Two Cdc2 Kinase Genes with Distinct Functions in Vegetative and Infectious Hyphae in

English version České info

In the model yeasts and filamentous fungi, CDC2 is an essential gene that encodes the only CDK essential for mitotic cell cycle progression. However, the wheat scab fungus F. graminearum contains two CDC2 orthologs. The cdc2A and cdc2B deletion mutants had no defects in vegetative growth but deletion of both is lethal. Whereas the cdc2B mutant was normal, the cdc2A mutant was almost non-pathogenic, indicating that only Cdc2A is essential in infectious hyphae. Cdc2A and Cdc2B differ in subcellular localization and only localization of Cdc2A to the nucleus was increased in cells active in mitosis. Furthermore, F. graminearum uniquely has two orthologs of Ipl1 Aurora kinase and mutants deleted of orthologs of five essential yeast mitotic kinase genes were viable. However, most of these mutants were significantly reduced in virulence. Overall, our data indicate that F. graminearum differs from the model fungi in CDK and other key mitotic kinase genes, and cell cycle regulation is different between vegetative and infectious hyphae. This is the first report on two Cdc2 kinases in fungi and they differ in subcellular localization and functions during sexual reproduction and plant infection.

Vyšlo v časopise: Two Cdc2 Kinase Genes with Distinct Functions in Vegetative and Infectious Hyphae in. PLoS Pathog 11(6): e32767. doi:10.1371/journal.ppat.1004913
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004913

Souhrn

Zdroje

1. Morgan DO (1997) Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu Rev Cell Dev Biol 13: 261–291. 9442875

2. Ubersax JA, Woodbury EL, Quang PN, Paraz M, Blethrow JD, et al. (2003) Targets of the cyclin-dependent kinase Cdk1. Nature 425: 859–864. 14574415

3. Liu J, Kipreos ET (2000) Evolution of cyclin-dependent kinases (CDKs) and CDK-activating kinases (CAKs): differential conservation of CAKs in yeast and metazoa. Mol Biol Evol 17: 1061–1074. 10889219

4. Morgan DO (2007) The Cell Cycle: Principles of Control: London: New Science Press.

5. Humphrey T, Pearce A (2005) Cell cycle molecules and mechanisms of the budding and fission yeasts. Methods Mol Biol 296: 3–29. 15576924

6. Malumbres M, Barbacid M (2007) Cell cycle kinases in cancer. Curr Opin Genet Dev 17: 60–65. 17208431

7. Booher R, Beach D (1986) Site-specific mutagenesis of cdc2+, a cell cycle control gene of the fission yeast Schizosaccharomyces pombe. Mol Cell Biol 6: 3523–3530. 3796591

8. Mendenhall MD, Hodge AE (1998) Regulation of Cdc28 cyclin-dependent protein kinase activity during the cell cycle of the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 62: 1191–1243. 9841670

9. Ferrari S (2006) Protein kinases controlling the onset of mitosis. Cell Mol Life Sci 63: 781–795. 16465440

10. Ma HT, Poon RY (2011) How protein kinases co-ordinate mitosis in animal cells. Biochem J 435: 17–31. doi: 10.1042/BJ20100284 21406064

11. Nigg EA (2001) Mitotic kinases as regulators of cell division and its checkpoints. Nat Rev Mol Cell Biol 2: 21–32. 11413462

12. Schmit TL, Ahmad N (2007) Regulation of mitosis via mitotic kinases: new opportunities for cancer management. Mol Cancer Ther 6: 1920–1931. 17620424

13. Saiz JE, Fisher RP (2002) A CDK-activating kinase network is required in cell cycle control and transcription in fission yeast. Curr Biol 12: 1100–1105. 12121616

14. Espinoza FH, Farrell A, Erdjument-Bromage H, Tempst P, Morgan DO (1996) A cyclin-dependent kinase-activating kinase (CAK) in budding yeast unrelated to vertebrate CAK. Science 273: 1714–1717. 8781234

15. Park G, Servin JA, Turner GE, Altamirano L, Colot HV, et al. (2011) Global analysis of serine-threonine protein kinase genes in Neurospora crassa. Eukaryot Cell 10: 1553–1564. doi: 10.1128/EC.05140-11 21965514

16. De Souza CP, Hashmi SB, Osmani AH, Andrews P, Ringelberg CS, et al. (2013) Functional analysis of the Aspergillus nidulans kinome. PLoS One 8: e58008. doi: 10.1371/journal.pone.0058008 23505451

