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Plant Cell Reports

, Volume 29, Issue 4, pp 307–315 | Cite as

Two Arabidopsis cyclin A3s possess G1 cyclin-like features

  • Ikuo Takahashi
  • Shoko Kojima
  • Norihiro Sakaguchi
  • Chikage Umeda-Hara
  • Masaaki Umeda
Original Paper

Abstract

A-type cyclins (CYCAs) are a type of mitotic cyclin and are closely related to cyclin B. Plant CYCAs are classified into three subtypes (CYCA1–CYCA3), among which CYCA3 has been suggested to show a biased expression during the G1-to-S phase. We characterised Arabidopsis CYCA3s (CYCA3;1–CYCA3;4) in terms of expression pattern and protein function. CYCA3;1 and CYCA3;2 transcripts were highly accumulated at the G1/S phase, whereas CYCA3;4 was constantly expressed during the cell cycle. Expressions of CYCA3;1 and CYCA3;2 were observed in actively dividing tissues, such as root and shoot apical meristems and lateral root primordia. Overexpression of CYCA3;1 or CYCA3;2 distorted apical dominance in Arabidopsis, indicating that they have critical functions in shoot meristems. In insect cells, CYCA3;1 formed an active kinase complex with CDKA;1, an orthologue of the yeast Cdc2/Cdc28p, and phosphorylated retinoblastoma-related protein, a key regulator in the transition from the G1 to the S phase. Our results suggest that Arabidopsis CYCA3;1 and CYCA3;2 are distinct members of the G1 cyclin family that play an important role in meristematic tissues.

Keywords

Cell cycle Cyclin-dependent kinase Cyclin A RBR protein Arabidopsis thaliana Apical dominance 

Abbreviations

CaMV

Cauliflower mosaic virus

CDK

Cyclin-dependent kinase

CYC

Cyclin

GFP

Green fluorescent protein

GST

Glutathione S-transferase

His

Histidine

MS

Murashige and Skoog

ORF

Open reading frame

Rb

Retinoblastoma

RBR

Retinoblastoma-related

RT-PCR

Reverse transcription-polymerase chain reaction

Notes

Acknowledgments

We thank Dr. Taku Takahashi (Okayama University), Dr. Tsuyoshi Nakagawa (Shimane University), and Dr. Masami Sekine (Ishikawa Prefectural University) for providing the histone H4 probe, pGWB vectors, and the RBR plasmid, respectively. We also thank the ABRC at Ohio State University for providing the seeds of T-DNA insertion mutants. We are grateful to Dr. Ryoko Ohno (RIBS OKAYAMA) for her help in synchronisation of cultured cells. This work was supported by Grants-in-Aid for Scientific Research on Priority Areas (Grant Nos. 20053013 and 20061021) and a Grant-in-Aid for Scientific Research (B) (Grant No. 19370019) from the Ministry of Education, Culture, Sports, Science and Technology of Japan and by the Program for Promotion of Basic Research Activities for Innovative Biosciences.

Supplementary material

299_2010_817_MOESM1_ESM.doc (967 kb)
Supplementary material 1 (DOC 967 kb)

