Comparison of morphogenetic networks of filamentous fungi and yeast.

Fungi generally display either of two growth modes, yeast-like or filamentous, whereas dimorphic fungi, upon environmental stimuli, are able to switch between the yeast-like and the filamentous growth mode. Signal transduction pathways have been elucidated in the budding yeast Saccharomyces cerevisiae, establishing a morphogenetic network that links cell-cycle events with cellular morphogenesis. Recent molecular genetic studies in several filamentous fungal model systems revealed key components required for distinct steps from fungal spore germination to the maintenance of polar hyphal growth, mycelium formation, and nuclear division. This allows a mechanistic comparison of yeast-like and hyphal growth and the establishment of a core model morphogenetic network for filamentous growth including signaling via the cAMP pathway, Rho modules, and cell cycle kinases. Appreciating similarities between morphogenetic networks of the unicellular yeasts and the multicellular filamentous fungi will open new research directions, help in isolating the central network components, and ultimately pave the way to elucidate the central differences (of many) that distinguish, e.g., the growth mode of filamentous fungi from that of their yeast-like relatives, the role of cAMP signaling, and nuclear division.

[1]  S. Osmani,et al.  Mitotic Histone H3 Phosphorylation by the NIMA Kinase in Aspergillus nidulans , 2000, Cell.

[2]  A. Pardee,et al.  A restriction point for control of normal animal cell proliferation. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Zhenbiao Yang,et al.  Arabidopsis Rho-related GTPases: differential gene expression in pollen and polar localization in fission yeast. , 1998, Plant physiology.

[4]  J. Pringle,et al.  CDC42 and CDC43, two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae , 1990, The Journal of cell biology.

[5]  G. Martı́nez-Cadena,et al.  The small GTP-binding protein Rho is expressed differentially during spore germination of Phycomyces blakesleeanus. , 1999, Microbiology.

[6]  P. Philippsen,et al.  Cell polarity and hyphal morphogenesis are controlled by multiple rho-protein modules in the filamentous ascomycete Ashbya gossypii. , 2001, Genetics.

[7]  M. Mendenhall,et al.  Regulation of Cdc28 Cyclin-Dependent Protein Kinase Activity during the Cell Cycle of the Yeast Saccharomyces cerevisiae , 1998, Microbiology and Molecular Biology Reviews.

[8]  G C Johnston,et al.  Regulation of cell size in the yeast Saccharomyces cerevisiae , 1979, Journal of bacteriology.

[9]  D. Lew.  Cell-cycle checkpoints that ensure coordination between nuclear and cytoplasmic events in Saccharomyces cerevisiae. , 2000, Current opinion in genetics & development.

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

[11]  Zu-Wen Sun,et al.  Mitotic Phosphorylation of Histone H3 Is Governed by Ipl1/aurora Kinase and Glc7/PP1 Phosphatase in Budding Yeast and Nematodes , 2000, Cell.

[12]  S. Osmani,et al.  bimA encodes a member of the tetratricopeptide repeat family of proteins and is required for the completion of mitosis in Aspergillus nidulans. , 1991, Journal of cell science.

[13]  Stefan Hohmann,et al.  The Yeast Glycerol 3-Phosphatases Gpp1p and Gpp2p Are Required for Glycerol Biosynthesis and Differentially Involved in the Cellular Responses to Osmotic, Anaerobic, and Oxidative Stress* , 2001, The Journal of Biological Chemistry.

[14]  Markus J. Tamás,et al.  Molecular and physiological characterization of the NAD‐dependent glycerol 3‐phosphate dehydrogenase in the filamentous fungus Aspergillus nidulans , 2001, Molecular microbiology.

[15]  Sabine Martin,et al.  Phospholipase C Binds to the Receptor-like GPR1Protein and Controls Pseudohyphal Differentiation inSaccharomyces cerevisiae * , 1999, The Journal of Biological Chemistry.

[16]  J. Sweigard,et al.  Magnaporthe grisea Pth11p Is a Novel Plasma Membrane Protein That Mediates Appressorium Differentiation in Response to Inductive Substrate Cues , 1999, Plant Cell.

[17]  E. Bremer,et al.  Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments , 1998, Archives of Microbiology.

