Home LiteratureArticle Details
PMID: 15004270 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Expression of a nondegradable cyclin B1 affects plant development and leads to endomitosis by inhibiting the formation of a phragmoplast.

The Plant cell ·Vol. 16 ·No. 3 ·2004-03-00 ·Pages 643-57

Weingartner M, Criqui MC, Mészáros T, Binarova P, Schmit AC, Helfer A, Derevier A, Erhardt M, Bögre L, Genschik P

Abstract

In plants after the disassembly of mitotic spindle, a specific cytokinetic structure called the phragmoplast is built, and after cytokinesis, microtubules populate the cell cortex in an organized orientation that determines cell elongation and shape. Here, we show that impaired cyclin B1 degradation, resulting from a mutation within its destruction box, leads to an isodiametric shape of epidermal cells in leaves, stems, and roots and retarded growth of seedlings. Microtubules in these misshaped cells are grossly disorganized, focused around the nucleus, whereas they were entirely missing or abnormally organized along the cell cortex. A high percentage of cells expressing nondestructible cyclin B1 had doubled DNA content as a result of undergoing endomitosis. During anaphase the cytokinesis-specific syntaxin KNOLLE could still localize to the midplane of cell division, whereas NPK1-activating kinesin-like protein 1, a cytokinetic kinesin-related protein, was unable to do so, and instead of the formation of a phragmoplast, the midzone microtubules persisted between the separated nuclei, which eventually fused. In summary, our results show that the timely degradation of mitotic cyclins in plants is required for the reorganization of mitotic microtubules to the phragmoplast and for proper cytokinesis. Subsequently, the presence of nondegradable cyclin B1 leads to a failure in organizing properly the cortical microtubules that determine cell elongation and shape.

MeSH Terms
Base Sequence Cell Division Cyclin B/genetics,metabolism Cyclin B1 Cyclin-Dependent Kinases/metabolism DNA, Plant/genetics,metabolism Gene Expression Genes, Plant Microtubules/metabolism Mitosis Mutation Phenotype Plant Proteins/metabolism Plants, Genetically Modified Polyploidy Seedlings/metabolism Spindle Apparatus/metabolism Tobacco/genetics,growth & development,metabolism
Chemicals
Cyclin B Cyclin B1 DNA, Plant Plant Proteins Cyclin-Dependent Kinases
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Weingartner Magdalena
Max Planck Institute of Molecular Plant Physiology, 14476 Golm, Germany.
Criqui Marie-Claire
Mészáros Tamás
Binarova Pavla
Schmit Anne-Catherine
Helfer Anne
Derevier Aude
Erhardt Mathieu
Bögre László
Genschik Pascal
References (84)
84 references, click to expand
  1. Endomitosis of human megakaryocytes are due to abortive mitosis.
    Blood. 1998 May 15;91(10):3711-23 PMID: 9573008
  2. Identification of a novel vertebrate cyclin: cyclin B3 shares properties with both A- and B-type cyclins.
    EMBO J. 1994 Feb 1;13(3):595-605 PMID: 8313904
  3. Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-DPa transcription factor.
    EMBO J. 2002 Mar 15;21(6):1360-8 PMID: 11889041
  4. Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis.
