Skip to main content
SpringerLink
Log in

Isolation of a new mitotic-like cyclin from Arabidopsis: complementation of a yeast cyclin mutant with a plant cyclin

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Cyclins, a large family of proteins, are the regulatory subunits of cyclin-dependent protein kinases that are essential activators of cell cycle progression in eukaryotes. Here we report isolation of a new cyclin cDNA (cyc1bAt) from Arabidopsis cDNA libraries using polymerase chain reaction amplified cyclin-box sequences as probes. The deduced amino acid sequence of the isolated cDNA showed the highest sequence similarity with mitotic cyclins. However, the nucleotide and predicted amino acid sequence of cyc1bAt is different from five other mitotic-like cyclins that have recently been isolated from the same system, indicating that it is a new mitotic-like cyclin. These results, together with previous reports, suggest that there are at least six different mitotic-like cyclins in Arabidopsis. Expression of cyc1bAt in yeast G1 cyclin-minus mutant (DL1) rescued the cyclin-minus phenotype, demonstrating that plant mitotic-like cyclin can complement cyclin function in yeast. Analysis of expression of cyc1bAt in different tissues by reverse transcription-polymerase chain reaction using primers corresponding to a unique region of the cDNA showed that cyc1bAt is differentially expressed in different tissues with highest expression in flowers and no detectable expression in leaves.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Day IS, Reddy ASN: Cloning of a family of cyclins from Arabidopsis thaliana. Biochim Biophys Acta 1218: 115–118 (1994).

    Google Scholar 

  2. Dingwall C, Laskey RA: Nuclear targeting sequences: a consensus? Trends Biochem Sci 16: 478–481 (1991).

    Google Scholar 

  3. Doerner P: Cell cycle regulation in plants. Plant Physiol 106: 823–827 (1994).

    Google Scholar 

  4. Dulic V, Lees E, Reed SI: Association of human cyclin E with a periodic G1-S phase protein kinase. Science 257: 1958–1961 (1992).

    Google Scholar 

  5. Durfee T, Becherer K, Chen P-L, Yeh S-H, Yang Y, Kilburn AE, Lee W-H, Elledge SJ: The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Devel 7: 555–569 (1993).

    Google Scholar 

  6. Evans T, Rosenthal ET, Youngblom J, Distel D, Hunt T: Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell 33: 389–396 (1983).

    Google Scholar 

  7. Ferreira PCG, Hemerly AS, Engeler JA, C.B., S.B., Van-Montagu M, Engler G, Inze D. Three discrete classes of Arabidopsis cyclins are expressed during different intervals of the cell cycle. Proc Natl Acad Sci USA 91: 11313–11317 (1994).

    Google Scholar 

  8. Ferreira PCG, Hemerly AS, Engler JA, Montagu MV, Engler G, Inze D: Developmental expression of the Arabidopsis cyclin gene cyc1At. Plant Cell 6: 1763–1774 (1994).

    Google Scholar 

  9. Fobert PR, Coen ES, Murphy GJP, Doonan JH: Patterns of cell division revealed by transcriptional regulation of genes during the cell cycle in plants. EMBO J 13: 616–624 (1994).

    Google Scholar 

  10. Fordham-Skelton AP, Safadi F, Golovkin M, Reddy ASN: A non-radioactive method for isolating complementary DNAs encoding calmodulin-binding proteins. Plant Mol Biol Rep 12: 355–363 (1994).

    Google Scholar 

  11. Galaktionov K, Beach D: Specific activation of cdc25 tyrosine phosphatases by B-type cyclins: evidence for multiple roles of mitotic cyclins. Cell 67: 1181–1194 (1991).

    Google Scholar 

  12. Galbraith DW, Harkins KR, Knapp S: Systemic endopolyploidy in Arabidopsis thaliana. Plant Physiol 96: 985–989 (1991).

    Google Scholar 

  13. Gallant P, Nigg EA: Identification of a novel vertebrate cyclin: cyclin B3 shares properties with both A- and B-type cyclins. EMBO J 10: 595–605 (1994).

    Google Scholar 

  14. Gautier J, Norbury C, Lohka M, Nurse P, Maller J: Purfied maturation-promoting factor contains the product of a Xenopus homolog of the fission yeast cell cycle control gene cdc2+. Cell 54: 433–439 (1988).

    Google Scholar 

  15. Glotzer M, Murray AW, Kirschner MW: Cyclin is degraded by the ubiquitin pathway. Nature 349: 132–138 (1991).

    Google Scholar 

  16. Gyuris J, Golemis E, Chertkov H, Brent R: Cid1, a human G1 and S phase protein phosphatase that associates with Cdk2. Cell 75: 791–803 (1993).

    Google Scholar 

  17. Hata S, Kouchi H, Suzuka I, Ishii T: Isolation and characterization of cDNA clones for plant cyclins. EMBO J 10: 2681–2688 (1991).

    Google Scholar 

  18. Hemerly A, Bergounioux C, Van Montagu M, Inzé D, Ferreira P: Genes regulating the plant cell cycle: isolation of mitotic-like cyclin from Arabidopsis thaliana. Proc Natl Acad Sci USA 89: 3295–3299 (1992).

    Google Scholar 

  19. Jacobs TJ: Control of the cell cycle. Devel Biol 153: 1–15 (1992).

    Google Scholar 

  20. Kaffman A, Herskowitz I, Tjian R, O'Shea EK: Phosphorylation of the transcription factor PH04 by a cyclin-CDK comples; PH080-PH085. Science 263: 1153–1156 (1994).