[18]  S. Osmani,et al.  Checkpoint defects leading to premature mitosis also cause endoreplication of DNA in Aspergillus nidulans. , 1999, Molecular biology of the cell.

[19]  A. Pardee.  G1 events and regulation of cell proliferation. , 1989, Science.

[20]  Gerald R. Fink,et al.  Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: Regulation by starvation and RAS , 1992, Cell.

[21]  S. Osmani,et al.  Regulation of the mRNA levels of nimA, a gene required for the G2-M transition in Aspergillus nidulans , 1987, The Journal of cell biology.

[22]  M. Werner-Washburne,et al.  Expressed sequences from conidial, mycelial, and sexual stages of Neurospora crassa. , 1997, Fungal genetics and biology : FG & B.

[23]  M. Polymenis,et al.  Coupling of cell division to cell growth by translational control of the G1 cyclin CLN3 in yeast. , 1997, Genes & development.

[24]  Zhenbiao Yang,et al.  Inhibition of Pollen Tube Elongation by Microinjected Anti-Rop1Ps Antibodies Suggests a Crucial Role for Rho-Type GTPases in the Control of Tip Growth. , 1997, The Plant cell.

[25]  J. Xu,et al.  Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[26]  J. Feijó,et al.  Growing Pollen Tubes Possess a Constitutive Alkaline Band in the Clear Zone and a Growth-dependent Acidic Tip , 1999, The Journal of cell biology.

[27]  Curt Wittenberg,et al.  An essential G1 function for cyclin-like proteins in yeast , 1989, Cell.

[28]  F. Klis,et al.  Cell wall perturbation in yeast results in dual phosphorylation of the Slt2/Mpk1 MAP kinase and in an Slt2-mediated increase in FKS2-lacZ expression, glucanase resistance and thermotolerance. , 2000, Microbiology.

[29]  S. Osmani,et al.  Parallel activation of the NIMA and p34cdc2 cell cycle-regulated protein kinases is required to initiate mitosis in A. nidulans , 1991, Cell.

[30]  P. Leiderer,et al.  Optical measurements of invasive forces exerted by appressoria of a plant pathogenic fungus , 1999, Science.

[31]  J. Heitman,et al.  The G protein-coupled receptor gpr1 is a nutrient sensor that regulates pseudohyphal differentiation in Saccharomyces cerevisiae. , 2000, Genetics.

[32]  John E. Linz,et al.  Evidence that MRas1 and MRas3 proteins are associated with distinct cellular functions during growth and morphogenesis in the fungus Mucor racemosus. , 1999, Fungal genetics and biology : FG & B.

[33]  Heath,et al.  The Cytoplasmic pH Influences Hyphal Tip Growth and Cytoskeleton-Related Organization , 1997, Fungal genetics and biology : FG & B.

[34]  S. Harris,et al.  The duplication cycle in Aspergillus nidulans. , 1997, Fungal genetics and biology : FG & B.

[35]  J. Szeberényi,et al.  Different Roles for RhoA During Neurite Initiation, Elongation, and Regeneration in PC12 Cells , 1999, Journal of neurochemistry.

[36]  A. Walmsley,et al.  cAMP signalling in pathogenic fungi: control of dimorphic switching and pathogenicity. , 2000, Trends in microbiology.

[37]  J. Heinisch,et al.  The protein kinase C‐mediated MAP kinase pathway involved in the maintenance of cellular integrity in Saccharomyces cerevisiae , 1999, Molecular microbiology.

[38]  J. Pringle,et al.  Roles of the CDC24 gene product in cellular morphogenesis during the Saccharomyces cerevisiae cell cycle , 1981, The Journal of cell biology.

[39]  W. H. Mager,et al.  The control of intracellular glycerol in Saccharomyces cerevisiae influences osmotic stress response and resistance to increased temperature , 2000, Molecular microbiology.

[40]  L. Lim,et al.  Phosphatidylinositol 3-Kinase, Cdc42, and Rac1 Act Downstream of Ras in Integrin-Dependent Neurite Outgrowth in N1E-115 Neuroblastoma Cells , 2000, Molecular and Cellular Biology.

[41]  Douglas I. Johnson,et al.  The Cdc42p GTPase Is Involved in a G2/M Morphogenetic Checkpoint Regulating the Apical-Isotropic Switch and Nuclear Division in Yeast* , 1999, The Journal of Biological Chemistry.