    Plant Cell. 2001 Jul;13(7):1653-68 PMID: 11449057
  5. Mitosis in plants: how far we have come at the molecular level?
    Curr Opin Plant Biol. 2002 Dec;5(6):487-93 PMID: 12393010
  6. APC-dependent proteolysis of the mitotic cyclin Clb2 is essential for mitotic exit.
    Nature. 2002 Aug 1;418(6897):556-62 PMID: 12152084
  7. The role of proteolysis in cell cycle progression in Schizosaccharomyces pombe.
    EMBO J. 1996 Oct 1;15(19):5268-79 PMID: 8895572
  8. Microtubule organization in the green kingdom: chaos or self-order?
    J Cell Sci. 2002 Apr 1;115(Pt 7):1345-54 PMID: 11896182
  9. Anaphase is initiated by proteolysis rather than by the inactivation of maturation-promoting factor.
    Cell. 1993 Jul 2;73(7):1393-402 PMID: 8391932
  10. Expression of the plant cyclin-dependent kinase inhibitor ICK1 affects cell division, plant growth and morphology.
    Plant J. 2000 Dec;24(5):613-23 PMID: 11123800
  11. Cell cycle function of a rice B2-type cyclin interacting with a B-type cyclin-dependent kinase.
    Plant J. 2003 May;34(4):417-25 PMID: 12753582
  12. G2-and early-M-specific expression of the NTCYC1 cyclin gene in Nicotiana tabacum cells.
    Plant Mol Biol. 1996 Dec;32(6):1093-101 PMID: 9002608
  13. A plant-specific cyclin-dependent kinase is involved in the control of G2/M progression in plants.
    J Biol Chem. 2001 Sep 28;276(39):36354-60 PMID: 11477067
  14. Nuclear localization of cyclin B1 mediates its biological activity and is regulated by phosphorylation.
    Proc Natl Acad Sci U S A. 1997 Jan 21;94(2):502-7 PMID: 9012813
  15. Complexity, cross talk and integration of plant MAP kinase signalling.
    Curr Opin Plant Biol. 2002 Oct;5(5):415-24 PMID: 12183180
  16. The role of cyclin synthesis and degradation in the control of maturation promoting factor activity.
    Nature. 1989 May 25;339(6222):280-6 PMID: 2566918
  17. Centrosomes and mitotic poles.
    Exp Cell Res. 1984 Jul;153(1):1-15 PMID: 6734733
  18. Long-range communication between chromatin and microtubules in Xenopus egg extracts.
    Curr Biol. 2003 Sep 30;13(19):1728-33 PMID: 14521840
  19. Expression of N-terminally truncated cyclin B in the Drosophila larval brain leads to mitotic delay at late anaphase.
    J Cell Sci. 1994 Oct;107 ( Pt 10):2729-38 PMID: 7876341
  20. Kinetics of endomitosis in primary murine megakaryocytes.
    J Cell Physiol. 2001 Sep;188(3):291-303 PMID: 11473355
  21. Microtubule-associated proteins in plants--why we need a MAP.
    Nat Rev Mol Cell Biol. 2001 Jan;2(1):40-7 PMID: 11413464
  22. Mitotic kinases as regulators of cell division and its checkpoints.
    Nat Rev Mol Cell Biol. 2001 Jan;2(1):21-32 PMID: 11413462
  23. Destruction of the CDC28/CLB mitotic kinase is not required for the metaphase to anaphase transition in budding yeast.
    EMBO J. 1993 May;12(5):1969-78 PMID: 8491189
  24. Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development.
