mendoza-Mendoza, A., Eskova, A., Weise, C., Czajkowski, R., & Kahmann,

R.(2009) Hap2 regulates thepheromone response transcription factor prf1 in Ustilago maydis. Mol Microbiol. 72, 683-698.

Brefort, T., Doehlemann, G., Mendoza-Mendoza, A., Reissmann, S., Djamei,

A., & Kahmann, R.(2009) Ustilago maydis as a pathogen. Annu. Rev. Phytopathol. 47, 423-45.

Dong,X., & Kahmann, R. (2009) Battle for survival: plants and their allies

and enemies. Curr. Opin. Plant Biol. 12, 387-389.

Rispail, N., Soanes, D.M., Ant, C., Czajkowski, R., Grünler, A., Huguet, R., Perez-Nadales, E.,

Poli, A., Sartorel, E., Valiante, V., Yang, M., Beffa, R., Brakhage, A.A., Gow, N.A., Kahmann, R., Lebrun, M.H., Lenasi, H., Perez-Martin, J., Talbot, N.J., Wendland, J., & Di Pietro, A. (2009) Comparative genomics of MAP kinase and calcium-calcineurin signalling components in plant and human pathogenic fungi. Fungal Genet. Biol. 46:287-98.

Winterberg, B., Uhlmann, S., Linne, U., Lessing, F., Marahiel, M.A., Eichhorn, H.,Kahmann. R.,

& Schirawski, J. (2010) Elucidation of the complete ferrichrome A biosynthetic pathway in Ustilago maydis. Mol. Microbiol. 75, 1260-1271.

Horst, R.J., Doehlemann, G., Wahl, R., Hofmann, J., Schmiedl, A., Kahmann,

R., Kämper, J., Sonnewald, U., & Voll, L.M. (2010) Ustilago maydis infection strongly alters organic nitrogen allocation in maize and stimulates productivity of systemic source leaves. Plant Physiol. 152, 293-308.

Schipper, K., Doehlemann, G., Brefort, T., Djamei, A., Liang, L., Khrunyk, Y.,

Schirawski, J., & Kahmann R (2010) The effectors of smut fungi. In Biology of Plant-Microbe Interactions, Proceedings of the 14th International Congress of Plant Microbe Interactions (H. Antoun et al., eds.) Vol.7, pp1-8.

Lanver, D., Mendoza-Mendoza, A., Brachmann, A., & Kahmann, R.(2010)

Sho1 and Msb2-related proteins regulate appressorium development in the smut fungus Ustilago maydis. Plant Cell. 22(6):2085-2101.

Khrunyk, Y., Münch, K., Schipper, K., Lupas, A.N., & Kahmann, R.(2010) The use of FLP-mediated recombination for the functional analysis of an effector gene family in the biotrophic smut fungus Ustilago maydis. New Phytol. 187(4):957-968.

Berndt, P., Lanver, D., & Kahmann, R. (2010) The AGC Ser/Thr kinase Aga1 is essential for appressorium formation and maintenance of the actin cytoskeleton in the smut fungus Ustilago maydis. Mol. Microbiol. 78, 1484-1499.

Schirawski, J., Mannhaupt, G., Münch, K., Brefort, T., Schipper, K., Doehlemann, G., Di Stasio, M., Rössel, N., Mendoza-Mendoza, M.,Pester, D., Müller, O., Winterberg, B., Meyer, E., Ghareeb, H., Wollenberg, T., Münsterkötter, M.^, Wong, P., Walter, M., Stukenbrock, E., Güldener, U., & Kahmann, R. (2010) Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330, 1546-1548.

Van der Linde, K., Kastner, C., Kumlehn, J., Kahmann, R., & Doehlemann, G. (2011) Systemic virus induced gene silencing allows functional characterisation of maize genes during the biotrophic interaction with Ustilago maydis. New Phytol. 189, 471-483.

Doehlemann, G., Schipper, K., and Kahmann, R. (2011) The effectors of smut fungi. In Effectors of Plant Pathogenic Microbes (F. Martin and S. Kamoun, eds.).Blackwell-Publishing (in press).

Kahmann, R. & Schirawski, J. (2007) Mating in the smut fungi: from a and b to the downstream cascades.In Sex in Fungi, (J. Heitman et al., eds.) ASM Press, Washington, 377-388

Molina, L. & Kahmann, R. (2007) An Ustilago maydis gene involved in H2O2 detoxification is required for virulence. Plant Cell 19, 2293-2309.

Doehlemann, G., Wahl, R., Vranes, M., de Vries, R.P., Kamper, J. & Kahmann, R. (2008) Establishment of compatibility in the Ustilago maydis/maize pathosystem. J Plant Physiol. 165, 29-40.

