Skip to main content
SpringerLink
Log in

Pathocycles: Ustilago maydis as a model to study the relationships between cell cycle and virulence in pathogenic fungi

  • Review
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Activation of virulence in pathogenic fungi often involves differentiation processes that need the reset of the cell cycle and induction of a new morphogenetic program. Therefore, the fungal capability to modify its cell cycle constitutes an important determinant in carrying out a successful infection. The dimorphic fungus Ustilago maydis is the causative agent of corn smut disease and has lately become a highly attractive model in addressing fundamental questions about development in pathogenic fungi. The different morphological and genetic changes of U. maydis cells during the pathogenic process advocate an accurate control of the cell cycle in these transitions. This is why this model pathogen deserves attention as a powerful tool in analyzing the relationships between cell cycle, morphogenesis, and pathogenicity. The aim of this review is to summarize recent advances in the unveiling of cell cycle regulation in U. maydis. We also discuss the connection between cell cycle and virulence and how cell cycle control is an important downstream target in the fungus-plant interaction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agrios GN (1997) Plant pathology. Academic Press, London, UK

    Google Scholar 

  • Amon A, Irniger S, Nasmyth K (1994) Closing the cell cycle circle in yeast: G2 cyclin proteolysis initiated at mitosis persist until the activation of G1 cyclins in the next cycle. Cell 77:1037–1050

    PubMed  CAS  Google Scholar 

  • Andrews BJ, Herskowitz I (1989) The yeast Swi4 protein contains a motif present in developmental regulators and is part of a complex involved in cell cycle-dependent transcription. Nature 342:830–833

    PubMed  CAS  Google Scholar 

  • Bachewich C, Whiteway M (2005) Cyclin Cln3p links G1 progression to hyphal and pseudohyphal development in Candida albicans. Eukaryot Cell 4:95–102

    PubMed  CAS  Google Scholar 

  • Bähler J (2005) Cell-cycle control of gene expression in budding and fission yeast. Annu Rev Genet 39:69–94

    PubMed  Google Scholar 

  • Banuett F, Herskowitz I (1996) Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis. Development 122:2965–2976

    PubMed  CAS  Google Scholar 

  • Banuett F, Herskowitz I (2002) Bud morphogenesis and the actin and microtubule cytoskeletons during budding in the corn smut fungus, Ustilago maydis. Fungal Genet Biol 37:149–170

    PubMed  Google Scholar 

  • Basse CW, Steinberg G (2004) Ustilago maydis, model system for analysis of the molecular basis of fungal pathogenicity. Mol Plant Pathol 5:83–92

    PubMed  Google Scholar 

  • Bechinger C, Giebel KF, Schnell M, Leiderer P, Deising HB, Bastmeyer M (1999) Optical measurement of invasive forces exerted by appressoria of a plant pathogenic fungus. Science 285:1896–1899

    PubMed  CAS  Google Scholar 

  • Benton BK, Tinkelenberg AH, Jean D, Plump SD, Cross FR (1993) Genetic analysis of Cln/Cdc28 regulation of cell morphogenesis in budding yeast. EMBO J 12:5267–5275

    PubMed  CAS  Google Scholar 

  • Blanco M A, Sánchez-Díaz A, de Prada JM, Moreno S (2000) APC ste9/srw1 promotes degradation of mitotic cyclins in G1 and is inhibited by cdc2 phosphorylation. EMBO J 19:3945–3955

    PubMed  CAS  Google Scholar 

  • Bölker M (2001) Ustilago maydis, a valuable model system for the study of fungal dimorphism and virulence. Microbiology 147:1395–1401

    PubMed  Google Scholar 

  • Bölker M, Urban M, Kahmann R (1992) The a mating type locus of U. maydis specifies cell signaling components. Cell 68:441–450

    PubMed  Google Scholar 

  • Booher R, Beach D (1987) Interaction between cdc13 + and cdc2 + in the control of mitosis in fission yeast; dissociation of the G1 and G2 roles of the cdc2 + protein kinase. EMBO J 6:3441–3447

    PubMed  CAS  Google Scholar 

  • Booher RN, Deshaies RJ, Kirschner MW (1993) Properties of Saccharomyces cerevisiae Wee1 and its differential regulation of p34CDC28 in response to G1 and G2 cyclins. EMBO J 12:3417–3426

    PubMed  CAS  Google Scholar 

  • Bottin A, Kämper J, Kahmann R (1996) Isolation of a carbon source-regulated gene from Ustilago maydis. Mol Gen Genet 25:342–352

    Google Scholar 

  • Brachmann A, Weinzierl G, Kämper J, Kahmann R (2001) Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol Microbiol 42:1047–1063

