Advertisement

Plant Molecular Biology

, Volume 62, Issue 1–2, pp 99–110 | Cite as

ASK1, a SKP1 homolog, is required for nuclear reorganization, presynaptic homolog juxtaposition and the proper distribution of cohesin during meiosis in Arabidopsis

  • Dazhong Zhao
  • Xiaohui Yang
  • Li Quan
  • Ljudmilla Timofejeva
  • Nathan W. Rigel
  • Hong MaEmail author
  • Christopher A. MakaroffEmail author
Article

Abstract

Nuclear reorganization and juxtaposition of homologous chromosomes at late leptotene/early zygotene are essential steps before chromosome synapsis at pachytene. We report the results of detailed studies, which demonstrate that nuclear reorganization and homolog juxtapositioning processes are defective in a null mutant, ask1-1. Our results from 4, 6-diamino-2-phenylindole (DAPI)-stained spreads showed that the “synizetic knot”, which is typically found in wild type (WT) meiosis during late leptotene and zygotene, was missing in the ask1-1 mutant. Furthermore, ask1-1 meiocytes exhibited only limited homolog juxtaposition at centromere regions at early zygotene. Immunodetection of the cohesin protein SYN1 identified ask1 defects in cohesin distribution from zygotene to anaphase I. Analysis of meiotic chromosomes in ask1-1 and syn1 single mutants, as well as an ask1-1 syn1 double mutant indicate that ASK1 is required for normal SYN1 distribution during meiotic prophase I and suggest that ask1 associated defects may be primarily related to SYN1 mislocalization.

Keywords

Arabidopsis thaliana ASK1 Homolog juxtaposition Meiosis SYN1 synizetic knot Cohesin Synapsis 

Abbreviations

AE

axial element

CE

central element

DAPI

4, 6-diamino-2-phenylindole

LEs

lateral elements

SC

synaptonemal complex

TEM

transmission electron microscopy

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

We thank A. Omeis and J. Wang for plant care. We also thank E. Harris and M. Henry for their help with the identification of the ask1-1 syn1 double mutant plants. We are grateful for comments on this manuscript from C. Chen, W. Li, L. Harper, W. Ni, G. Wang, L.M. Zahn, W. Zhang, and M. Zolan. This work was supported by grants from the National Science Foundation [MCB-0092075 (HM); MCB-0322171 (CAM)], the National Institutes of Health [RO1 GM63871 (HM)], and the Department of Energy [DE-FG02-02ER15332 (HM and DZ)] and by funds from the Department of Biology and the Huck Institutes of the Life Sciences at the Pennsylvania State University. H.M. gratefully acknowledges the support of the John Simon Guggenheim Memorial Foundation.