Reineke, G., Heinze, B., Schirawski, J., Buettner, H., Kahmann, R. & Basse, C.W. (2008) Indole-3-acetic acid formation by the smut fungus Ustilago maydis contributes to increased auxin levels in infected maize tissue but is not essential for host tumor formation. Mol. Plant Pathol. 9, 339-355.

Doehlemann, G., Wahl, R., Horst, R., Voll, L., Usadel, B., Poiree, F., Stitt, M.,Sonnewald, U.,Pons, J., Kahmann, R. & Kämper, J. (2008) The biotrophic fungus Ustilago maydis suppresses plant cell death and reprograms metabolism of its host. Plant Journal 56, 181-195.

Mueller, O., Kahmann, R., Aguilar, G., Trejo-Aguilar, B., Wu, A., & de Vries, A.P. (2008) The secretome of the maize pathogen Ustilago maydis. Fungal Genetics & Biol. 45, Suppl. 1: S63-70.

Doehlemann, G., van der Linde, K., Assmann, D., Schwammbach, D., Hof, A.,Mohanty, A., Jackson, D., & Kahmann, R.(2009) Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells.PLoS Pathog. Feb;5(2):e1000290. Epub 2009 Feb 6.PMID: 19197359

Mendoza-Mendoza, A., Berndt, P., Djamei, A., Weise, C., Linne, U., Marahiel, M.,Vranes, M., Kämper, J., & Kahmann, R.(2009) Physical-chemical plant-derived signals induce differentiation in Ustilago maydis. Mol Microbiol.71, 895-911.

Di Stasio, M., Brefort, T., Mendoza-Mendoza, A., Münch, K., & Kahmann, R.(2009) The dual specificity phosphatase Rok1 negatively regulates mating and pathogenicity in Ustilago maydis. Mol. Microbiol. 73,73-88.

Mendoza-Mendoza, A., Eskova, A., Weise, C., Czajkowski, R., & Kahmann,

R.(2009) Hap2 regulates thepheromone response transcription factor prf1 in Ustilago maydis. Mol Microbiol. 72, 683-698.

Brefort, T., Doehlemann, G., Mendoza-Mendoza, A., Reissmann, S., Djamei, A., & Kahmann, R.(2009) Ustilago maydis as a pathogen. Annu. Rev. Phytopathol. 47, 423-45.

Dong,X., & Kahmann, R. (2009) Battle for survival: plants and their allies and enemies. Curr. Opin. Plant Biol. 12, 387-389.

Rispail, N., Soanes, D.M., Ant, C., Czajkowski, R., Grünler, A., Huguet, R., Perez-Nadales, E., Poli, A., Sartorel, E., Valiante, V., Yang, M., Beffa, R., Brakhage, A.A., Gow, N.A., Kahmann, R., Lebrun, M.H., Lenasi, H., Perez-Martin, J., Talbot, N.J., Wendland, J., & Di Pietro, A. (2009) Comparative genomics of MAP kinase and calcium-calcineurin signalling components in plant and human pathogenic fungi. Fungal Genet. Biol. 46:287-98.

Winterberg, B., Uhlmann, S., Linne, U., Lessing, F., Marahiel, M.A., Eichhorn, H.,Kahmann. R., & Schirawski, J. (2010) Elucidation of the complete ferrichrome A biosynthetic pathway in Ustilago maydis. Mol. Microbiol. 75, 1260-1271.

Horst, R.J., Doehlemann, G., Wahl, R., Hofmann, J., Schmiedl, A., Kahmann, R., Kämper, J., Sonnewald, U., & Voll, L.M. (2010) Ustilago maydis infection strongly alters organic nitrogen allocation in maize and stimulates productivity of systemic source leaves. Plant Physiol. 152, 293-308.

Schipper, K., Doehlemann, G., Brefort, T., Djamei, A., Liang, L., Khrunyk, Y., Schirawski, J., & Kahmann R (2010) The effectors of smut fungi. In Biology of Plant-Microbe Interactions, Proceedings of the 14th International Congress of Plant Microbe Interactions (H. Antoun et al., eds.) Vol.7, pp1-8.

Lanver, D., Mendoza-Mendoza, A., Brachmann, A., & Kahmann, R.(2010) Sho1 and Msb2-related proteins regulate appressorium development in the smut fungus Ustilago maydis. Plant Cell. 22(6):2085-2101.

Doehlemann, G., Schipper, K., and Kahmann, R. (2011) The effectors of smut fungi. In Effectors of Plant Pathogenic Microbes (F. Martin and S. Kamoun, eds.).Blackwell-Publishing (in press).