17. Osmani AH, van Peij N, Mischke M, O'Connell MJ, Osmani SA (1994) A single p34cdc2 protein kinase (encoded by nimXcdc2) is required at G1 and G2 in Aspergillus nidulans. J Cell Sci 107 (Pt 6): 1519–1528. 7962194

18. Borkovich KA, Alex LA, Yarden O, Freitag M, Turner GE, et al. (2004) Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol Mol Biol Rev 68: 1–108. 15007097

19. Wang C, Zhang S, Hou R, Zhao Z, Zheng Q, et al. (2011) Functional analysis of the kinome of the wheat scab fungus Fusarium graminearum. PLoS Pathog 7: e1002460. doi: 10.1371/journal.ppat.1002460 22216007

20. Tsuchiy D, Lacefield S (2013) Cdk1 modulation ensures the coordination of cell-cycle events during the switch from meiotic prophase to mitosis. Current Biology 23: 1505–1513. doi: 10.1016/j.cub.2013.06.031 23871241

21. Proctor RH, Hohn TM, McCormick SP. Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol Plant Microbe Interact. 1995;8(4):593–601. Epub 1995/07/01. 8589414.

22. Seo JA, Kim JC, Lee DH, Lee YW. Variation in 8-ketotrichothecenes and zearalenone production by Fusarium graminearum isolates from corn and barley in Korea. Mycopathologia. 1996;134(1):31–7. doi: 10.1007/Bf00437050 20882466

23. Gardiner DM, Kazan K, Manners JM. Nutrient profiling reveals potent inducers of trichothecene biosynthesis in Fusarium graminearum. Fungal Genetics and Biology. 2009;46(8):604–13. doi: 10.1016/j.fgb.2009.04.004 19406250

24. Zhang XW, Jia LJ, Zhang Y, Jiang G, Li X, et al. (2012) In planta stage-specific fungal gene profiling elucidates the molecular strategies of Fusarium graminearum growing inside wheat coleoptiles. Plant Cell 24: 5159–5176. doi: 10.1105/tpc.112.105957 23266949

25. Gu X (2006) A simple statistical method for estimating type-II (cluster-specific) functional divergence of protein sequences. Mol Biol Evol 23: 1937–1945. 16864604

26. Gu X (1999) Statistical methods for testing functional divergence after gene duplication. Mol Biol Evol 16: 1664–1674. 10605109

27. 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. 14685274

28. Sgarlata C, Perez-Martin J (2005) Inhibitory phosphorylation of a mitotic cyclin-dependent kinase regulates the morphogenesis, cell size and virulence of the smut fungus Ustilago maydis. J Cell Sci 118: 3607–3622. 16046476

29. 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. 8253069

30. Norbury C, Blow J, Nurse P (1991) Regulatory phosphorylation of the p34cdc2 protein kinase in vertebrates. EMBO J 10: 3321–3329. 1655417

31. Kaldis P, Pitluk ZW, Bany IA, Enke DA, Wagner M, Winter E, et al. Localization and regulation of the cdk-activating kinase (Cak1p) from budding yeast. J Cell Sci. 1998;111 (Pt 24):3585–96. Epub 1998/11/20. 9819350.

32. Kaldis P. The cdk-activating kinase (CAK): from yeast to mammals. Cell Mol Life Sci. 1999;55(2):284–96. Epub 1999/04/03. 10188587.

33. Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, et al. (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464: 367–373. doi: 10.1038/nature08850 20237561

34. Coleman JJ, Rounsley SD, Rodriguez-Carres M, Kuo A, Wasmann CC, et al. (2009) The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet 5: e1000618. doi: 10.1371/journal.pgen.1000618 19714214

35. Conant GC, Wolfe KH (2008) Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 9: 938–950. doi: 10.1038/nrg2482 19015656

36. Presser A, Elowitz MB, Kellis M, Kishony R (2008) The evolutionary dynamics of the Saccharomyces cerevisiae protein interaction network after duplication. Proc Natl Acad Sci U S A 105: 950–954. doi: 10.1073/pnas.0707293105 18199840

37. Son H, Lee J, Lee Y-W (2013) A novel gene, GEA1, is required for ascus cell-wall development in the ascomycete fungus Fusarium graminearum. Microbiology 159: 1077–1085. doi: 10.1099/mic.0.064287-0 23619001