References

  1. Armstrong S, Franklin F, Jones G (2001) Nucleolus-associated telomere clustering and pairing preceed meiotic chromosome synapsis in Arabidopsis thaliana. J Cell Sci 114:4207–04217PubMedGoogle Scholar
  2. Azumi Y, Liu D, Zhao D, Li W, Wang G, Hu Y, Ma H (2002) Homolog interaction during meiotic prophase I in Arabidopsis requires the SOLO DANCERS gene encoding a novel cyclin-like protein. EMBO J 21:3081–3095PubMedCrossRefGoogle Scholar
  3. Bai C, Sen P, Hofmann K, Ma L, Goebl M, Harper JW, Elledge SJ (1996) Skp1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 86:263–274PubMedCrossRefGoogle Scholar
  4. Bai X, Peirson B, Dong F, Cai X, Makaroff C (1999) Isolation and characterization of SYN1, a Rad21-like gene essential for meiosis in Arabidopsis. Plant Cell 11:417–430PubMedCrossRefGoogle Scholar
  5. Bass HW, Marshall WF, Sedat JW, Agard DA, Cande WZ (1997) Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase. J Cell Biol 137:5–18PubMedCrossRefGoogle Scholar
  6. Bass HW, RieraLizarazu O, Ananiev EV, Bordoli SJ, Rines HW, Phillips RL, Sedat JW, Agard DA, Cande WZ (2000) Evidence for the coincident initiation of homolog pairing and synapsis during the telomere-clustering (bouquet) stage of meiotic prophase. J Cell Sci 113:1033–1042PubMedGoogle Scholar
  7. Bhatt AM, Lister C, Page T, Fransz P, Findlay K, Jones GH, Dickinson HG, Dean C (1999) The Dif1 gene of Arabidopsis is required for meiotic chromosome segregation and belongs to the Rec8/Rad21 cohesin gene family. Plant J 19:463–472PubMedCrossRefGoogle Scholar
  8. Bleuyard JY, White CI (2004) The Arabidopsis homologue of Xrcc3 plays an essential role in meiosis. EMBO J 23:439–449PubMedCrossRefGoogle Scholar
  9. Blumenthal SSD, Clark GB, Roux SJ (2004) Biochemical and immunological characterization of pea nuclear intermediate filament proteins. Planta 218:965–975PubMedCrossRefGoogle Scholar
  10. Brandizzi F, Irons SL, Evans DE (2004) The plant nuclear envelope: new prospects for a poorly understood structure. New Phyt 163:227–246CrossRefGoogle Scholar
  11. Bundock P, Hooykaas P (2002) Severe developmental defects, hypersensitivity to DNA-damaging agents, and lengthened telomeres in Arabidopsis mre11 mutants. Plant Cell 14:2451–2462PubMedCrossRefGoogle Scholar
  12. Cai X, Dong FG, Edelmann RE, Makaroff CA (2003) The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing. J Cell Sci 116:2999–3007PubMedCrossRefGoogle Scholar
  13. Caryl AP, Armstrong SJ, Jones GH, Franklin FCH (2000) A homologue of the yeast Hop1 gene is inactivated in the Arabidopsis meiotic mutant asy1. Chromosoma 109:62–71PubMedCrossRefGoogle Scholar
  14. Chen CB, Zhang W, Timofejeva L, Gerardin Y, Ma H (2005) The Arabidopsis ROCK-N-ROLLERS gene encodes a homolog of the yeast ATP-dependent DNA helicase Mer3 and is required for normal meiotic crossover formation. Plant J 43:321–334PubMedCrossRefGoogle Scholar
  15. Connelly C, Hieter P (1996) Budding yeast Skp1 encodes an evolutionarily conserved kinetochore protein required for cell cycle progression. Cell 86:275–285PubMedCrossRefGoogle Scholar
  16. Couteau F, Belzile F, Horlow C, Grandjean O, Vezon D, Doutriaux MP (1999) Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. Plant Cell 11:1623–1634PubMedCrossRefGoogle Scholar
  17. Cowan CR, Carlton PM, Cande WZ (2001) The polar arrangement of telomeres in interphase and meiosis. Rab1 organization and the bouquet. Plant Physiol 125:532–538PubMedCrossRefGoogle Scholar
  18. Dawe RK (1998) Meiotic chromosome organization and segregation in plants. Annu Rev Plant Physiol Plant Mol Biol 49:371–395PubMedCrossRefGoogle Scholar
  19. de la Espina SMD (1995) Nuclear matrix isolated from plant cells. Int Rev Cytol 162:75–139Google Scholar
  20. Doutriaux MP, Couteau F, Bergounioux C, White C (1998) Isolation and characterisation of the Rad51 and Dmc1 homologs from Arabidopsis thaliana. Mol Gen Genet 257:283–291PubMedCrossRefGoogle Scholar
  21. Enenkel C, Lehmann A, Kloetzel PM (1999) GFP-labelling of 26s proteasomes in living yeast: insight into proteasomal functions at the nuclear envelope. Mol Biol Rep 26:131–135PubMedCrossRefGoogle Scholar
  22. Feldman RM, Correll CC, Kaplan KB, Deshaies RJ (1997) A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated cdk inhibitor Sic1p. Cell 91:221–230PubMedCrossRefGoogle Scholar