[42]  G. Roeder,et al.  The pachytene checkpoint in S. cerevisiae depends on Swe1-mediated phosphorylation of the cyclin-dependent kinase Cdc28. , 1999, Molecular cell.

[43]  T. Hunt,et al.  The proteolysis of mitotic cyclins in mammalian cells persists from the end of mitosis until the onset of S phase. , 1996, The EMBO journal.

[44]  M. Kirschner,et al.  Identification of BIME as a Subunit of the Anaphase-Promoting Complex , 1996, Science.

[45]  D. Drubin,et al.  The ADF/cofilin proteins: stimulus-responsive modulators of actin dynamics. , 1995, Molecular biology of the cell.

[46]  J. Doonan,et al.  Spindle formation and chromatin condensation in cells blocked at interphase by mutation of a negative cell cycle control gene , 1988, Cell.

[47]  O. Yarden,et al.  Protein phosphatase 2A is involved in hyphal growth of Neurospora crassa , 1998, Molecular and General Genetics MGG.

[48]  J. Hamer,et al.  Interaction between developmental and cell cycle regulators is required for morphogenesis in Aspergillus nidulans , 1999, The EMBO journal.

[49]  N. Chua,et al.  Rac Homologues and Compartmentalized Phosphatidylinositol 4, 5-Bisphosphate Act in a Common Pathway to Regulate Polar Pollen Tube Growth , 1999, The Journal of cell biology.

[50]  N. Morris.  Nucleosome structure in Aspergillus nidulans , 1976, Cell.

[51]  T. Svitkina,et al.  Actin machinery: pushing the envelope. , 2000, Current opinion in cell biology.

[52]  R. Dean,et al.  G Protein α Subunit Genes Control Growth, Development, and Pathogenicity of Magnaporthe grisea , 1997 .

[53]  B. Tye.  MCM proteins in DNA replication. , 1999, Annual review of biochemistry.

[54]  S. Osmani,et al.  Regulation of the anaphase-promoting complex/cyclosome by bimAAPC3 and proteolysis of NIMA. , 1998, Molecular biology of the cell.

[55]  J. Thevelein,et al.  Opposite roles of trehalase activity in heat-shock recovery and heat-shock survival in Saccharomyces cerevisiae. , 1999, The Biochemical journal.

[56]  S. Reed,et al.  Cell cycle control of morphogenesis in budding yeast. , 1995, Current opinion in genetics & development.

[57]  M. Momany,et al.  Aspergillus nidulans swo mutants show defects in polarity establishment, polarity maintenance and hyphal morphogenesis. , 1999, Genetics.

[58]  P. Scacheri,et al.  nimO, an Aspergillus gene related to budding yeast Dbf4, is required for DNA synthesis and mitotic checkpoint control. , 1999, Journal of cell science.

[59]  J. Grindlay,et al.  The Bub2p spindle checkpoint links nuclear migration with mitotic exit. , 2000, Molecular cell.

[60]  D. Callaham,et al.  Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: effect of BAPTA-type buffers and hypertonic media. , 1994, The Plant cell.

[61]  M. Goebl,et al.  CDC55, a Saccharomyces cerevisiae gene involved in cellular morphogenesis: identification, characterization, and homology to the B subunit of mammalian type 2A protein phosphatase , 1991, Molecular and cellular biology.

[62]  L. Wu,et al.  A Role for NIMA in the Nuclear Localization of Cyclin B in Aspergillus nidulans , 1998, The Journal of cell biology.

[63]  C. Scazzocchio,et al.  Post-transcriptional control and kinetic characterization of proline transport in germinating conidiospores of Aspergillus nidulans. , 1995, FEMS microbiology letters.

[64]  F. Banuett.  Signalling in the Yeasts: An Informational Cascade with Links to the Filamentous Fungi , 1998, Microbiology and Molecular Biology Reviews.

[65]  P. Philippsen,et al.  Determination of cell polarity in germinated spores and hyphal tips of the filamentous ascomycete Ashbya gossypii requires a rhoGAP homolog. , 2000, Journal of cell science.

[66]  S. Osmani,et al.  The NIMA protein kinase is hyperphosphorylated and activated downstream of p34cdc2/cyclin B: coordination of two mitosis promoting kinases. , 1995, The EMBO journal.

