The Gβ-Subunit-Encoding Gene bpp1 Controls Cyclic-AMP Signaling in Ustilago maydis

ABSTRACT In the phytopathogenic fungus Ustilago maydis, fusion of haploid cells is a prerequisite for infection. This process is controlled by a pheromone-receptor system. The receptors belong to the seven-transmembrane class that are coupled to heterotrimeric G proteins. Of four Gα subunits in U. maydis, only gpa3 has a function during mating and cyclic AMP (cAMP) signaling. Activation of the cAMP cascade induces pheromone gene expression; however, it does not lead to the induction of conjugation tubes seen after pheromone stimulation. To investigate the possibility that a Gβ subunit participates in pheromone signaling, we isolated the single β subunit gene, bpp1, from U. maydis. bpp1 deletion mutants grew filamentously and showed attenuated pheromone gene expression, phenotypes associated with Δgpa3 strains. In addition, a constitutively active allele of gpa3 suppressed the phenotype of the bpp1 deletion strains. We suggest that Bpp1 and Gpa3 are components of the same heterotrimeric G protein acting on adenylyl cyclase. Interestingly, while Δgpa3 strains are impaired in pathogenicity, Δbpp1 mutants are able to induce plant tumors. This could indicate that Gpa3 operates independently of Bpp1 during pathogenic development.

[1]  M. Bölker,et al.  Tagging pathogenicity genes inUstilago maydis by restriction enzyme-mediated integration (REMI) , 1995, Molecular and General Genetics MGG.

[2]  M. Bölker,et al.  Identification of the pheromone response element inUstilago maydis , 1996, Molecular and General Genetics MGG.

[3]  G. A. White,et al.  Isolation, characterization and sequence of a gene conferring resistance to the systemic fungicide carboxin from the maize smut pathogen, Ustilago maydis , 1991, Current Genetics.

[4]  M. Feldbrügge,et al.  Mating and Pathogenic Development of the Smut Fungus Ustilago maydis Are Regulated by One Mitogen-Activated Protein Kinase Cascade , 2003, Eukaryotic Cell.

[5]  M. Feldbrügge,et al.  PKA and MAPK phosphorylation of Prf1 allows promoter discrimination in Ustilago maydis , 2003, The EMBO journal.

[6]  Gyungsoon Park,et al.  The G‐beta subunit MGB1 is involved in regulating multiple steps of infection‐related morphogenesis in Magnaporthe grisea , 2003, Molecular microbiology.

[7]  D. Nuss,et al.  Constitutively activated Galpha negatively regulates virulence, reproduction and hydrophobin gene expression in the chestnut blight fungus Cryphonectria parasitica. , 2003, Fungal genetics and biology : FG & B.

[8]  Sona Jain,et al.  The G protein β subunit FGB1 regulates development and pathogenicity in Fusarium oxysporum , 2003, Current Genetics.

[9]  J. Heitman,et al.  The Gα Protein Gpa2 Controls Yeast Differentiation by Interacting with Kelch Repeat Proteins that Mimic Gβ Subunits , 2002 .

[10]  K. Borkovich,et al.  A G-Protein β Subunit Required for Sexual and Vegetative Development and Maintenance of Normal Gα Protein Levels in Neurospora crassa , 2002, Eukaryotic Cell.

[11]  I. Sakai,et al.  Type-specific Regulation of Adenylyl Cyclase , 2001, The Journal of Biological Chemistry.

[12]  J. Kämper,et al.  Identification of genes in the bW/bE regulatory cascade in Ustilago maydis , 2001, Molecular microbiology.

[13]  C. Sánchez-Martínez,et al.  Dimorphism in fungal pathogens: Candida albicans and Ustilago maydis--similar inputs, different outputs. , 2001, Current opinion in microbiology.

[14]  C. S. Hoffman,et al.  The git5 Gbeta and git11 Ggamma form an atypical Gbetagamma dimer acting in the fission yeast glucose/cAMP pathway. , 2001, Genetics.

[15]  J. Heitman,et al.  Signal Transduction Cascades Regulating Fungal Development and Virulence , 2000, Microbiology and Molecular Biology Reviews.

[16]  C. S. Hoffman,et al.  Glucose monitoring in fission yeast via the Gpa2 galpha, the git5 Gbeta and the git3 putative glucose receptor. , 2000, Genetics.

[17]  M. Feldbrügge,et al.  Activation of the cAMP pathway in Ustilago maydis reduces fungal proliferation and teliospore formation in plant tumors. , 2000, Molecular plant-microbe interactions : MPMI.

[18]  D. Andrews,et al.  The Ustilago maydis ubc4 and ubc5 genes encode members of a MAP kinase cascade required for filamentous growth. , 2000, Molecular plant-microbe interactions : MPMI.

[19]  C. S. Hoffman,et al.  The fission yeast git5 gene encodes a Gbeta subunit required for glucose-triggered adenylate cyclase activation. , 2000, Genetics.

[20]  J. Heitman,et al.  The G-Protein β Subunit GPB1 Is Required for Mating and Haploid Fruiting in Cryptococcus neoformans , 2000, Molecular and Cellular Biology.