References

  1. Boniotti MB, Gutierrez C (2001) A cell-cycle-regulated kinase activity phosphorylates plant retinoblastoma protein and contains, in Arabidopsis, a CDKA/cyclin D complex. Plant J 28:341–350CrossRefPubMedGoogle Scholar
  2. Braissant O, Wahli W (1998) Differential expression of peroxisome proliferator-activated receptor-alpha, -beta, and -gamma during rat embryonic development. Endocrinology 139:2748–2754CrossRefPubMedGoogle Scholar
  3. Burssens S, de Almeida Engler J, Beeckman T, Richard C, Shaul O, Ferreira P, Van Montagu M, Inzé D (2000) Developmental expression of the Arabidopsis thaliana CycA2;1 gene. Planta 211:623–631CrossRefPubMedGoogle Scholar
  4. Chaubet-Gigot N (2000) Plant A-type cyclins. Plant Mol Biol 43:659–675CrossRefPubMedGoogle Scholar
  5. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  6. Cockcroft CE, den Boer BGW, Healy JMS, Murray JAH (2000) Cyclin D control of growth rate in plants. Nature 405:575–579CrossRefPubMedGoogle Scholar
  7. Coverley D, Pelizon C, Trewick S, Laskey RA (2000) Chromatin-bound Cdc6 persists in S and G2 phases in human cells, while soluble Cdc6 is destroyed in a cyclin A-cdk2 dependent process. J Cell Sci 113:1929–1938PubMedGoogle Scholar
  8. Coverley D, Laman H, Laskey RA (2002) Distinct roles for cyclins E and A during DNA replication complex assembly and activation. Nat Cell Biol 4:523–528CrossRefPubMedGoogle Scholar
  9. Dewitte W, Riou-Khamlichi C, Scofield S, Healy JMS, Jacqmard A, Kilby NJ, Murray JAH (2003) Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 15:79–92CrossRefPubMedGoogle Scholar
  10. Doerner P, Jørgensen J-E, You R, Steppuhn J, Lamb C (1996) Control of root growth and development by cyclin expression. Nature 380:520–523CrossRefPubMedGoogle Scholar
  11. Gutiérrez R, Quiroz-Figueroa F, Vázquez-Ramos JM (2005) Maize cyclin D2 expression, associated kinase activity and effect of phytohormones during germination. Plant Cell Physiol 46:166–173CrossRefPubMedGoogle Scholar
  12. Harbour JW, Dean DC (2000) The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev 14:2393–2409CrossRefPubMedGoogle Scholar
  13. Huntley R, Healy S, Freeman D, Lavender P, de Jager S, Greenwood J, Makker J, Walker E, Jackman M, Xie Q, Bannister AJ, Kouzarides T, Gutiérrez C, Doonan JH, Murray JAH (1998) The maize retinoblastoma protein homologue ZmRb-1 is regulated during leaf development and displays conserved interactions with G1/S regulators and plant cyclin D (CycD) proteins. Plant Mol Biol 37:155–169CrossRefPubMedGoogle Scholar
  14. Imai KK, Ohashi Y, Tsuge T, Yoshizumi T, Matsui M, Oka A, Aoyama T (2006) The A-type cyclin CYCA2;3 is a key regulator of ploidy levels in Arabidopsis endoreduplication. Plant Cell 18:382–396CrossRefPubMedGoogle Scholar
  15. Kono A, Umeda-Hara C, Lee J, Ito M, Uchimiya H, Umeda M (2003) Arabidopsis D-type cyclin CYCD4;1 is a novel cyclin partner of B2-type cyclin-dependent kinase. Plant Physiol 132:1315–1321CrossRefPubMedGoogle Scholar
  16. Kono A, Ohno R, Umeda-Hara C, Uchimiya H, Umeda M (2006) A distinct type of cyclin D, CYCD4;2, involved in the activation of cell division in Arabidopsis. Plant Cell Rep 25:540–545CrossRefPubMedGoogle Scholar
  17. Kono A, Umeda-Hara C, Adachi S, Nagata N, Konomi M, Nakagawa T, Uchimiya H, Umeda M (2007) The Arabidopsis D-type cyclin CYCD4 controls cell division in the stomatal lineage of the hypocotyl epidermis. Plant Cell 19:1265–1277CrossRefPubMedGoogle Scholar
  18. Masubelele NH, Dewitte W, Menges M, Maughan S, Collins C, Huntley R, Nieuwland J, Scofield S, Murray JAH (2005) D-type cyclins activate division in the root apex to promote seed germination in Arabidopsis. Proc Natl Acad Sci USA 102:15694–15699CrossRefPubMedGoogle Scholar
  19. Menges M, Murray JA (2002) Synchronous Arabidopsis suspension cultures for analysis of cell-cycle gene activity. Plant J 30:203–212CrossRefPubMedGoogle Scholar
  20. Menges M, de Jager SM, Gruissem W, Murray JAH (2005) Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J 41:546–566CrossRefPubMedGoogle Scholar
  21. Mészáros T, Miskolczi P, Ayaydin F, Pettkó-Szandtner A, Peres A, Magyar Z, Horváth GV, Bakó L, Fehér A, Dudits D (2000) Multiple cyclin-dependent kinase complexes and phosphatases control G2/M progression in alfalfa cells. Plant Mol Biol 43:595–605CrossRefPubMedGoogle Scholar
  22. Nakagami H, Sekine M, Murakami H, Shinmyo A (1999) Tobacco retinoblastoma-related protein phosphorylated by a distinct cyclin-dependent kinase complex with Cdc2/cyclin D in vitro. Plant J 18:243–252CrossRefPubMedGoogle Scholar