[67]  Guang-Chao Chen,et al.  Rho1p, a Yeast Protein at the Interface Between Cell Polarization and Morphogenesis , 1996, Science.

[68]  B. Antonsson,et al.  Protein kinase C in yeast. Characteristics of the Saccharomyces cerevisiae PKC1 gene product. , 1994, The Journal of biological chemistry.

[69]  L. Wu,et al.  Isolation of a Functional Homolog of the Cell Cycle-specific NIMA Protein Kinase of Aspergillus nidulans and Functional Analysis of Conserved Residues (*) , 1995, The Journal of Biological Chemistry.

[70]  J. Thevelein.  Signal transduction in yeast , 1994, Yeast.

[71]  F. Townsley,et al.  Proteolytic ratchets that control progression through mitosis. , 1998, Trends in cell biology.

[72]  H. Wang,et al.  Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. , 1999, Science.

[73]  C. d’Enfert,et al.  Neutral trehalases catalyse intracellular trehalose breakdown in the filamentous fungi Aspergillus nidulans and Neurospora crassa , 1999, Molecular microbiology.

[74]  Divergent cAMP Signaling Pathways Regulate Growth and Pathogenesis in the Rice Blast Fungus Magnaporthe grisea , 1998, Plant Cell.

[75]  A. Vancura,et al.  Phosphoinositide-specific phospholipase C interacts with phosphatidylinositol kinase homolog TOR2. , 1998, Biochemical and biophysical research communications.

[76]  M. Kirschner,et al.  Properties of Saccharomyces cerevisiae wee1 and its differential regulation of p34CDC28 in response to G1 and G2 cyclins. , 1993, The EMBO journal.

[77]  T. Som,et al.  Developmental decisions in Aspergillus nidulans are modulated by Ras activity , 1994, Molecular and cellular biology.

[78]  K. Toenjes,et al.  The guanine-nucleotide-exchange factor Cdc24p is targeted to the nucleus and polarized growth sites , 1999, Current Biology.

[79]  G. Martı́nez-Cadena,et al.  The GTP-binding protein G alpha s is present in dormant spores and expressed differentially during spore germination of the fungus Phycomyces blakesleeanus. , 1995, Microbiology.

[80]  G. Faye,et al.  Civ1 (CAK In Vivo), a Novel Cdk-Activating Kinase , 1996, Cell.

[81]  I. Herskowitz,et al.  A role for the Pkc1 MAP kinase pathway of Saccharomyces cerevisiae in bud emergence and identification of a putative upstream regulator , 1997, The EMBO journal.

[82]  R. Dean,et al.  The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. , 1997, The Plant cell.

[83]  J. Doonan,et al.  sodVIC is an alpha-COP-related gene which is essential for establishing and maintaining polarized growth in Aspergillus nidulans. , 1999, Fungal genetics and biology : FG & B.

[84]  Marc Bickle,et al.  The Yeast Phosphatidylinositol Kinase Homolog TOR2 Activates RHO1 and RHO2 via the Exchange Factor ROM2 , 1997, Cell.

[85]  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.

[86]  S. Osmani,et al.  The G2/M DNA damage checkpoint inhibits mitosis through Tyr15 phosphorylation of p34cdc2 in Aspergillus nidulans , 1997, The EMBO journal.

[87]  S. Gold,et al.  Characterization and Molecular Genetic Complementation of Mutants Affecting Dimorphism in the FungusUstilago maydis , 1998 .

[88]  J. Tinsley,et al.  Analysis of actin and actin-related protein 3 (ARP3) gene expression following induction of hyphal tip formation and apolar growth in Neurospora , 1998, Molecular and General Genetics MGG.

[89]  P. Kaldis,et al.  The Cdk-Activating Kinase (CAK) from Budding Yeast , 1996, Cell.

[90]  K Nasmyth,et al.  Mass spectrometric analysis of the anaphase-promoting complex from yeast: identification of a subunit related to cullins. , 1998, Science.

[91]  R. Li.  Mitosis: Shutting the door behind when you leave , 2000, Current Biology.

[92]  L. Vidali,et al.  The role of plant villin in the organization of the actin cytoskeleton, cytoplasmic streaming and the architecture of the transvacuolar strand in root hair cells of Hydrocharis , 2000, Planta.