    PubMed  CAS  Google Scholar 

  • Brachmann A, König J, Julius C, Feldbrügge M (2004) A reverse genetic approach for generating gene replacement mutants in Ustilago maydis. Mol Genet Genomics 272:216–226

    PubMed  CAS  Google Scholar 

  • Breeding CS, Hudson J, Balasubramanian MK, Hemmingsen SM, Young PG, Gould KL (1998) The cdr2 gene encodes a regulator of G2/M progression and cytokinesis in Schizosaccharomyces pombe. Mol Biol Cell 9:3399–3415

    PubMed  CAS  Google Scholar 

  • Brefort T, Müller P, Kahmann R (2005) The high-mobility-group domain transcription factor Rop1 is a direct regulator of prf1 in Ustilago maydis. Eukaryot Cell 4:379–391

    PubMed  CAS  Google Scholar 

  • Bueno A, Russell P (1993) Two fission yeast B-type cyclins, Cig2 and Cdc13, have different functions in mitosis. Mol Cell Biol 13:2286–2297

    PubMed  CAS  Google Scholar 

  • Castillo-Lluva S, García-Muse T, Pérez-Martín J (2004) A member of the Fizzy-related family of APC activators is required at different stages of plant infection by Ustilago maydis. J Cell Sci 117:4143–4156

    PubMed  CAS  Google Scholar 

  • Castillo-Lluva S, Pérez-Martín J (2005) The induction of the mating program in the phytopathogen Ustilago maydis is controlled by a G1 cyclin. Plant Cell 17:3544–3560

    PubMed  CAS  Google Scholar 

  • Chang F, Herskowitz I (1990) Identification of a gene necessary for cell cycle arrest by a negative growth factor of yeast: FAR1 is an inhibitor of a G1 cyclin. Cell 63:999–1011

    PubMed  CAS  Google Scholar 

  • Chapa y Lazo B, Bates S, Sudbery P (2005) The G1 cyclin Cln3 regulates morphogenesis in Candida albicans. Eukaryot Cell 4:90–94

    PubMed  CAS  Google Scholar 

  • Colomina N, Garí E, Gallego C, Herrero E, Aldea M (1999) G1 cyclins block the Ime1 pathway to make mitosis and meiosis incompatible in budding yeast. EMBO J 18:320–329

    PubMed  CAS  Google Scholar 

  • Connolly T, Beach D (1994) Interaction between the Cig1 and Cig2 B-type cyclins in the fission yeast cell cycle. Mol Cell Biol 14:768–776

    PubMed  CAS  Google Scholar 

  • Costanzo M, Nishikawa JL, Tang X, Millman JS, Schub O, Breitkreuz K, Dewar D, Rupes I, Andrews B, Tyers M (2004) CDK activity antagonizes Whi5, an inhibitor of G1/S transcription in yeast. Cell 117:899–913

    PubMed  CAS  Google Scholar 

  • Cross FR (1995) Starting the cell cycle: what’s the point? Curr Opin Cell Biol 7:790–797

    PubMed  CAS  Google Scholar 

  • Cvrkova F, Nasmyth K (1993) Yeast G1 cyclins CLN1 and CLN2 and a GAP-like protein have a role in bud formation. EMBO J 12:5277–5286

    Google Scholar 

  • Daga RR, Jimenez J (1999) Translational control of the Cdc25 cell cycle phosphatase: a molecular mechanism coupling mitosis to cell growth. J Cell Sci 112:3137–3146

    PubMed  CAS  Google Scholar 

  • Davey J (1998) Fusion of a fission yeast. Yeast 14:1529–1566

    PubMed  CAS  Google Scholar 

  • de Bruin RA, McDonald WH, Kalashnikova TI, Yates J, Wittenberg C (2004) Cln3 activates G1-specific transcription via phosphorylation of the SBF bound repressor Whi5. Cell 117:887–898

    PubMed  Google Scholar 

  • Deshaies RJ (1999) SCF and cullin/RING H2-based ubiquitin ligases. Annu Rev Cell Dev Biol 15:435–467

    PubMed  CAS  Google Scholar 

  • Devault A, Fesquet D, Cavadore JC, Garrrigues AM, Labbé JC, Lorca T, Picard A, Philippe M, Dorée M (1992) Cyclin A potentiates maturation-promoting factor activation in the early Xenopus embryo via inhibition of the tyrosine kinase that phosphorylates Cdc2. J Cell Biol 118:1109–1120

    PubMed  CAS  Google Scholar 

  • Dunphy WG (1994) The decision to enter mitosis. Trends Cell Biol 4:202–207

    PubMed  CAS  Google Scholar 

  • Eckstein JW, Beer-Romero P, Berdo I (1996) Identification of an essential acidic residue in Cdc25 protein phosphatase and a general three-dimensional model for a core region in protein phosphatases. Protein Sci 5:5–12