    EMBO J. 1995 Aug 15;14(16):3925-36 PMID: 7664733
  25. Cyclin destruction in mitosis: a crucial task of Cdc20.
    FEBS Lett. 2002 Dec 4;532(1-2):7-11 PMID: 12459453
  26. The NPK1 mitogen-activated protein kinase kinase kinase is a regulator of cell-plate formation in plant cytokinesis.
    Genes Dev. 2001 Feb 1;15(3):352-63 PMID: 11159915
  27. Phosphorylation by CDK1 regulates XMAP215 function in vitro.
    Cell Motil Cytoskeleton. 1999;43(4):310-21 PMID: 10423272
  28. Exit from mitosis is regulated by Drosophila fizzy and the sequential destruction of cyclins A, B and B3.
    EMBO J. 1995 Oct 2;14(19):4827-38 PMID: 7588612
  29. Genome-wide analysis of core cell cycle genes in Arabidopsis.
    Plant Cell. 2002 Apr;14(4):903-16 PMID: 11971144
  30. Plant cytokinesis: motoring to the finish.
    Curr Biol. 2002 Mar 19;12(6):R206-8 PMID: 11909547
  31. Four-dimensional control of the cell cycle.
    Nat Cell Biol. 1999 Jul;1(3):E73-9 PMID: 10559915
  32. Dynamic recruitment of Cdc2 to specific microtubule structures during mitosis.
    Plant Cell. 2001 Aug;13(8):1929-43 PMID: 11487703
  33. Gamma-tubulin distribution during cortical microtubule reorganization at the M/G1 interface in tobacco BY-2 cells.
    Eur J Cell Biol. 2003 Jan;82(1):43-51 PMID: 12602947
  34. Plant cyclins: a unified nomenclature for plant A-, B- and D-type cyclins based on sequence organization.
    Plant Mol Biol. 1996 Dec;32(6):1003-18 PMID: 9002599
  35. Phosphorylation and activation of 13S condensin by Cdc2 in vitro.
    Science. 1998 Oct 16;282(5388):487-90 PMID: 9774278
  36. Cell cycle -dependent proteolysis in plants. Identification Of the destruction box pathway and metaphase arrest produced by the proteasome inhibitor mg132
    Plant Cell. 1998 Dec;10(12):2063-76 PMID: 9836745
  37. All aboard the cyclin train: subcellular trafficking of cyclins and their CDK partners.
    Trends Cell Biol. 1999 Jun;9(6):207-10 PMID: 10354564
  38. Cell cycle-dependent proteolysis and ectopic overexpression of cyclin B1 in tobacco BY2 cells.
    Plant J. 2000 Dec;24(6):763-73 PMID: 11135110
  39. The Arabidopsis HOBBIT gene encodes a CDC27 homolog that links the plant cell cycle to progression of cell differentiation.
    Genes Dev. 2002 Oct 1;16(19):2566-75 PMID: 12368267
  40. Microtubule polymerization dynamics.
    Annu Rev Cell Dev Biol. 1997;13:83-117 PMID: 9442869
  41. Aurora-A overexpression reveals tetraploidization as a major route to centrosome amplification in p53-/- cells.
    EMBO J. 2002 Feb 15;21(4):483-92 PMID: 11847097
  42. Self-organization of treadmilling microtubules into a polar array.
    Trends Cell Biol. 2002 Oct;12(10):462-5 PMID: 12441249
  43. MOR1 is essential for organizing cortical microtubules in plants.
    Nature. 2001 May 31;411(6837):610-3 PMID: 11385579
  44. A new class of microtubule-associated proteins in plants.
    Nat Cell Biol. 2000 Oct;2(10):750-3 PMID: 11025667
  45. Cyclin is degraded by the ubiquitin pathway.
    Nature. 1991 Jan 10;349(6305):132-8 PMID: 1846030
  46. Degradation of cyclin B is required for the onset of anaphase in Mammalian cells.
    J Biol Chem. 2003 Sep 26;278(39):37865-73 PMID: 12865421
  47. Active cyclin B1-Cdk1 first appears on centrosomes in prophase.
    Nat Cell Biol. 2003 Feb;5(2):143-8 PMID: 12524548
  48. Cell cycle phase specificity of putative cyclin-dependent kinase variants in synchronized alfalfa cells.
    Plant Cell. 1997 Feb;9(2):223-35 PMID: 9061953
  49. The schedule of destruction of three mitotic cyclins can dictate the timing of events during exit from mitosis.
    Curr Biol. 2001 May 1;11(9):671-83 PMID: 11369230
  50. Endoreplication cell cycles: more for less.
    Cell. 2001 May 4;105(3):297-306 PMID: 11348589
  51. The cdc2Ms Kinase Is Differently Regulated in the Cytoplasm and in the Nucleus.
    Plant Physiol. 1997 Mar;113(3):841-852 PMID: 12223648
  52. The mitotic spindle: a self-made machine.
    Science. 2001 Oct 19;294(5542):543-7 PMID: 11641489
  53. The anaphase-promoting complex: it's not just for mitosis any more.
    Genes Dev. 2002 Sep 1;16(17):2179-206 PMID: 12208841
  54. Re-staging mitosis: a contemporary view of mitotic progression.
    Nat Cell Biol. 2001 Jan;3(1):E3-6 PMID: 11146636
  55. Acentrosomal microtubule nucleation in higher plants.
    Int Rev Cytol. 2002;220:257-89 PMID: 12224551
  56. The CDK inhibitor NtKIS1a is involved in plant development, endoreduplication and restores normal development of cyclin D3; 1-overexpressing plants.
    J Cell Sci. 2002 Mar 1;115(Pt 5):973-82 PMID: 11870216
  57. 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. 2003 Feb 1;116(Pt 3):487-98 PMID: 12508110
  58. Molecular aspects of microtubule dynamics in plants.
    Curr Opin Plant Biol. 2001 Dec;4(6):513-9 PMID: 11641067
  59. Sustained microtubule treadmilling in Arabidopsis cortical arrays.
    Science. 2003 Jun 13;300(5626):1715-8 PMID: 12714675
  60. Caenorhabditis elegans cyclin A- and B-type genes: a cyclin A multigene family, an ancestral cyclin B3 and differential germline expression.
    J Cell Sci. 1995 Jun;108 ( Pt 6):2415-24 PMID: 7545687
  61. Specialization and targeting of B-type cyclins.
    Mol Cell. 1999 Jul;4(1):11-9 PMID: 10445023
  62. Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins.