[93]  Kim Nasmyth,et al.  Closing the cell cycle circle in yeast: G2 cyclin proteolysis initiated at mitosis persists until the activation of G1 cyclins in the next cycle , 1994, Cell.

[94]  I. Heath,et al.  Direct evidence for Ca2+ regulation of hyphal branch induction , 1997, Fungal genetics and biology : FG & B.

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

[96]  P. Nurse,et al.  Premature chromatin condensation upon accumulation of NIMA. , 1994, The EMBO journal.

[97]  N. Osherov,et al.  Conidial germination in Aspergillus nidulans requires RAS signaling and protein synthesis. , 2000, Genetics.

[98]  R. Ballester,et al.  A family of genes required for maintenance of cell wall integrity and for the stress response in Saccharomyces cerevisiae. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[99]  R. Dean,et al.  The cAMP-dependent protein kinase catalytic subunit is required for appressorium formation and pathogenesis by the rice blast pathogen Magnaporthe grisea. , 1995, The Plant cell.

[100]  M. Snyder,et al.  Molecular basis of cell integrity and morphogenesis in Saccharomyces cerevisiae. , 1995, Microbiological reviews.

[101]  B. Errede,et al.  Mid2 Is a Putative Sensor for Cell Integrity Signaling in Saccharomyces cerevisiae , 1999, Molecular and Cellular Biology.

[102]  B. Futcher,et al.  Inhibition of Gl cyclin activity by the Ras/cAMP pathway in yeast , 1994, Nature.

[103]  H. Prokisch,et al.  Impairment of calcineurin function in Neurospora crassa reveals its essential role in hyphal growth, morphology and maintenance of the apical Ca2+ gradient , 1997, Molecular and General Genetics MGG.

[104]  J. Broach,et al.  Efficient transition to growth on fermentable carbon sources in Saccharomyces cerevisiae requires signaling through the Ras pathway , 1998, The EMBO journal.

[105]  M. Snyder,et al.  Spa2p Interacts with Cell Polarity Proteins and Signaling Components Involved in Yeast Cell Morphogenesis , 1998, Molecular and Cellular Biology.

[106]  A. Pardo,et al.  Characterization of small GTPases Cdc42 and Rac and the relationship between Cdc42 and actin cytoskeleton in vegetative and ectomycorrhizal hyphae of Suillus bovinus. , 2001, Molecular plant-microbe interactions : MPMI.

[107]  I. Heath,et al.  Plasma membrane-adjacent actin filaments, but not microtubules, are essential for both polarization and hyphal tip morphogenesis in Saprolegnia ferax and Neurospora crassa. , 2000, Fungal genetics and biology : FG & B.

[108]  K. Shimizu,et al.  Genetic involvement of a cAMP-dependent protein kinase in a G protein signaling pathway regulating morphological and chemical transitions in Aspergillus nidulans. , 2001, Genetics.

[109]  S. Osmani,et al.  Cell cycle regulation in Aspergillus by two protein kinases. , 1996, The Biochemical journal.

[110]  Chandra L. Theesfeld,et al.  The Morphogenesis Checkpoint in Saccharomyces cerevisiae: Cell Cycle Control of Swe1p Degradation by Hsl1p and Hsl7p , 1999, Molecular and Cellular Biology.

[111]  L S Robertson,et al.  The yeast A kinases differentially regulate iron uptake and respiratory function. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[112]  Zhenbiao Yang,et al.  Control of Pollen Tube Tip Growth by a Rop GTPase–Dependent Pathway That Leads to Tip-Localized Calcium Influx , 1999, Plant Cell.

[113]  M. Wigler,et al.  Cloning and characterization of BCY1, a locus encoding a regulatory subunit of the cyclic AMP-dependent protein kinase in Saccharomyces cerevisiae , 1987, Molecular and cellular biology.

[114]  A. Murray,et al.  S-phase feedback control in budding yeast independent of tyrosine phosphorylation of P34cdc28 , 1992, Nature.

[115]  M. O'Connell,et al.  An extra copy of nimEcyclinB elevates pre‐MPF levels and partially suppresses mutation of nimTcdc25 in Aspergillus nidulans. , 1992, The EMBO journal.

