Identification of Meiotic Cyclins Reveals Functional Diversification among Plant Cyclin Genes

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Meiosis is a modified cell division in which a single S-phase is followed by two rounds of chromosome segregation resulting in the production of haploid gametes. The meiotic mode of chromosome segregation requires extensive remodeling of the basic cell cycle machinery and employment of unique regulatory mechanisms. Cyclin-dependent kinases (CDKs) and cyclins represent an ancient molecular module that drives and regulates cell cycle progression. The cyclin gene family has undergone a massive expansion in angiosperm plants, but only a few cyclins were thoroughly characterized. In this study we performed a systematic immunolocalization screen to identify Arabidopsis thaliana A- and B-type cyclins expressed in meiosis. Many of these cyclins exhibit cell-type-specific expression in vegetative tissues and distinct subcellular localization. We found six A-type cyclins and a single B-type cyclin (CYCB3;1) to be expressed in male meiosis. Mutant analysis revealed that these cyclins contribute to distinct meiosis-related processes. While A2 cyclins are important for chromosome segregation, CYCB3;1 prevents ectopic cell wall formation. We further show that cyclin SDS does not contain a D-box and is constitutively expressed throughout meiosis. Analysis of plants carrying cyclin SDS with an introduced D-box motif determined that, in addition to its function in recombination, SDS acts together with CYCB3;1 in suppressing unscheduled cell wall synthesis. Our phenotypic and expression data provide extensive evidence that multiplication of cyclins is in plants accompanied by functional diversification.

Vyšlo v časopise: Identification of Meiotic Cyclins Reveals Functional Diversification among Plant Cyclin Genes. PLoS Genet 9(5): e32767. doi:10.1371/journal.pgen.1003508
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003508

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Zdroje

1. PetronczkiM, SiomosMF, NasmythK (2003) Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112: 423–440.

2. MarstonAL, AmonA (2004) Meiosis: cell-cycle controls shuffle and deal. Nat Rev Mol Cell Biol 5: 983–997.

3. van WervenFJ, AmonA (2011) Regulation of entry into gametogenesis. Philos Trans R Soc Lond B Biol Sci 366: 3521–3531.

4. KimbleJ (2011) Molecular regulation of the mitosis/meiosis decision in multicellular organisms. Cold Spring Harb Perspect Biol 3: a002683.

5. MaH (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56: 393–434.

6. YangWC, ShiDQ, ChenYH (2010) Female gametophyte development in flowering plants. Annu Rev Plant Biol 61: 89–108.

7. EdlingerB, SchlogelhoferP (2011) Have a break: determinants of meiotic DNA double strand break (DSB) formation and processing in plants. J Exp Bot 62: 1545–1563.

8. ArmstrongSJ, JonesGH (2003) Meiotic cytology and chromosome behaviour in wild-type Arabidopsis thaliana. J Exp Bot 54: 1–10.

9. OsmanK, HigginsJD, Sanchez-MoranE, ArmstrongSJ, FranklinFC (2011) Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol 190: 523–544.

10. HamantO, MaH, CandeWZ (2006) Genetics of Meiotic Prophase I in Plants. Annu Rev Plant Biol 57: 267–302.

11. MercierR, GrelonM (2008) Meiosis in plants: ten years of gene discovery. Cytogenet Genome Res 120: 281–290.

12. MercierR, VezonD, BullierE, MotamayorJC, SellierA, et al. (2001) SWITCH1 (SWI1): a novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis. Genes Dev 15: 1859–1871.

13. PawlowskiWP, WangCJ, GolubovskayaIN, SzymaniakJM, ShiL, et al. (2009) Maize AMEIOTIC1 is essential for multiple early meiotic processes and likely required for the initiation of meiosis. Proc Natl Acad Sci U S A 106: 3603–3608.

14. CromerL, HeymanJ, TouatiS, HarashimaH, AraouE, et al. (2012) OSD1 promotes meiotic progression via APC/C inhibition and forms a regulatory network with TDM and CYCA1;2/TAM. PLoS Genet 8: e1002865 doi:10.1371/journal.pgen.1002865.

15. d'ErfurthI, JolivetS, FrogerN, CatriceO, NovatchkovaM, et al. (2009) Turning meiosis into mitosis. PLoS Biol 7: e1000124 doi:10.1371/journal.pbio.1000124.

16. RossKJ, FranszP, ArmstrongSJ, VizirI, MulliganB, et al. (1997) Cytological characterization of four meiotic mutants of Arabidopsis isolated from T-DNA-transformed lines. Chromosome Res 5: 551–559.

17. GloverJ, GrelonM, CraigS, ChaudhuryA, DennisE (1998) Cloning and characterization of MS5 from Arabidopsis: a gene critical in male meiosis. Plant J 15: 345–356.