38. Son H, Seo YS, Min K, Park AR, Lee J, et al. (2011) A phenome-based functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathog 7: e1002310. doi: 10.1371/journal.ppat.1002310 22028654

39. Hou Z, Xue C, Peng Y, Katan T, Kistler HC, et al. (2002) A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol Plant Microbe Interact 15: 1119–1127. 12423017

40. Wang Y, Liu W, Hou Z, Wang C, Zhou X, et al. (2011) A novel transcriptional factor important for pathogenesis and ascosporogenesis in Fusarium graminearum. Mol Plant Microbe Interact 24: 118–128. doi: 10.1094/MPMI-06-10-0129 20795857

41. Zheng Q, Hou R, Juanyu, Zhang, Ma J, et al. (2013) The MAT locus genes play different roles in sexual reproduction and pathogenesis in Fusarium graminearum. PLoS One 8: e66980. doi: 10.1371/journal.pone.0066980 23826182

42. Harvey SL, Charlet A, Haas W, Gygi SP, Kellogg DR (2005) Cdk1-dependent regulation of the mitotic inhibitor Wee1. Cell 122: 407–420. 16096060

43. Perez-Martin J, Castillo-Lluva S, Sgarlata C, Flor-Parra I, Mielnichuk N, et al. (2006) Pathocycles: Ustilago maydis as a model to study the relationships between cell cycle and virulence in pathogenic fungi. Mol Genet Genomics 276: 211–229. 16896795

44. Saunders DG, Aves SJ, Talbot NJ (2010) Cell cycle-mediated regulation of plant infection by the rice blast fungus. Plant Cell 22: 497–507. doi: 10.1105/tpc.109.072447 20190078

45. Veneault-Fourrey C, Barooah M, Egan M, Wakley G, Talbot NJ (2006) Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science 312: 580–583. 16645096

46. Bourett TM, Howard RJ (1990) In vitro development of penetration structures in the rice blast fungus Magnaporthe grisea. Canadian Journal of Botany 68: 329–342.

47. Rittenour WR, Harris SD (2010) An in vitro method for the analysis of infection-related morphogenesis in Fusarium graminearum. Mol Plant Pathol 11: 361–369. doi: 10.1111/j.1364-3703.2010.00609.x 20447284

48. Booher RN, Alfa CE, Hyams JS, Beach DH (1989) The fission yeast cdc2/cdc13/suc1 protein kinase: regulation of catalytic activity and nuclear localization. Cell 58: 485. 2569363

49. Wittenberg C, Richardson SL, Reed SI (1987) Subcellular localization of a protein kinase required for cell cycle initiation in Saccharomyces cerevisiae: evidence for an association between the CDC28 gene product and the insoluble cytoplasmic matrix. J Cell Biol 105: 1527–1538. 3312233

50. Wu L, Osmani SA, Mirabito PM (1998) A role for NIMA in the nuclear localization of cyclin B in Aspergillus nidulans. J Cell Biol 141: 1575–1587. 9647650

51. Bordon-Pallier F, Jullian N, Ferrari P, Girard AM, Bocquel MT, et al. (2004) Inhibitors of Civ1 kinase belonging to 6-aminoaromatic-2-cyclohexyldiamino purine series as potent anti-fungal compounds. Biochim Biophys Acta 1697: 211–223. 15023362

52. Oconnell MJ, Osmani AH, Morris NR, Osmani SA. An Extra Copy of Nimecyclinb Elevates Pre-Mpf Levels and Partially Suppresses Mutation of Nimtcdc25 in Aspergillus-Nidulans. Embo Journal. 1992;11(6):2139–49. 1534750

53. Carmena M, Earnshaw WC (2003) The cellular geography of aurora kinases. Nat Rev Mol Cell Biol 4: 842–854. 14625535

54. Chan CS, Botstein D (1993) Isolation and characterization of chromosome-gain and increase-in-ploidy mutants in yeast. Genetics 135: 677–691. 8293973

55. Petersen J, Paris J, Willer M, Philippe M, Hagan IM (2001) The S. pombe aurora-related kinase Ark1 associates with mitotic structures in a stage dependent manner and is required for chromosome segregation. J Cell Sci 114: 4371–4384. 11792803

56. Leverson JD, Huang HK, Forsburg SL, Hunter T (2002) The Schizosaccharomyces pombe aurora-related kinase Ark1 interacts with the inner centromere protein Pic1 and mediates chromosome segregation and cytokinesis. Mol Biol Cell 13: 1132–1143. 11950927