[116]  Michael N. Hall,et al.  Cell Wall Stress Depolarizes Cell Growth via Hyperactivation of Rho1 , 1999, The Journal of cell biology.

[117]  S. Moreno,et al.  Threshold level of protein kinase A activity and polarized growth in Mucor rouxii. , 2000, Microbiology.

[118]  J. Hamer,et al.  The Aspergillus nidulans sepA gene encodes an FH1/2 protein involved in cytokinesis and the maintenance of cellular polarity , 1997, The EMBO journal.

[119]  S. Harris,et al.  Morphogenesis is coordinated with nuclear division in germinating Aspergillus nidulans conidiospores. , 1999, Microbiology.

[120]  J. Kronstad,et al.  Signaling via cAMP in fungi: interconnections with mitogen-activated protein kinase pathways , 1998, Archives of Microbiology.

[121]  Sergio Moreno,et al.  Conservation of mitotic controls in fission and budding yeasts , 1989, Cell.

[122]  M. Peter,et al.  Phosphorylation of the Cdc42 exchange factor Cdc24 by the PAK-like kinase Cla4 may regulate polarized growth in yeast. , 2000, Molecular cell.

[123]  D. Kellogg,et al.  Control of mitotic events by the Cdc42 GTPase, the Clb2 cyclin and a member of the PAK kinase family , 1998, Current Biology.

[124]  A. Bretscher,et al.  Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. , 2000, Journal of cell science.

[125]  J. Cooper,et al.  Actin dynamics: Assembly and disassembly of actin networks , 2000, Current Biology.

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

[127]  L. Alberghina,et al.  Repression of growth-regulated Gl cyclin expression by cyclic AMP in budding yeast , 1994, Nature.

[128]  P. Nurse.  Universal control mechanism regulating onset of M-phase , 1990, Nature.

[129]  Matthias Peter,et al.  Nuclear sequestration of the exchange factor Cdc24 by Far1 regulates cell polarity during yeast mating , 2000, Nature Cell Biology.

[130]  Troy Ketela,et al.  Saccharomyces cerevisiae Mid2p Is a Potential Cell Wall Stress Sensor and Upstream Activator of thePKC1-MPK1 Cell Integrity Pathway , 1999, Journal of bacteriology.

[131]  J. Thevelein,et al.  Induction of neutral trehalase Nth1 by heat and osmotic stress is controlled by STRE elements and Msn2/Msn4 transcription factors: variations of PKA effect during stress and growth , 2000, Molecular microbiology.

[132]  J. Xu,et al.  MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. , 1996, Genes & development.

[133]  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.

[134]  J. Hamer,et al.  hyp loci control cell pattern formation in the vegetative mycelium of Aspergillus nidulans. , 1998, Genetics.

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

[136]  D. E. Levin,et al.  Wsc1 and Mid2 Are Cell Surface Sensors for Cell Wall Integrity Signaling That Act through Rom2, a Guanine Nucleotide Exchange Factor for Rho1 , 2001, Molecular and Cellular Biology.

[137]  J. D. de Winde,et al.  Novel sensing mechanisms and targets for the cAMP–protein kinase A pathway in the yeast Saccharomyces cerevisiae , 1999, Molecular microbiology.

[138]  E. Schaftingen,et al.  Glycerol Formation After the Breaking of Dormancy of Phycomyces-blakesleeanus Spores - Role of An Interconvertible Glycerol-3-phosphatase , 1985 .

[139]  S. Reed,et al.  Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins , 1993, The Journal of cell biology.

[140]  D. Hall,et al.  Regulation of the Cln3–Cdc28 kinase by cAMP in Saccharomyces cerevisiae , 1998, The EMBO journal.

[141]  J. Thevelein,et al.  Cyclic AMP and the stimulation of trehalase activity in the yeast Saccharomyces cerevisiae by carbon sources, nitrogen sources and inhibitors of protein synthesis. , 1985, Journal of general microbiology.

[142]  A. Brown,et al.  Regulatory networks controlling Candida albicans morphogenesis. , 1999, Trends in microbiology.

[143]  Robson,et al.  Polarized Growth of Fungal Hyphae Is Defined by an Alkaline pH Gradient , 1996, Fungal genetics and biology : FG & B.