    J Cell Biol. 1993 Mar;120(6):1305-20 PMID: 8449978
  63. Sub-cellular localisation of GFP-tagged tobacco mitotic cyclins during the cell cycle and after spindle checkpoint activation.
    Plant J. 2001 Dec;28(5):569-81 PMID: 11849596
  64. A glucocorticoid-mediated transcriptional induction system in transgenic plants.
    Plant J. 1997 Mar;11(3):605-12 PMID: 9107046
  65. Cyclin-dependent kinases and cell division in plants- the nexus
    Plant Cell. 1999 Apr;11(4):509-22 PMID: 10213774
  66. Closing the cell cycle circle in yeast: G2 cyclin proteolysis initiated at mitosis persists until the activation of G1 cyclins in the next cycle.
    Cell. 1994 Jul 1;77(7):1037-50 PMID: 8020094
  67. Isolation of a human cyclin cDNA: evidence for cyclin mRNA and protein regulation in the cell cycle and for interaction with p34cdc2.
    Cell. 1989 Sep 8;58(5):833-46 PMID: 2570636
  68. Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3.
    Plant Cell. 2003 Jan;15(1):79-92 PMID: 12509523
  69. A simple and general method for transferring genes into plants.
    Science. 1985 Mar 8;227(4691):1229-31 PMID: 17757866
  70. Whose end is destruction: cell division and the anaphase-promoting complex.
    Genes Dev. 1999 Aug 15;13(16):2039-58 PMID: 10465783
  71. The anaphase-promoting complex: proteolysis in mitosis and beyond.
    Mol Cell. 2002 May;9(5):931-43 PMID: 12049731
  72. First glance at the plant APC/C, a highly conserved ubiquitin-protein ligase.
    Trends Plant Sci. 2003 Feb;8(2):83-9 PMID: 12597875
  73. Identification of a novel microtubule-associated protein that regulates microtubule organization and cytokinesis by using a GFP-screening strategy.
    Curr Biol. 2002 Nov 19;12(22):1946-51 PMID: 12445389
  74. Cyclin B2 undergoes cell cycle-dependent nuclear translocation and, when expressed as a non-destructible mutant, causes mitotic arrest in HeLa cells.
    J Cell Biol. 1992 Apr;117(1):213-24 PMID: 1532584
  75. Translation of cyclin mRNA is necessary for extracts of activated xenopus eggs to enter mitosis.
    Cell. 1989 Mar 24;56(6):947-56 PMID: 2564315
  76. Expansion of the cell plate in plant cytokinesis requires a kinesin-like protein/MAPKKK complex.
    Cell. 2002 Apr 5;109(1):87-99 PMID: 11955449
  77. Treatment of Vicia faba root tip cells with specific inhibitors to cyclin-dependent kinases leads to abnormal spindle formation.
    Plant J. 1998 Dec;16(6):697-707 PMID: 10069076
  78. Plant CDC2 is not only targeted to the pre-prophase band, but also co-localizes with the spindle, phragmoplast, and chromosomes.
    FEBS Lett. 1997 Dec 1;418(3):229-34 PMID: 9428718
  79. Chromosome condensation: packaging the genome.
    Curr Biol. 2001 May 15;11(10):R384-7 PMID: 11378401
  80. The HOBBIT gene is required for formation of the root meristem in the Arabidopsis embryo.
    Development. 1998 Feb;125(3):521-31 PMID: 9425146
  81. The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin.
    J Cell Biol. 1997 Dec 15;139(6):1485-93 PMID: 9396754
  82. Plant mitosis promoting factor disassembles the microtubule preprophase band and accelerates prophase progression in Tradescantia.
    Cell Biol Int. 1996 Apr;20(4):275-87 PMID: 8664851
  83. The cyclin-dependent kinase inhibitor Roughex is involved in mitotic exit in Drosophila.
    Curr Biol. 2001 Feb 6;11(3):151-60 PMID: 11231149
  84. The Arabidopsis HINKEL gene encodes a kinesin-related protein involved in cytokinesis and is expressed in a cell cycle-dependent manner.
    Curr Biol. 2002 Jan 22;12(2):153-8 PMID: 11818068
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2004-03-00
Pages
643-57
Language
English
Region
England
NLM ID
9208688
PMCID
PMC385278
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com