    Article  PubMed  CAS  Google Scholar 

  • Feldbrügge M, Kämper J, Steinberg G, Kahmann R (2004) Regulation of mating and pathogenic development in Ustilago maydis. Curr Opin Microbiol 7:666–672

    PubMed  Google Scholar 

  • Fink G, Steinberg G (2006) Dynein-dependent motility of microtubules and nucleation sites supports polarization of the tubulin array in the fungus Ustilago maydis. Mol Biol Cell 17:3242–3253

    PubMed  CAS  Google Scholar 

  • Fisher DL, Nurse P (1996) A single fission yeast mitotic cyclin B p34cdc2 kinase promotes both S-phase and mitosis in the absence of G1 cyclins. EMBO J 15:850–860

    PubMed  CAS  Google Scholar 

  • Flor-Parra I, Vranes M, Kämper J, Pérez-Martín J (2006) Biz1, a zinc finger protein that is required for plant invasion by Ustilago maydis regulates the levels of a mitotic cyclin. Plant Cell (in press)

  • Forsburg SL, Nurse P (1994) Analysis of the Schizosaccharomyces pombe cyclin puc1: evidence for a role in cell cycle exit. J Cell Sci 107:601–613

    PubMed  CAS  Google Scholar 

  • Fotheringham S, Holloman WK (1990) Pathways of transformation in Ustilago maydis determined by DNA conformation. Genetics 124:833–843

    PubMed  CAS  Google Scholar 

  • Fuchs U, Manns I, Steinberg G (2005) Microtubules are dispensable for the initial pathogenic development but required for long-distance hyphal growth in the corn smut fungus Ustilago maydis. Mol Biol Cell 16:2746–2758

    PubMed  CAS  Google Scholar 

  • Furuno N, den Elzen N, Pines J (1999) Human cyclin A is required for mitosis until mid prophase. J Cell Biol 147:295–306

    PubMed  CAS  Google Scholar 

  • Gallego C, Gari E, Colomina N, Herrero E, Aldea M (1997) The Cln3 cyclin is down-regulated by translational repression and degradation during the G1 arrest caused by nitrogen deprivation in budding yeast. EMBO J 16:7196–7206

    PubMed  CAS  Google Scholar 

  • García-Muse T, Steinberg G, Pérez-Martín J (2003) Pheromone-induced G2 arrest in the phytopathogenic fungus Ustilago maydis. Eukaryot Cell 2:494–500

    PubMed  Google Scholar 

  • García-Muse T, Steinberg G, Pérez-Martín J (2004) Characterization of B-type cyclins in the smut fungus Ustilago maydis: roles in morphogenesis and pathogenicity. J Cell Sci 117:487–506

    PubMed  Google Scholar 

  • Garrido E, Pérez-Martín J (2003) The crk1 gene encodes an Ime2-related protein that is required for morphogenesis in the plant pathogen Ustilago maydis. Mol Microbiol 47:729–743

    PubMed  CAS  Google Scholar 

  • Garrido E, Voß U, Müller P, Castillo-Lluva S, Kahmann R, Pérez-Martín J (2004) The induction of sexual development and virulence in the smut fungus Ustilago maydis depends on Crk1, a novel MAPK protein. Genes Dev 18:3117–3130

    PubMed  CAS  Google Scholar 

  • Gow NA (1995) Yeast-hyphal dimorphism. In: Gow NAR, Gadd GM (eds) The growing fungus. Chapman and Hall, London, pp 403–422

    Google Scholar 

  • Hagan IM (1998) The fission yeast microtubule cytoskeleton. J Cell Sci 111:1603–1612

    PubMed  CAS  Google Scholar 

  • Hagan I, Hayles J, Nurse P (1988) Cloning and sequencing of the cyclin-related cdc13 + geneand a cytological study of its role in fission yeast mitosis. J Cell Sci 91:587–595

    PubMed  CAS  Google Scholar 

  • Hartmann HA, Kahmann R, Bölker M (1996) The pheromone response factor coordinates filamentous growth and pathogenic development in Ustilago maydis. EMBO J 15:1632–1641

    PubMed  CAS  Google Scholar 

  • Hartmann HA, Krüger J, Lottspeich F, Kahmann R (1999) Environmental signals controlling sexual development of the corn smut fungus Ustilago maydis through the transcriptional regulator Prf1. Plant Cell 11:1293–1305

    PubMed  CAS  Google Scholar 

  • Harvey SL, Kellogg DR (2003) Conservation of mechanisms controlling entry into mitosis: budding yeast Wee1 delays entry into mitosis and is required for cell size control. Curr Biol 13:264–275

    PubMed  CAS  Google Scholar 

  • Jacobs CW, Mattichak SJ, Knowles JF (1994) Budding patterns during the cell cycle of the maize smut pathogen Ustilago maydis. Can J Bot 72:1675–1680