  23. Nakagami H, Kawamura K, Sugisaka K, Sekine M, Shinmyo A (2002) Phosphorylation of retinoblastoma-related protein by the cyclin D/cyclin-dependent kinase complex is activated at the G1/S-phase transition in tobacco. Plant Cell 14:1847–1857CrossRefPubMedGoogle Scholar
  24. Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y, Toyooka K, Matsuoka K, Jinbo T, Kimura T (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng 104:34–41CrossRefPubMedGoogle Scholar
  25. Nishitani H, Lygerou Z, Nishimoto T (2004) Proteolysis of DNA replication licensing factor Cdt1 in S-phase is performed independently of geminin through its N-terminal region. J Biol Chem 279:30807–30816CrossRefPubMedGoogle Scholar
  26. Qi R, John PCL (2007) Expression of genomic AtCYCD2;1 in Arabidopsis induces cell division at smaller cell sizes: implications for the control of plant growth. Plant Physiol 144:1587–1597CrossRefPubMedGoogle Scholar
  27. Reichheld J-P, Chaubet N, Shen WH, Renaudin J-P, Gigot C (1996) Multiple A-type cyclins express sequentially during the cell cycle in Nicotiana tabacum BY2 cells. Proc Natl Acad Sci USA 93:13819–13824CrossRefPubMedGoogle Scholar
  28. Renaudin JP, Doonan JH, Freeman D, Hashimoto J, Hirt H, Inzé D, Jacobs T, Kouchi H, Rouzé P, Sauter M, Savouré A, Sorrell DA, Sundaresan V, Murray JAH (1996) Plant cyclins: a unified nomenclature for plant A-, B- and D-type cyclins based on sequence organization. Plant Mol Biol 32:1003–1018CrossRefPubMedGoogle Scholar
  29. Renaudin JP, Savouré A, Philippe H, Van Montagu M, Inzé D, Rouzé P (1998) Characterization and classification of plant cyclin sequences related to A- and B-type cyclins. In: Francis D, Dudits D, Inzé D (eds) Plant cell division. Portland Press, London, pp 67–98Google Scholar
  30. Roudier F, Fedorova E, Györgyey J, Feher A, Brown S, Kondorosi A, Kondorosi E (2000) Cell cycle function of a Medicago sativa A2-type cyclin interacting with a PSTAIRE-type cyclin-dependent kinase and a retinoblastoma protein. Plant J 23:73–83CrossRefPubMedGoogle Scholar
  31. Shen WH (2002) The plant E2F-Rb pathway and epigenetic control. Trends Plant Sci 7:505–511CrossRefPubMedGoogle Scholar
  32. Sherr CJ (1996) Cancer cell cycles. Science 274:1672–1677CrossRefPubMedGoogle Scholar
  33. Sherr CJ, Roberts JM (2004) Living with or without cyclins and cyclin-dependent kinases. Genes Dev 18:2699–2711CrossRefPubMedGoogle Scholar
  34. Shimotohno A, Matsubayashi S, Yamaguchi M, Uchimiya H, Umeda M (2003) Differential phosphorylation activities of CDK-activating kinases in Arabidopsis thaliana. FEBS Lett 534:69–74CrossRefPubMedGoogle Scholar
  35. Sugimoto N, Tatsumi Y, Tsurumi T, Matsukage A, Kiyono T, Nishitani H, Fujita M (2004) Cdt1 phosphorylation by cyclin A-dependent kinases negatively regulates its function without affecting geminin binding. J Biol Chem 279:19691–19697CrossRefPubMedGoogle Scholar
  36. Takatsuka H, Ohno R, Umeda M (2009) The Arabidopsis cyclin-dependent kinase-activating kinase CDKF;1 is a major regulator of cell proliferation and cell expansion but is dispensable for CDKA activation. Plant J 59:475–487CrossRefPubMedGoogle Scholar
  37. Umeda M, Bhalerao RP, Schell J, Uchimiya H, Koncz C (1998) A distinct cyclin-dependent kinase-activating kinase of Arabidopsis thaliana. Proc Natl Acad Sci USA 95:5021–5026CrossRefPubMedGoogle Scholar
  38. Umeda M, Umeda-Hara C, Uchimiya H (2000) A cyclin-dependent kinase-activating kinase regulates differentiation of root initial cells in Arabidopsis. Proc Natl Acad Sci USA 97:13396–13400CrossRefPubMedGoogle Scholar
  39. Wyrzykowska J, Pien S, Shen WH, Fleming AJ (2002) Manipulation of leaf shape by modulation of cell division. Development 129:957–964PubMedGoogle Scholar
  40. Yamaguchi M, Fabian T, Sauter M, Bhalerao RP, Schrader J, Sandberg G, Umeda M, Uchimiya H (2000) Activation of CDK-activating kinase is dependent on interaction with H-type cyclins in plants. Plant J 24:11–20CrossRefPubMedGoogle Scholar
  41. Yang R, Müller C, Huynh V, Fung YK, Yee AS, Koeffler HP (1999) Functions of cyclin A1 in the cell cycle and its interactions with transcription factor E2F-1 and the Rb family of proteins. Mol Cell Biol 19:2400–2407PubMedGoogle Scholar
  42. Yu Y, Steinmetz A, Meyer D, Brown S, Shen W-H (2003) The tobacco A-type cyclin, Nicta;CYCA3;2, at the nexus of cell division and differentiation. Plant Cell 15:2763–2777CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Ikuo Takahashi
    • 1
  • Shoko Kojima
    • 1
  • Norihiro Sakaguchi
    • 1
  • Chikage Umeda-Hara
    • 1
  • Masaaki Umeda
    • 1
  1. 1.Graduate School of Biological SciencesNara Institute of Science and TechnologyIkomaJapan

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