[144]  G. Bécard,et al.  Intracellular pH in arbuscular mycorrhizal fungi. A symbiotic physiological marker , 1998, Plant physiology.

[145]  J. Chernoff,et al.  Plant GTPases: the Rhos in bloom. , 2000, Trends in cell biology.

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

[147]  J. Rine,et al.  Yeast spore germination: a requirement for Ras protein activity during re‐entry into the cell cycle , 1997, The EMBO journal.

[148]  N. Talbot,et al.  Glycerol generates turgor in rice blast , 1997, Nature.

[149]  J. Heitman,et al.  Signal transduction cascades regulating pseudohyphal differentiation of Saccharomyces cerevisiae. , 2000, Current opinion in microbiology.

[150]  J. Vandekerckhove,et al.  Villin Function in the Organization of the Actin Cytoskeleton , 1999, The Journal of Biological Chemistry.

[151]  K Nasmyth,et al.  CLB5 and CLB6, a new pair of B cyclins involved in DNA replication in Saccharomyces cerevisiae. , 1993, Genes & development.

[152]  S. Osmani,et al.  A single p34cdc2 protein kinase (encoded by nimXcdc2) is required at G1 and G2 in Aspergillus nidulans. , 1994, Journal of cell science.

[153]  S. Osmani,et al.  Mitotic destruction of the cell cycle regulated NIMA protein kinase of Aspergillus nidulans is required for mitotic exit. , 1995, The EMBO journal.

[154]  P. Kaldis,et al.  Dephosphorylation of cyclin-dependent kinases by type 2C protein phosphatases. , 1999, Genes & development.

[155]  Aljoscha Nern,et al.  Nucleocytoplasmic Shuttling of the Cdc42p Exchange Factor Cdc24p , 2000, The Journal of cell biology.

[156]  K Tanaka,et al.  Rom1p and Rom2p are GDP/GTP exchange proteins (GEPs) for the Rho1p small GTP binding protein in Saccharomyces cerevisiae. , 1996, The EMBO journal.

[157]  J. Condeelis,et al.  Bundling of actin filaments by elongation factor 1 alpha inhibits polymerization at filament ends , 1996, The Journal of cell biology.

[158]  J. Hirsch,et al.  GPR1 encodes a putative G protein‐coupled receptor that associates with the Gpa2p Gα subunit and functions in a Ras‐independent pathway , 1998, The EMBO journal.

[159]  S. Osmani,et al.  Two S‐phase checkpoint systems, one involving the function of both BIME and Tyr15 phosphorylation of p34cdc2, inhibit NIMA and prevent premature mitosis. , 1996, The EMBO journal.

[160]  A. F. Hofmann,et al.  Identification and characterization of genes required for hyphal morphogenesis in the filamentous fungus Aspergillus nidulans. , 1999, Genetics.

[161]  K. Nasmyth,et al.  Regulation of p34CDC28 tyrosine phosphorylation is not required for entry into mitosis in S. cerevisiae , 1992, Nature.

[162]  R. Aramayo,et al.  Loss of growth polarity and mislocalization of septa in a Neurospora mutant altered in the regulatory subunit of cAMP‐dependent protein kinase. , 1996, The EMBO journal.

[163]  E. Nigg,et al.  Characterization of mammalian NIMA-related kinases. , 1997, Methods in enzymology.

[164]  A. Means,et al.  Expression of the noncatalytic domain of the NIMA kinase causes a G2 arrest in Aspergillus nidulans. , 1994, The EMBO journal.

[165]  R. Mullins,et al.  How WASP-family proteins and the Arp2/3 complex convert intracellular signals into cytoskeletal structures. , 2000, Current opinion in cell biology.

[166]  J. Hamer,et al.  Identification and characterization of Aspergillus nidulans mutants defective in cytokinesis. , 1994, Genetics.

[167]  C. Wittenberg,et al.  Regulation of Cell Size by Glucose Is Exerted via Repression of the CLN1 Promoter , 1998, Molecular and Cellular Biology.

[168]  A. Bretscher,et al.  Polarization of cell growth in yeast. , 2000, Journal of cell science.

[169]  P. Philippsen,et al.  A PAK-like protein kinase is required for maturation of young hyphae and septation in the filamentous ascomycete Ashbya gossypii. , 2000, Journal of cell science.