    Google Scholar 

  • Jagadish MN, Carter BL (1977) Genetic control of cell division in yeast cultured at different growth rates. Nature 269:145–147

    PubMed  CAS  Google Scholar 

  • Johnston GC, Pringle JR, Hartwell LH (1977) Coordination of growth with cell division in the yeast Saccharomyces cerevisiae. Exp Cell Res 105:79–98

    PubMed  CAS  Google Scholar 

  • Jorgensen P, Nishikawa JL, Breitkreutz BJ, Tyers M (2002) Systematic identification of pathways that couple cell growth and cell division in yeast. Science 297:395–400

    PubMed  CAS  Google Scholar 

  • Kahmann R, Steinberg G, Basse C, Feldbrügge M, Kämper J (2000) Ustilago maydis, the causative agent of corn smut disease. In: Kronstad JW (eds), Fungal pathology. Kluwer Academic Publishers, Dodrecht, The Netherlands

    Google Scholar 

  • Kahmann R, Kämper J (2004) Ustilago maydis: how its biology relates to pathogenic development. New Phytol 16:31–42

    Google Scholar 

  • Kaldis P (1999) The Cdk-activating kinase (CAK): from yeast to mammals. Cell Mol Life Sci 55:284–296

    PubMed  CAS  Google Scholar 

  • Kanoh J, Russell P (1998) The protein kinase Cdr2, related to Nim1/Cdr1 mitotic inducer, regulates the onset of mitosis in fission yeast. Mol Biol Cell 9:3321–3334

    PubMed  CAS  Google Scholar 

  • Kellogg DR (2003) Wee1-dependent mechanisms required for coordination of cell growth and cell division. J Cell Sci 116:4883–4890

    PubMed  CAS  Google Scholar 

  • Kitamura K, Maekawa H, Shimoda C (1998) Fission yeast Ste9, a homolog of Hct1/Cdh1 and Fizzy-related, is a novel negative regulator of cell cycle progression during G1-phase. Mol Biol Cell 9:1065–1080

    PubMed  CAS  Google Scholar 

  • Koch C, Nasmyth K (1994) Cell cycle regulated transcription in yeast. Curr Opin Cell Biol 6:451–459

    PubMed  CAS  Google Scholar 

  • Koch C, Moll T, Neuberg M, Ahorn H, Nasmyth K (1993) A role for the transcription factors Mbp1 and swi4 in progression from G1 to S phase. Science 261:1551–1557

    PubMed  CAS  Google Scholar 

  • Kojic M, Holloman WK (2000) Shuttle vectors for genetic manipulations in Ustilago maydis. Can J Microbiol 46:333–338

    PubMed  CAS  Google Scholar 

  • Krylov D, Nasmyth K, Koonin EV (2003) Evolution of eukaryotic cell cycle regulation: stepwise addition of regulatory kinases and late advent of the CDKs. Current Biol 13:173–177

    CAS  Google Scholar 

  • Kumar R, Reynolds DM, Shevchenko A, Goldstone SD, Dalton S (2000) Forkhead transcription factors, Fkh1p and Fkh2p, collaborate with Mcm1p to control transcription required for M-phase. Curr Biol 10:896–906

    PubMed  CAS  Google Scholar 

  • Lee KS, Park JE, Asano S, Park CJ (2005) Yeast polo-like kinases: functionally conserved multitask mitotic regulators. Oncogene 24:217–229

    PubMed  CAS  Google Scholar 

  • Lenz JH, Schuchardt I, Straube A, Steinberg G (2006) A dynein loading zone for retrograde endosome motility at microtubule plus-end. EMBO J 25:2275–2286

    PubMed  CAS  Google Scholar 

  • Lew DJ (2000) Cell cycle checkpoints that ensure coordination between nuclear and cytoplasmic events in Saccharomyces cerevisiae. Curr Opin Genet Dev 10:47–53

    PubMed  CAS  Google Scholar 

  • Lew DJ, Reed SI (1993) Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins. J Cell Biol 16:6794–6803

    Google Scholar 

  • Loeb JDJ, Kerensteva TA, Pan T, Sepulveda-Becerra M, Liu H (1999a) Saccharomyces cerevisiae G1 cyclins are differentially involved in invasive and pseudohyphal growth independent of the filamentation mitogen-activated protein kinase pathway. Genetics 153:1535–1546

    CAS  Google Scholar 

  • Loeb JDJ, Sepulveda-Becerra M, Hazan I, Liu H (1999b) A G1 cyclin is necessary for maintenance of filamentous growth in Candida albicans. Mol Cell Biol 1:4019–4027

    Google Scholar 

  • Lowndes NF, Johnson AL, Breeden L, Johnston LH (1992) Swi6 protein is required for transcription of the periodically expressed DNA synthesis genes in budding yeast. Nature 357:505–508