57. Marumoto T, Zhang D, Saya H (2005) Aurora-A—a guardian of poles. Nat Rev Cancer 5: 42–50. 15630414

58. Barr AR, Gergely F (2007) Aurora-A: the maker and breaker of spindle poles. J Cell Sci 120: 2987–2996. 17715155

59. Vader G, Medema RH, Lens SM (2006) The chromosomal passenger complex: guiding Aurora-B through mitosis. J Cell Biol 173: 833–837. 16769825

60. Ruchaud S, Carmena M, Earnshaw WC (2007) Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 8: 798–812. 17848966

61. Fu J, Bian M, Liu J, Jiang Q, Zhang C (2009) A single amino acid change converts Aurora-A into Aurora-B-like kinase in terms of partner specificity and cellular function. Proc Natl Acad Sci U S A 106: 6939–6944. doi: 10.1073/pnas.0900833106 19357306

62. Schweitzer B, Philippsen P (1992) NPK1, a nonessential protein kinase gene in Saccharomyces cerevisiae with similarity to Aspergillus nidulans nimA. Mol Gen Genet 234: 164–167. 1495480

63. Leslie JF, and Summerell B. A.. (2006) The Fusarium laboratory manual: Blackwell Publishing, Ames, IA.

64. Zheng D, Zhang S, Zhou X, Wang C, Xiang P, et al. (2012) The FgHOG1 pathway regulates hyphal growth, stress responses, and plant infection in Fusarium graminearum. PLoS One 7: e49495. doi: 10.1371/journal.pone.0049495 23166686

65. Bluhm BH, Zhao X, Flaherty JE, Xu JR, Dunkle LD (2007) RAS2 regulates growth and pathogenesis in Fusarium graminearum. Mol Plant Microbe Interact 20: 627–636. 17555271

66. Wang G, Wang C, Hou R, Zhou X, Li G, et al. (2012) The AMT1 arginine methyltransferase gene is important for plant infection and normal hyphal growth in Fusarium graminearum. PLoS One 7: e38324. doi: 10.1371/journal.pone.0038324 22693618

67. Bruno KS, Tenjo F, Li L, Hamer JE, Xu JR (2004) Cellular localization and role of kinase activity of PMK1 in Magnaporthe grisea. Eukaryot Cell 3: 1525–1532. 15590826

68. Zhou X, Xu JR (2011) Efficient approaches for generating GFP fusion and epitope-tagging constructs in filamentous fungi. In: Xu JR, Bluhm B, editors. Fungal Genomics: Methods and Protocols. Heidelberg: Humana Press. pp. 199–212.

69. Hu S, Zhou X, Gu X, Cao S, Wang C, et al. (2014) The cAMP-PKA pathway regulates growth, sexual and asexual differentiation, and pathogenesis in Fusarium graminearum. Mol Plant Microbe Interact 27: 557–566. doi: 10.1094/MPMI-10-13-0306-R 24450772

70. Zhou X, Zhang H, Li G, Shaw B, Xu JR (2012) The Cyclase-associated protein Cap1 is important for proper regulation of infection-related morphogenesis in Magnaporthe oryzae. PLoS Pathog 8: e1002911. doi: 10.1371/journal.ppat.1002911 22969430

71. Zhou X, Liu W, Wang C, Xu Q, Wang Y, et al. (2011) A MADS-box transcription factor MoMcm1 is required for male fertility, microconidium production and virulence in Magnaporthe oryzae. Mol Microbiol 80: 33–53. doi: 10.1111/j.1365-2958.2011.07556.x 21276092

72. Liu W, Zhou X, Li G, Li L, Kong L, et al. (2011) Multiple plant surface signals are sensed by different mechanisms in the rice blast fungus for appressorium formation. PLoS Pathog 7: e1001261. doi: 10.1371/journal.ppat.1001261 21283781

73. Gu X, Zou Y, Su Z, Huang W, Zhou Z, et al. (2013) An update of DIVERGE software for functional divergence analysis of protein family. Mol Biol Evol 30: 1713–1719. doi: 10.1093/molbev/mst069 23589455

74. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307–321. doi: 10.1093/sysbio/syq010 20525638

75. Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104–2105. 15647292

76. Cuomo CA, Guldener U, Xu JR, Trail F, Turgeon BG, et al. (2007) The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317: 1400–1402. 17823352