  23. Fransz P, Alonso-Blanco C, Liharska TB, Peeters AJM, Zabel P, de Jung J (1996) High resolution physical mapping in Arabidopsis thaliana and tomato by fluorescence in situ hybridization to extended DNA fibers. Plant J 9:421–430PubMedCrossRefGoogle Scholar
  24. Fransz P, Armstrong S, AlonsoBlanco C, Fischer TC, TorresRuiz RA, Jones G (1998) Cytogenetics for the model system Arabidopsis thaliana. Plant J 13:867–876PubMedCrossRefGoogle Scholar
  25. Gallego ME, Jeanneau M, Granier F, Bouchez D, Bechtold N, White CI (2001) Disruption of the Arabidopsis Rad50 gene leads to plant sterility and mms sensitivity. Plant J 25:31–41PubMedCrossRefGoogle Scholar
  26. Gindullis F, Rose A, Patel S, Meier I (2002) Four signature motifs define the first class of structurally related large coiled-coil proteins in plants. BMC Gen 3:9–15CrossRefGoogle Scholar
  27. Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSpo11–1 is necessary for efficient meiotic recombination in plants. EMBO J 20:589–600PubMedCrossRefGoogle Scholar
  28. Hartung F, Puchta H (2000) Molecular characterisation of two paralogous Spo11 homologues in Arabidopsis thaliana. Nucl Acid Res 28:1548–1554CrossRefGoogle Scholar
  29. Hershko A, Ciechanover A (1998) The ubiquitin system. Ann Rev Biochem 67:425–479PubMedCrossRefGoogle Scholar
  30. Higgins JD, Armstrong SJ, Franklin FCH, Jones GH (2004) The Arabidopsis MutS homolog AtMsh4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev 18:2557–2570PubMedCrossRefGoogle Scholar
  31. Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FCH (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19:2488–2500PubMedCrossRefGoogle Scholar
  32. Li WX, Yang XH, Lin ZG, Timofejeva L, Xiao R, Makaroff CA, Ma H (2005) The AtRad51c gene is required for normal meiotic chromosome synapsis and double-stranded break repair in Arabidopsis. Plant Physiol 138:965–976CrossRefGoogle Scholar
  33. Loidl J (1990) The initiation of meiotic chromosomes pairing: the cytological view. Genome 33:759–778PubMedGoogle Scholar
  34. Martinez-Perez E, Shaw P, Reader S, Aragon-Alcaide L, Miller T, Moore G (1999) Homologous chromosome pairing in wheat. J Cell Sci 112:1761–1769PubMedGoogle Scholar
  35. Martinez-Zapater JM, Estelle MA, Somerville CR (1986) A highly repeated DNA sequence in Arabidopsis thaliana. Mol Gen Genet 204:417–423CrossRefGoogle Scholar
  36. Masuda K, Xu ZJ, Takahashi S, Ito A, Ono M, Nomura K, Inoue M (1997) Peripheral framework of carrot cell nucleus contains a novel protein predicted to exhibit a long alpha-helical domain. Exp Cell Res 232:173–181PubMedCrossRefGoogle Scholar
  37. Mattout-Drubezki A, Gruenbaum Y (2003) Dynamic interactions of nuclear lamina proteins with chromatin and transcriptional machinery. Cell Mol Life Sci 60:2053–2063PubMedCrossRefGoogle Scholar
  38. Mercier R, Jolivet S, Vezon D, Huppe E, Chelysheva L, Giovanni M, Nogue F, Doutriaux MP, Horlow C, Grelon M, Mezard C (2005) Two meiotic crossover classes cohabit in Arabidopsis: one is dependent on Mer3, whereas the other one is not. Curr Biol 15:692–701PubMedCrossRefGoogle Scholar
  39. Nayak S, Santiago FE, Jin H, Lin D, Schedl T, Kipreos ET (2002) The Caenorhabditis elegans Skp1-related gene family: diverse functions in cell proliferation, morphogenesis, and meiosis. Curr Biol 12:277–287PubMedCrossRefGoogle Scholar
  40. Owen HA, Makaroff CA (1995) Ultrastructure of microsporogenesis and microgametogenesis in Arabidopsis thaliana (l) heynh ecotype wassilewskija (Brassicaceae). Protoplasma 185:7–21CrossRefGoogle Scholar
  41. Ross KJ, Fransz P, Armstrong SJ, Vizir I, Mulligan B, Franklin FCH, Jones GH (1997) Cytological characterization of four meiotic mutants of Arabidopsis isolated from T-DNA-transformed lines. Chrom Res 5:551–559PubMedCrossRefGoogle Scholar
  42. Ross KJ, Fransz P, Jones GH (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chrom Res 4:507–516PubMedCrossRefGoogle Scholar
  43. Scherthan H (2001) A bouquet makes ends meet. Nature Rev Mol Cell Biol 2:621–627CrossRefGoogle Scholar
  44. Scherthan H, Weich S, Schwegler H, Heyting C, Harle M, Cremer T (1996) Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J Cell Biol 134:1109–1125PubMedCrossRefGoogle Scholar
  45. Schulman BA, Carrano AC, Jeffrey PD, Bowen Z, Kinnucan ER, Finnin MS, Elledge SJ, Harper JW, Pagano M, Pavletich NP (2000) Insights into SCF ubiquitin ligases from the structure of the Skp1–Skp2 complex. Nature 408:381–386PubMedCrossRefADSGoogle Scholar