    PubMed  CAS  Google Scholar 

  • Lundgren K, Walworth N, Booher R, Dembski M, Kirschner M, Beach D (1991) Mik1 and Wee1 cooperate in the inhibitory tyrosine phosphorylation of Cdc2. Cell 64:1111–1122

    PubMed  CAS  Google Scholar 

  • Martín-Castellanos C, Labib K, Moreno S (1996) B-type cyclins regulate G1 progression in fission yeast in opposition to the p25rum1 CDK inhibitor. EMBO J 15:839–849

    PubMed  Google Scholar 

  • McMillan JN, Longtine MS, Sia RA, Theesfeld CL, Bardes ES, Pringle JR, Lew DJ (1999) The morphogenesis checkpoint in Saccharomyces cerevisiae: cell cycle control of Swe1p degradation by Hsl1p and Hsl7p. Mol Cell Biol 19:6929–6939

    PubMed  CAS  Google Scholar 

  • McNeill SA, Nurse P (1997) Cell cycle control in fission yeast. In: Pringle JR, Broach JR, Jones EW (eds) The molecular and cellular biology of the yeast saccharomyces, vol 3. Cell cycle and cell biology. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, pp 697–763

    Google Scholar 

  • Millar JB, McGowan CH, Lenaers G, Jones R, Russell P (1991) p80cdc25 mitotic inducer is the tyrosine phosphatase that activates p34cdc2 kinase in fission yeast. EMBO J 10:4301–4309

    PubMed  CAS  Google Scholar 

  • Millar JBA, Lanaers G, Russell P (1992) Pyp3 PTPase acts as a mitotic inducer in fission yeast. EMBO J 11:4933–4941

    PubMed  CAS  Google Scholar 

  • Mitchison JM, Nurse P (1985) Growth in cell length in the fission yeast Schizosaccharomyces pombe. J Cell Sci 75:357–376

    PubMed  CAS  Google Scholar 

  • Mondesert O, McGowan CH, Russell P (1996) Cig2, a B-type cyclin, promotes the onset of S in Schizosaccharomyces pombe. Mol Cell Biol 16:1527–1533

    PubMed  CAS  Google Scholar 

  • Moreno S, Nurse P (1994) Regulation of progression through the G1 phase of the cell cycle by the rum1 gene. Nature 367:236–242

    PubMed  CAS  Google Scholar 

  • Müller P, Aichinger C, Feldbrügge M, Kahmann R (1999) The MAP kinase kpp2 regulates mating and pathogenic development in Ustilago maydis. Mol Microbiol 34:1007–1017

    PubMed  Google Scholar 

  • Müller P, Weinzierl G, Brachmann A, Feldbrügge M, Kahmann R (2003) Mating and pathogenic development of the smut fungus Ustilago maydis are regulated by one mitogen-activated protein kinase cascade. Eukaryot Cell 2:1187–1199

    PubMed  Google Scholar 

  • Murray AW (2004) Recycling the cell cycle: cyclins revisited. Cell 116:221–234

    PubMed  CAS  Google Scholar 

  • Pardee AB (1989) G1 events and regulation of cell proliferation. Science 246:603–608

    PubMed  CAS  Google Scholar 

  • Parviz F, Heideman W (1998) Growth-independent regulation of CLN3 mRNA levels by nutrients in Saccharomyces cerevisiae. J Bacteriol 180:225–230

    PubMed  CAS  Google Scholar 

  • Peter M, Herskowitz I (1994a) Joining the complex: cyclin-dependent kinase inhibitory proteins and the cell cycle. Cell 79:181–184

    CAS  Google Scholar 

  • Peter M, Herskowitz I (1994b) Direct inhibition of the yeast cyclin-dependent kinase Cdc28-Cln by Far1. Science 265:1228–1231

    CAS  Google Scholar 

  • Peter M, Garttner A, Horecka J, Ammere G, Herskowitz I (1993) Far1 links the signal transduction pathway to the cell cycle machinery in yeast. Cell 73:747–760

    PubMed  CAS  Google Scholar 

  • Peters JM (2002) The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol Cell 9:931–943

    PubMed  CAS  Google Scholar 

  • Pic A, Lim FL, Ross SJ, Veal EA, Johnson AL, Sultan MR, West AG, Johnston LH, Sharrocks AD, Morgan BA (2000) The forkhead protein Fkh2 is a component of the yeast cell cycle transcription factor SFF. EMBO J 19:3750–3761

    PubMed  CAS  Google Scholar 

  • Pines J (1995) Cyclins and cyclin-dependent kinases: a biochemical view. Biochem J 308:697–711