    Google Scholar 

  21. Kemp BE, Pearson RB: Protein kinase recognition sequence motifs. Trends Biochem Sci 15: 342–346 (1990).

    Google Scholar 

  22. Koff A, Cross F, Fisher A, Schumacher J, Leguellec K, Philippe M, Roberts JM: Human cyclin E, a new cyclin that interacts with two members of the CDC2 gene family. Cell 66: 1217–1228 (1991).

    Google Scholar 

  23. Lew DJ, Dulic V, Reed SI: Isolation of three novel human cyclins by rescue of G1 cyclin (Cln) function in yeast. Cell 66: 1197–1206 (1991).

    Google Scholar 

  24. Lippuner V, Chou IT, Scott SV, Ettinger WF, Theg SM, Gasser CS: Cloning and characterization of chlorplast and cytosolic forms of cyclophilin from Arabidopsis thaliana. J Biol Chem 269: 7863–7868 (1994).

    Google Scholar 

  25. Lohka MJ, Hayes MK, Maller JL: Purification of maturation-promoting factor, an intracellular regulation of early mitotic events. Proc Natl Acad Sci USA 85: 3009–3013 (1988).

    Google Scholar 

  26. Meaday V, Moore L, Ogas J, Tyers M, Andrews B: The PCL2 ORFD-PHO85 cyclin-dependent kinase complex: a cell cycle regulator in yeast. Science 266: 1391–1395 (1994).

    Google Scholar 

  27. Melaragno JE, Mehrotra B, Coleman AW: Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5: 1661–1668 (1993).

    Google Scholar 

  28. Meyerson M, Enders GH, Wu C-L, Su L-K, Gorka C, Nelson C, Harlow E, Tsai L-H: A family of human cdc2-related protein kinases. EMBO J 11: 2909–2917 (1992).

    Google Scholar 

  29. Norbury C, Nurse P: Animal cell cycles and their control. Annu Rev Biochem 61: 441–470 (1992).

    Google Scholar 

  30. Nugent JHA, Alfa CE, Young T, Hyams JS: Conserved structural motifs in cyclins identified by sequence analysis. J Cell Sci 99: 669–674 (1991).

    Google Scholar 

  31. Nurse P: Universal control mechanism regulating onset of M-phase. Nature 344: 503–508 (1990).

    Google Scholar 

  32. Ohtsubo M, Roberts JM: Cyclin-dependent regulation of G1 in mammalian fibrobalsts. Science 259: 1908–1912 (1993).

    Google Scholar 

  33. Pines J: Cyclins and cylin-dependent kinases: take your partners. Trends Biochem Sci 18: 195–197 (1993).

    Google Scholar 

  34. Reddy ASN: Cell cycle control in plants. In: Pessarakli (eds) Handbook of Plant and Crop Physiology, pp. 147–167. Marcel Dekker, New York (1994).

    Google Scholar 

  35. Reed S, Hadwiger JA, Lorincz AT: Protein kinase activity associated with the product of the yeast cell division cycle gene CDC28. Proc Natl Acad Sci USA 82: 4055–4059 (1985).

    Google Scholar 

  36. Renaudin J, Colasanti J, Rime H, Yuan Z, Sundaresan V: Cloning of four cyclins from maize indicates that higher plants have three structurally distinct groups of mitotic cyclins. Proc Natl Acad Sci USA 91: 7375–7379 (1994).

    Google Scholar 

  37. Rogers SO, Bendich AJ: Extraction of DNA from plant tissues. In: Gelvin BS, Schilperoort RA (eds) Plant Molecular Biology Manual, pp. A6:1–10. Kluwer Academic Publishers, Dordrecht (1988).

    Google Scholar 

  38. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).

    Google Scholar 

  39. Sherr CJ: Mammalian G1 cyclins. Cell 73: 1059–1065 (1993).

    Google Scholar 

  40. Sikorski RS, Boeke JD: In vitro mutagenesis and plasmid shuffling: from cloned gene to mutant yeast. Meth Enzymol 194: 302–318 (1991).

    Google Scholar 

  41. Soni R, Carmichael JP, Shah ZH, Murray JAH: A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell 7: 85–103 (1995).

    Google Scholar 

  42. Szarka S, Fitch M, Schaerer S, Moloney M: Classification and expression of a family of cyclin gene homologues in Brassica napus. Plant Mol Biol 27: 263–275 (1995).

    Google Scholar 

  43. Tsai L-H, Harlow E, Meyerson M: Isolation of the human cdk2 gene that encodes the cyclin A- and adenovirus E1A-associated p33 kinase. Nature 353: 174–177 (1991).

    Google Scholar 

  44. Xiong Y, Connolly T, Futcher B, Beach D: Human D-type cyclin. Cell 65: 691–699 (1991).

    Google Scholar 

  45. Zheng X-F, Ruderman JV: Functional analysis of the P box, a domain in cyclin B required for the activation of cdc25. Cell 75: 155–164 (1993).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, Colorado State University, 80523, Fort Collins, CO, USA

    Irene S. Day, A. S. N. Reddy & Maxim Golovkin

  2. Program in Cell and Molecular Biology, Colorado State University, 80523, Fort Collins, CO, USA

    Irene S. Day, A. S. N. Reddy & Maxim Golovkin

Authors
  1. Irene S. Day
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. S. N. Reddy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maxim Golovkin
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Day, I.S., Reddy, A.S.N. & Golovkin, M. Isolation of a new mitotic-like cyclin from Arabidopsis: complementation of a yeast cyclin mutant with a plant cyclin. Plant Mol Biol 30, 565–575 (1996). https://doi.org/10.1007/BF00049332

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00049332

Key words

Search

Navigation