[21]  Michael Feldbrügge,et al.  Ustilago maydis, the Causative Agent of Corn Smut Disease , 2000 .

[22]  M. Feldbrügge,et al.  The MAP kinase Kpp2 regulates mating and pathogenic development in Ustilago maydis , 1999, Molecular microbiology.

[23]  S. Gold,et al.  A MAP kinase encoded by the ubc3 gene of Ustilago maydis is required for filamentous growth and full virulence , 1999, Molecular microbiology.

[24]  F. Lottspeich,et al.  Environmental Signals Controlling Sexual Development of the Corn Smut Fungus Ustilago maydis through the Transcriptional Regulator Prf1 , 1999, Plant Cell.

[25]  Temple F. Smith,et al.  The WD repeat: a common architecture for diverse functions. , 1999, Trends in biochemical sciences.

[26]  R. Kahmann,et al.  Crosstalk between cAMP and pheromone signalling pathways in Ustilago maydis , 1998, Molecular and General Genetics MGG.

[27]  J. Kronstad,et al.  Identification of a cAMP-dependent protein kinase catalytic subunit required for virulence and morphogenesis in Ustilago maydis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[28]  D. Nuss,et al.  Targeted disruption of a fungal G-protein beta subunit gene results in increased vegetative growth but reduced virulence. , 1997, Molecular plant-microbe interactions : MPMI.

[29]  S. Gold,et al.  The Ustilago maydis regulatory subunit of a cAMP-dependent protein kinase is required for gall formation in maize. , 1997, The Plant cell.

[30]  M. Bölker,et al.  G proteins in Ustilago maydis: transmission of multiple signals? , 1997, The EMBO journal.

[31]  J. Kämper,et al.  Isolation of a carbon source-regulated gene from Ustilago maydis , 1996, Molecular and General Genetics MGG.

[32]  Bolker,et al.  Ustilago maydis Mating Hyphae Orient Their Growth toward Pheromone Sources , 1996, Fungal genetics and biology : FG & B.

[33]  T. Smith,et al.  Folding of proteins with WD-repeats: comparison of six members of the WD-repeat superfamily to the G protein beta subunit. , 1996, Biochemistry.

[34]  M. Bölker,et al.  The pheromone response factor coordinates filamentous growth and pathogenicity in Ustilago maydis. , 1996, The EMBO journal.

[35]  R. Kahmann,et al.  Genetic Regulation of Mating and Dimorphism in Ustilago Maydis , 1995 .

[36]  R. Kahmann,et al.  Filament-specific expression of a cellulase gene in the dimorphic fungus Ustilago maydis. , 1995, Biological chemistry Hoppe-Seyler.

[37]  J. Kämper,et al.  Multiallelic recognition: Nonself-dependent dimerization of the bE and bW homeodomain proteins in ustilago maydis , 1995, Cell.

[38]  S. Gold,et al.  cAMP regulates morphogenesis in the fungal pathogen Ustilago maydis. , 1994, Genes & development.

[39]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[40]  Raman Nambudripad,et al.  The ancient regulatory-protein family of WD-repeat proteins , 1994, Nature.

[41]  I. Herskowitz,et al.  Identification of fuz7, a Ustilago maydis MEK/MAPKK homolog required for a-locus-dependent and -independent steps in the fungal life cycle. , 1994, Genes & development.

[42]  S. Gold,et al.  Identification and complementation of a mutation to constitutive filamentous growth in Ustilago maydis. , 1993, Molecular plant-microbe interactions : MPMI.

[43]  I. Herskowitz,et al.  The a locus governs cytoduction in Ustilago maydis , 1992, Journal of bacteriology.

[44]  F. Banuett.  Ustilago maydis, the delightful blight. , 1992, Trends in genetics : TIG.

[45]  B. Gillissen,et al.  A two-component regulatory system for self/non-self recognition in Ustilago maydis , 1992, Cell.

[46]  M. Bölker,et al.  The a mating type locus of U. maydis specifies cell signaling components , 1992, Cell.

[47]  A. Gilman,et al.  Type-specific regulation of adenylyl cyclase by G protein beta gamma subunits. , 1991, Science.

[48]  A. Gilman,et al.  Cloning and expression of a widely distributed (type IV) adenylyl cyclase. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Melvin I. Simon,et al.  Diversity of G proteins in signal transduction , 1991, Science.

[50]  A. Brown,et al.  Receptor-effector coupling by G proteins. , 1990, Biochimica et biophysica acta.

[51]  I. Herskowitz,et al.  The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif , 1990, Cell.

[52]  I. Herskowitz,et al.  Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[53]  David Y. Thomas,et al.  The STE4 and STE18 genes of yeast encode potential β and γ subunits of the mating factor receptor-coupled G protein , 1989, Cell.

[54]  M. Whiteway,et al.  The STE4 and STE18 genes of yeast encode potential beta and gamma subunits of the mating factor receptor-coupled G protein. , 1989, Cell.

[55]  W. Holloman,et al.  Isolation and characterization of an autonomously replicating sequence from Ustilago maydis , 1988, Molecular and cellular biology.

[56]  F. Winston,et al.  A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. , 1987, Gene.

[57]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[58]  Robert C. King,et al.  Handbook of Genetics , 1976, Springer US.