    PubMed  CAS  Google Scholar 

  • Polymenis M, Schmidt EV (1997) Coupling of cell division to cell growth by translational control of the G1 cyclin CLN3 in yeast. Genes Dev 11:2522–2531

    PubMed  CAS  Google Scholar 

  • Pringle JR, Hartwell LH (1981) The Saccharomyces cell cycle. In: Strathern JN, Jones EW, Broach JR (eds) The molecular biology of the yeast Saccharomyces. Cold Spring harbor Laboratory Press, Cold Spring Harbor, New York, pp 97–142

    Google Scholar 

  • Reis T, Edgar BA (2004) Negative regulation of dE2F1 by cyclin-dependent kinases controls cell cycle timing. Cell 117:253–264

    PubMed  CAS  Google Scholar 

  • Richardson HE, Wittenberg C, Cross F, Reed SI (1989) An essential G1 function for cyclin-like proteins in yeast. Cell 59:1127–1133

    PubMed  CAS  Google Scholar 

  • Rua D, Tobe BT, Kron SJ (2001) Cell cycle control of yeast filamentous growth. Curr Opin Microbiol 4:720–727

    PubMed  CAS  Google Scholar 

  • Rudner AD, Murray AW (2000) Phosphorylation by Cdc28 activates the Cdc20-dependent activity of the anaphase-promoting complex. J Cell Biol 149:1377–1390

    PubMed  CAS  Google Scholar 

  • Rupes I (2002) Checking cell size in yeast. Trends Genet 18:479–485

    PubMed  CAS  Google Scholar 

  • Sarafan-Vasseur N, Lamy A, Bourguignon J, Le Pessot F, Hieter P, Sesboüé R, Bastard C, Frébourg T, Flaman JM (2002) Overexpression of B-type cyclins alters chromosomal segregation. Oncogene 21:2051–2057

    PubMed  CAS  Google Scholar 

  • Schneider BLL, Yang QH, Futcher B (1996) Linkage of replication to start by the Cdk inhibitor Sic1. Science 272:880–882

    Google Scholar 

  • Schuchardt I, Assmann D, thines E, Schuberth C, Steinberg G (2005) Myosin-V, kinesin-1, and kinesisn-3 cooperate in hyphal growth of the fungus Ustilago maydis. Mol Biol Cell 16:5191–5201

    PubMed  CAS  Google Scholar 

  • Schwab M, Lutum AS, Seufert W (1997) Yeast Hct1 is a regulator of Clb2 cyclin proteolysis. Cell 90:683–693

    PubMed  CAS  Google Scholar 

  • Schwob E, Böhm T, Mendenhall MD, Nasmyth K (1994) The B-type cyclin kinase inhibitor p40SIC1 controls the G1 to S transition in S. cerevisiae. Cell 79:233–244

    PubMed  CAS  Google Scholar 

  • Sgarlata C, Pérez-Martín J (2005a) Inhibitory phosphorylation of a mitotic cyclin-dependent kinase regulates the morphogenesis, cell size and virulence of the smut fungus Ustilago maydis. J Cell Sci 15:3607–3622

    Google Scholar 

  • Sgarlata C, Pérez-Martín J (2005b) The Cdc25 phosphatase is essential for the G2/M phase transition in the basidiomycete Ustilago maydis. Mol Microbiol 58:1482–1496

    Article  CAS  Google Scholar 

  • Sipiczki M (2000) Where does fission yeast sit on the tree of life? Genome Biol 1:1011–1014

    Google Scholar 

  • Sherr CJ, Roberts JM (1999) CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13:1501–1512

    PubMed  CAS  Google Scholar 

  • Snetselaar KM, Mims CW (1992) Sporidial fusion and infection of maize seedlings by the smut fungus Ustilago maydis. Mycologia 84:193–203

    Google Scholar 

  • Snetselaar KM, Mims CW (1993) Infection of maize stigmas by Ustilago maydis: light and electron microscopy. Phytopathology 83:843–850

    Google Scholar 

  • Snetselaar KM, Bölker M, Kahmann R (1996) Ustilago maydis mating hyphae orient their growth toward pheromone sources. Fungal Genet Biol 20:299–312

    PubMed  Google Scholar 

  • Snetselaar KM, McCann MP (1997) Using microdensitometry to correlate cell morphology with the nuclear cycle in Ustilago maydis. Mycologia 89:689–697

    Google Scholar 

  • Snetselaar KM, Carfioli MA, Cordisco KM (2001) Pollination can protect maize ovaries from infection by Ustilago maydis, the corn smut fungus. Can J Bot 79:1390–1399

    Google Scholar 

  • Spellig T, Bölker M, Lottspeich F, Frank RW, Kahmann R (1994) Pheromones trigger filamentous growth in Ustilago maydis. EMBO J 13:1620–1627