18. RiehsN, AkimchevaS, PuizinaJ, BulankovaP, IdolRA, et al. (2008) Arabidopsis SMG7 protein is required for exit from meiosis. J Cell Sci 121: 2208–2216.

19. BulankovaP, Riehs-KearnanN, NowackMK, SchnittgerA, RihaK (2010) Meiotic progression in Arabidopsis is governed by complex regulatory interactions between SMG7, TDM1, and the meiosis I-specific cyclin TAM. Plant Cell 22: 3791–3803.

20. ErricoA, DeshmukhK, TanakaY, PozniakovskyA, HuntT (2010) Identification of substrates for cyclin dependent kinases. Adv Enzyme Regul 50: 375–399.

21. BloomJ, CrossFR (2007) Multiple levels of cyclin specificity in cell-cycle control. Nat Rev Mol Cell Biol 8: 149–160.

22. WolgemuthDJ, RobertsSS (2010) Regulating mitosis and meiosis in the male germ line: critical functions for cyclins. Philos Trans R Soc Lond B Biol Sci 365: 1653–1662.

23. YokooR, ZawadzkiKA, NabeshimaK, DrakeM, ArurS, et al. (2012) COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell 149: 75–87.

24. CarlileTM, AmonA (2008) Meiosis I is established through division-specific translational control of a cyclin. Cell 133: 280–291.

25. AzumiY, LiuD, ZhaoD, LiW, WangG, et al. (2002) Homolog interaction during meiotic prophase I in Arabidopsis requires the SOLO DANCERS gene encoding a novel cyclin-like protein. Embo J 21: 3081–3095.

26. ChangL, MaH, XueHW (2009) Functional conservation of the meiotic genes SDS and RCK in male meiosis in the monocot rice. Cell Res 19: 768–782.

27. De MuytA, PereiraL, VezonD, ChelyshevaL, GendrotG, et al. (2009) A high throughput genetic screen identifies new early meiotic recombination functions in Arabidopsis thaliana. PLoS Genet 5: e1000654 doi:10.1371/journal.pgen.1000654.

28. WangY, MagnardJL, McCormickS, YangM (2004) Progression through meiosis I and meiosis II in Arabidopsis anthers is regulated by an A-type cyclin predominately expressed in prophase I. Plant Physiol 136: 4127–4135.

29. d'ErfurthI, CromerL, JolivetS, GirardC, HorlowC, et al. (2010) The cyclin-A CYCA1;2/TAM is required for the meiosis I to meiosis II transition and cooperates with OSD1 for the prophase to first meiotic division transition. PLoS Genet 6: e1000989 doi:10.1371/journal.pgen.1000989.

30. WangG, KongH, SunY, ZhangX, ZhangW, et al. (2004) Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Plant Physiol 135: 1084–1099.

31. VandepoeleK, RaesJ, De VeylderL, RouzeP, RombautsS, et al. (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14: 903–916.

32. GuoJ, SongJ, WangF, ZhangXS (2007) Genome-wide identification and expression analysis of rice cell cycle genes. Plant Mol Biol 64: 349–360.

33. HuX, ChengX, JiangH, ZhuS, ChengB, et al. (2010) Genome-wide analysis of cyclins in maize (Zea mays). Genet Mol Res 9: 1490–1503.

34. CriquiMC, WeingartnerM, CapronA, ParmentierY, ShenWH, et al. (2001) Sub-cellular localisation of GFP-tagged tobacco mitotic cyclins during the cell cycle and after spindle checkpoint activation. Plant J 28: 569–581.

35. BorucJ, MylleE, DudaM, De ClercqR, RombautsS, et al. (2010) Systematic localization of the Arabidopsis core cell cycle proteins reveals novel cell division complexes. Plant Physiol 152: 553–565.

36. Colon-CarmonaA, YouR, Haimovitch-GalT, DoernerP (1999) Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20: 503–508.

37. VannesteS, CoppensF, LeeE, DonnerTJ, XieZ, et al. (2011) Developmental regulation of CYCA2s contributes to tissue-specific proliferation in Arabidopsis. EMBO J 30: 3430–3441.

38. CoudreuseD, NurseP (2010) Driving the cell cycle with a minimal CDK control network. Nature 468: 1074–1079.

39. InzeD, De VeylderL (2006) Cell cycle regulation in plant development. Annu Rev Genet 40: 77–105.

40. SozzaniR, CuiH, Moreno-RisuenoMA, BuschW, Van NormanJM, et al. (2010) Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth. Nature 466: 128–132.

41. ImaiKK, OhashiY, TsugeT, YoshizumiT, MatsuiM, et al. (2006) The A-type cyclin CYCA2;3 is a key regulator of ploidy levels in Arabidopsis endoreduplication. Plant Cell 18: 382–396.