  46. Shen WH, Parmentier Y, Hellmann H, Lechner E, Dong A, Masson J, Granier F, Lepiniec L, Estelle M, Genschik P (2002) Null mutation of AtCul1 causes arrest in early embryogenesis in Arabidopsis. Mol Biol Cell 13:1916–1928PubMedCrossRefGoogle Scholar
  47. Skowyra D, Koepp DM, Kamura T, Conrad MN, Conaway RC, Conaway JW, Elledge SJ, Harper JW (1999) Reconstitution of G1 cyclin ubiquitination with complexes containing SCFGrr1 and Rbx1. Science 284:662–665PubMedCrossRefADSGoogle Scholar
  48. Sullivan JA, Shirasu K, Deng XW (2003) The diverse roles of ubiquitin and the 26S proteasome in the life of plants. Nat Rev Genet 4:948–958PubMedCrossRefGoogle Scholar
  49. Trelles-Sticken E, Scherthan H (1999) Bouquet formation in budding yeast does not require homologous chromosomes. Cytogen Cell Genet 85:181–181Google Scholar
  50. Tsvetkov LM, Yeh KH, Lee SJ, Sun H, Zhang H (1999) P27(Kip1) ubiquitination and degradation is regulated by the SCF(skp2) complex through phosphorylated thr187 in p27. Curr Biol 9:661–664PubMedCrossRefGoogle Scholar
  51. Wang Y, Yang M (2006) The Arabidopsis Skp1-like1 (ASK1) protein acts predominately from leptotene to pachytene and represses homologous recombination in male meiosis. Planta 223:613–617Google Scholar
  52. Wang YX, Magnard JL, McCormick S, Yang M (2004a) Progression through meiosis I and meiosis II in Arabidopsis anthers is regulated by an A-type cyclin predominately expressed in prophase I. Plant Physiol 136:4127–4135CrossRefGoogle Scholar
  53. Wang YX, Wu H, Liang GQ, Yang M (2004b) Defects in nucleolar migration and synapsis in male prophase I in the ask1-1 mutant of Arabidopsis. Sex Plant Repro 16:273–282CrossRefGoogle Scholar
  54. Wilkinson CRM, Wallace M, Morphew M, Perry P, Allshire R, Javerzat JP, McIntosh JR, Gordon C (1998) Localization of the 26S proteasome during mitosis and meiosis in fission yeast. EMBO J 17:6465–6476PubMedCrossRefGoogle Scholar
  55. Yang M, Hu Y, Lodhi M, McCombie WR, Ma H (1999a) The Arabidopsis Skp1-Like1 gene is essential for male meiosis and may control homologue separation. Proc Natl Acad Sci USA 96:11416–11421CrossRefADSGoogle Scholar
  56. Yang W.-C, Ye D, Xu J, Sundaresan V (1999b) The SPOROCYTELESS gene of Arabidopsis is required for the initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev 13:2108–2117Google Scholar
  57. Zhao D, Han T, Risseeuw E, Crosby W, Ma H (2003a) Conservation and divergence of ASK1 and ASK2 gene functions during male meiosis in Arabidopis. Plant Mol Bio 53:163–173CrossRefGoogle Scholar
  58. Zhao D, Ni W, Feng B, Han T, Petrasek MG, Ma H (2003b) Members of the ASK gene family exhibit a variety of expression patterns and may play diverse roles in Arabidopsis. Plant Physiol 133:203–217CrossRefGoogle Scholar
  59. Zhao D, Yang M, Solava J, Ma H (1999) The ASK1 gene regulates development and interacts with the UFO gene to control floral organ identity in Arabidopsis. Dev Genet 25:209–223PubMedCrossRefGoogle Scholar
  60. Zhao D, Yu Q, Chen M, Ma H (2001) The ASK1 gene regulates b function gene expression in cooperation with UFO and Leafy in Arabidopsis. Dev 128:2735–2746Google Scholar
  61. Zheng N, Schulman BA, Song L, Miller JJ, Jeffrey PD, Wang P, Chu C, Koepp DM, Elledge SJ, Pagano M, Conaway RC, Conaway JW, Harper JW, Pavletich NP (2002) Structure of the Cul1-Rbx1-Skp1-F Box Skp2 SCF ubiquitin ligase complex. Nature 416:703–709PubMedCrossRefADSGoogle Scholar
  62. Zickler D, Kleckner N (1998) The leptotene-zygotene transition of meiosis. Ann Rev Genet 32:619–702PubMedCrossRefGoogle Scholar
  63. Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Ann Rev Genet 33:603–754PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Dazhong Zhao
    • 1
    • 3
  • Xiaohui Yang
    • 2
  • Li Quan
    • 1
  • Ljudmilla Timofejeva
    • 1
    • 4
  • Nathan W. Rigel
    • 1
  • Hong Ma
    • 1
    Email author
  • Christopher A. Makaroff
    • 2
    Email author
  1. 1.Department of Biology and the Huck Institutes of the Life SciencesThe Pennsylvania State UniversityUniversity ParkUSA
  2. 2.Department of Chemistry and BiochemistryMiami UniversityOxfordUSA
  3. 3.Department of Biological SciencesUniversity of Wisconsin-MilwaukeeMilwaukeeUSA
  4. 4.Department of Gene TechnologyTallinn University of TechnologyTallinnEstonia

Personalised recommendations