    PubMed  CAS  Google Scholar 

  • Spellig T, Bottin A, Kahmann R (1996) Green fluorescent protein (GFP) as a new vital marker in the phytopathogenic fungus Ustilago maydis. Mol Gen Genet 252:503–509

    PubMed  CAS  Google Scholar 

  • Sprague GF, Thorner JW (1992) Pheromone response and signal transduction during the mating process of Saccharomyces cerevisiae. In: Broach JR, Pringle JR, Jones EW (eds), The molecular and cellular biology of the yeast saccharomyces: gene expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor New York

    Google Scholar 

  • Spruck CH, Won KA, Reed SI (1999) Deregulated cyclin E induces chromosome instability. Nature 401:297–300

    PubMed  CAS  Google Scholar 

  • Steinberg G, Wedlich-Söldner R, Brill M, Schulz I (2001) Microtubules in the fungal pathogen Ustilago maydis are highly dynamic and determine cell polarity. J Cell Sci 114:609–622

    PubMed  CAS  Google Scholar 

  • Stern B, Nurse P (1997) Fission yeast pheromone blocks S-phase by inhibiting the G1 cyclin B-p34cdc2 kinase. EMBO J 16:534–544

    PubMed  CAS  Google Scholar 

  • Stern B, Nurse P (1998) Cyclin B proteolysis and the cyclin-dependent kinase inhibitor Rum1p are required for pheromone-induced G1 arrest in fission yeast. Mol Biol Cell 9:1309–1321

    PubMed  CAS  Google Scholar 

  • Straube A, Enard W, Berner A, Wedlich-Soldner R, Kahmann R, Steinberg G (2001) A split motor domain in a cytoplasmic dynein. EMBO J 20:5091–5100

    PubMed  CAS  Google Scholar 

  • Straube A, Brill M, Oakley BR, Horio T, Steinberg G (2003) Microtubule organization requires cell cycle-dependent nucleation at dispersed cytoplasmic sites: polar and perinuclear microtubule organizing centers in the plant pathogen Ustilago maydis. Mol Biol Cell 14:642–657

    PubMed  CAS  Google Scholar 

  • Sveiczer A, Novak B, Mitchinson JM (1996) Mitotic control in the absence of Cdc25 mitotic inducer in fission yeast. J Cell Sci 109:2947–2957

    PubMed  CAS  Google Scholar 

  • Talbot NJ (2003) On the trail of a cereal killer: exploring the biology of Magnaporthe grisea. Annu Rev Microbiol 57:177–202

    PubMed  CAS  Google Scholar 

  • Tjandra H, Compton J, Kellogg D (1998) Control of mitotic events by the Cdc42 GTPase, the Clb2 cyclin and a member of the PAK kinase family. Curr Biol 8:991–1000

    PubMed  CAS  Google Scholar 

  • Tran PT, Marsh L, Doyve V, Inoue S, Chang F (2001) A mechanism for nuclear positioning in fission yeast based on microtubule pushing. J Cell Biol 153:397–411

    PubMed  CAS  Google Scholar 

  • Tsukuda T, Carleton S, Fotheringham S, Holloman WK (1988) Isolation and characterization of an autonomously replicating sequence from Ustilago maydis. Mol Cell Biol 8:3703–3709

    PubMed  CAS  Google Scholar 

  • Valdivieso MH, Sugimoto K, Jahng KY, Fernandes PMB, Wittenberg C (1993) FAR1 is required for post-transcriptional regulation of CLN2 gene expression in response to mating pheromone. Mol Cell Biol 13:1013–1022

    PubMed  CAS  Google Scholar 

  • Verma R, Annan RS, Huddleston MJ, Carr SA, Reynard G, Deshaies RJ (1997) Phosphorylation of Sic1 by G1 Cdk required for its degradation and entry into S phase. Science 278:455–460

    PubMed  CAS  Google Scholar 

  • Visintin R, Prinz S, Amon A (1997) CDC20 and CDH1: a family of substrate-specific activators of APC-dependent proteolysis. Science 278:460–463

    PubMed  CAS  Google Scholar 

  • Wang H, Gari E, Verges E, Gallego C, Aldea M (2004) Recruitment of Cdc28 by Whi3 restricts nuclear accumulation of the G1 cyclin-Cdk complex to late G1. EMBO J 23:180–190

    PubMed  CAS  Google Scholar 

  • Watanabe N, Broome M, Hunter T (1995) Regulation of the human WEE1 Hu CDK tyrosine 15-kinase during the cell cycle. EMBO J 14:1878–1891

    PubMed  CAS  Google Scholar 

  • Wedlich-Söldner R, Straube A, Friedrich MW, Steinberg G (2002) A balance of KIF1A-like kinesin and dynein organizes early endosomes in the fungus Ustilago maydis. EMBO J 21:2946–2957