42. WooRA, PoonRY (2003) Cyclin-dependent kinases and S phase control in mammalian cells. Cell Cycle 2: 316–324.

43. BoudolfV, LammensT, BorucJ, Van LeeneJ, Van Den DaeleH, et al. (2009) CDKB1;1 forms a functional complex with CYCA2;3 to suppress endocycle onset. Plant Physiol 150: 1482–1493.

44. YuY, SteinmetzA, MeyerD, BrownS, ShenWH (2003) The tobacco A-type cyclin, Nicta;CYCA3;2, at the nexus of cell division and differentiation. Plant Cell 15: 2763–2777.

45. TakahashiI, KojimaS, SakaguchiN, Umeda-HaraC, UmedaM (2010) Two Arabidopsis cyclin A3s possess G1 cyclin-like features. Plant Cell Rep 29: 307–315.

46. BorucJ, Van den DaeleH, HollunderJ, RombautsS, MylleE, et al. (2010) Functional modules in the Arabidopsis core cell cycle binary protein-protein interaction network. Plant Cell 22: 1264–1280.

47. CrossFR, BuchlerNE, SkotheimJM (2011) Evolution of networks and sequences in eukaryotic cell cycle control. Philos Trans R Soc Lond B Biol Sci 366: 3532–3544.

48. BentleyAM, NormandG, HoytJ, KingRW (2007) Distinct sequence elements of cyclin B1 promote localization to chromatin, centrosomes, and kinetochores during mitosis. Mol Biol Cell 18: 4847–4858.

49. TouatiSA, CladiereD, ListerLM, LeontiouI, ChambonJP, et al. (2012) Cyclin A2 Is Required for Sister Chromatid Segregation, But Not Separase Control, in Mouse Oocyte Meiosis. Cell Rep 2: 1077–87.

50. OteguiMS, StaehelinLA (2004) Electron tomographic analysis of post-meiotic cytokinesis during pollen development in Arabidopsis thaliana. Planta 218: 501–515.

51. OteguiM, StaehelinLA (2000) Cytokinesis in flowering plants: more than one way to divide a cell. Curr Opin Plant Biol 3: 493–502.

52. HushJ, WuL, JohnPC, HeplerLH, HeplerPK (1996) Plant mitosis promoting factor disassembles the microtubule preprophase band and accelerates prophase progression in Tradescantia. Cell Biol Int 20: 275–287.

53. SasabeM, BoudolfV, De VeylderL, InzeD, GenschikP, et al. (2011) Phosphorylation of a mitotic kinesin-like protein and a MAPKKK by cyclin-dependent kinases (CDKs) is involved in the transition to cytokinesis in plants. Proc Natl Acad Sci U S A 108: 17844–17849.

54. YangCY, SpielmanM, ColesJP, LiY, GhelaniS, et al. (2003) TETRASPORE encodes a kinesin required for male meiotic cytokinesis in Arabidopsis. Plant J 34: 229–240.

55. KatisVL, LippJJ, ImreR, BogdanovaA, OkazE, et al. (2010) Rec8 phosphorylation by casein kinase 1 and Cdc7-Dbf4 kinase regulates cohesin cleavage by separase during meiosis. Dev Cell 18: 397–409.

56. GutierrezGJ, VogtlinA, CastroA, FerbyI, SalvagiottoG, et al. (2006) Meiotic regulation of the CDK activator RINGO/Speedy by ubiquitin-proteasome-mediated processing and degradation. Nat Cell Biol 8: 1084–1094.

57. ChenZ, HigginsJD, HuiJT, LiJ, FranklinFC, et al. (2011) Retinoblastoma protein is essential for early meiotic events in Arabidopsis. EMBO J 30: 744–755.

58. GunbinKV, SuslovVV, TurnaevII, AfonnikovDA, KolchanovNA (2011) Molecular evolution of cyclin proteins in animals and fungi. BMC Evol Biol 11: 224.

59. SterkenR, KiekensR, CoppensE, VercauterenI, ZabeauM, et al. (2009) A population genomics study of the Arabidopsis core cell cycle genes shows the signature of natural selection. Plant Cell 21: 2987–2998.

60. CurtisMD, GrossniklausU (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133: 462–469.

61. HadiMZ, KemperE, WendelerE, ReissB (2002) Simple and versatile selection of Arabidopsis transformants. Plant Cell Rep 21: 130–135.

62. JeffersonRA, KavanaghTA, BevanMW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. Embo J 6: 3901–3907.

63. AlexanderMP (1969) Differential staining of aborted and nonaborted pollen. Stain Technology 44: 117–122.

64. OwenHA, MakaroffCA (1995) Ultrastructure of microsporogenesis and microgametogenesis in Arabidopsis thaliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae). Protoplasma 185: 7–21.