    PubMed  Google Scholar 

  • Weingartner M, Pelayo HR, Binarova P, Zwerger K, Melikant B, de la Torre C, Heberle-Bors E, Bögre L (2003) A plant cyclin B2 is degraded early in mitosis and its ectopic expression shortens G2-phase and alleviates the DNA-damage checkpoint. J Cell Sci 116:487–498

    PubMed  CAS  Google Scholar 

  • Whitehall S, Stacey P, Dawson K, Jones N (1999) Cell-cycle regulated transcription in fission yeast: Cdc10-Res protein interactions during the cell cycle and domains required for regulated transcription. Mol Biol Cell 10:3705–3715

    PubMed  CAS  Google Scholar 

  • Winsor B, Schiebel E (1997) An overview of the Saccharomyces cerevisiae microtubule and microfilament cytoskeleton. Yeast 13:399–434

    PubMed  CAS  Google Scholar 

  • Wu L, Shiozaki K, Aligue R, Russell P (1996) Spatial organization of the Nim1-Wee1-Cdc2 mitotic cdontrol network in Schizosaccharomyces pombe. Mol Biol Cell 7:1749–1758

    PubMed  CAS  Google Scholar 

  • Yamaguchi S, Murakami H, Okayama H (1997) A WD repeat protein controls the cell cycle and differentiation by negatively regulating cdc2/B-type cyclin complexes. Mol Biol Cell 8:2475–2486

    PubMed  CAS  Google Scholar 

  • Yamaguchi S, Okayama H, Nurse P (2000) Fission yeast fizzy-related protein srw1p is a G1-specific promoter of mitotic cyclin B degradation. EMBO J 19:3986–3977

    Google Scholar 

  • Yin XY, Grove L, Datta NS, Katula K, Long MW, Prochownik EV (2001) Inverse regulation of cyclin B1 by c-Myc and p53 and induction of tetraploidy by cyclin B1 overexpression. Cancer Res 61:6487–6493

    PubMed  CAS  Google Scholar 

  • Zachariae W, Nasmyth K (1999) Whose end is destruction: cell division and the anaphase-promoting complex. Genes Dev 13:2039–2058

    PubMed  CAS  Google Scholar 

  • Zheng X, Wang Y, Wang Y (2004) Hcg1, a novel hypgha-specific G1 cyclin-related protein regulates Candida albicans hyphal morphogenesis. EMBO J 23:1845–1856

    PubMed  CAS  Google Scholar 

  • Zhu G, Spellman PT, Volpe T, Brown PO, Botstein D, Davis TN, Futcher B (2000) Two yeast forkhead genes regulate the cell cycle and pseudohyphal growth. Nature 406:90–94

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This review summarizes the work performed in the laboratory of JPM since 2000. Along these years, the continuous and generous support of Regine Kahmann by providing technical help, material, and discussion has been crucial and determinant for the development of the topic. To enter into Ustilago maydis field represented for JPM an acceptance with open arms and friendship by the entire Ustilago community. JPM want to thank members of Max-Planck-Institut für Terrestrische Mikrobiologie at Marburg for hospitality and the availability to discuss any topic related to Ustilago. JPM really appreciate the friendship of Gero Steinberg, who helped me enter into the cell biology area; Michel Feldbrügge, who provided me with vectors and lots of ideas; Jöerg Kämper, for a lot of productive discussions and Andreas Brachmann, for smashing my head with questions. JPM also acknowledges the gift of Fig. 5 and critical reading of the manuscript from Gero Steinberg and the help with the English language from my wife, Loreto Carmona. The careful editing labor of one of the anonymous reviewers is also appreciated. The work of JPM is supported by the MCyT (BIO2005-02998).

Author information

Authors and Affiliations

  1. Departamento de Biotecnología Microbiana, Centro Nacional de Biotecnología-CSIC, Campus de Cantoblanco-UAM, 28049, Madrid, Spain

    José Pérez-Martín, Sonia Castillo-Lluva, Cecilia Sgarlata, Ignacio Flor-Parra, Natalia Mielnichuk, Joaquín Torreblanca & Natalia Carbó

Authors
  1. José Pérez-Martín
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sonia Castillo-Lluva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cecilia Sgarlata
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ignacio Flor-Parra
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Natalia Mielnichuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Joaquín Torreblanca
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Natalia Carbó
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José Pérez-Martín.

Additional information

Communicated by T. Nyström

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pérez-Martín, J., Castillo-Lluva, S., Sgarlata, C. et al. Pathocycles: Ustilago maydis as a model to study the relationships between cell cycle and virulence in pathogenic fungi. Mol Genet Genomics 276, 211–229 (2006). https://doi.org/10.1007/s00438-006-0152-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-006-0152-6

Keywords

Search

Navigation