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. 1995 Aug;7(8):1143–1155. doi: 10.1105/tpc.7.8.1143

Distinct classes of mitotic cyclins are differentially expressed in the soybean shoot apex during the cell cycle.

H Kouchi 1, M Sekine 1, S Hata 1
PMCID: PMC160940  PMID: 7549477

Abstract

Protein phosphorylation by the complexes of cyclin and cyclin-dependent kinase plays a key role in cell cycle progression in all eukaryotes. The amplification by polymerase chain reaction of a cyclin box from developing root nodules and root apices of soybean showed the expression of a number of different molecular species of mitotic cyclins in plant meristems, and they were classified into five distinct groups based on their sequence similarities. The complete soybean cyclin cDNAs, cyc1Gm to cyc5Gm, corresponding to each group were isolated, and their predicted amino acid sequences showed clear similarities to mitotic cyclins identified from various organisms. These genes are expressed predominantly in such meristematic tissues as root and shoot apices and young developing nodules. Double-target in situ hybridization involving histone H4 as an S-phase marker allowed us to estimate the phases during which these cyclin genes are abundantly expressed. The results indicated that cyc5Gm is expressed in G2-to-M phases and cyc3Gm is expressed from late S-to-G2 phases. These expression patterns, together with the sequence criteria, strongly suggest that cyc3Gm and cyc5Gm encode the plant cognates for A- and B-type cyclins, respectively. In addition, the expression of cyc1Gm was restricted during a short period in S phase, suggesting that it belongs to a novel class of plant cyclins. Sequence comparison of 18 plant mitotic cyclins cloned thus far showed that they can be divided into four distinct structural groups with different functions in cell cycle progression.

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Selected References

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  1. Bergounioux C., Perennes C., Hemerly A. S., Qin L. X., Sarda C., Inze D., Gadal P. A cdc2 gene of Petunia hybrida is differentially expressed in leaves, protoplasts and during various cell cycle phases. Plant Mol Biol. 1992 Dec;20(6):1121–1130. doi: 10.1007/BF00028898. [DOI] [PubMed] [Google Scholar]
  2. Colasanti J., Tyers M., Sundaresan V. Isolation and characterization of cDNA clones encoding a functional p34cdc2 homologue from Zea mays. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3377–3381. doi: 10.1073/pnas.88.8.3377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Evans T., Rosenthal E. T., 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. 1983 Jun;33(2):389–396. doi: 10.1016/0092-8674(83)90420-8. [DOI] [PubMed] [Google Scholar]
  4. Feiler H. S., Jacobs T. W. Cloning of the pea cdc2 homologue by efficient immunological screening of PCR products. Plant Mol Biol. 1991 Sep;17(3):321–333. doi: 10.1007/BF00040628. [DOI] [PubMed] [Google Scholar]
  5. Ferreira P. C., Hemerly A. S., Villarroel R., Van Montagu M., Inzé D. The Arabidopsis functional homolog of the p34cdc2 protein kinase. Plant Cell. 1991 May;3(5):531–540. doi: 10.1105/tpc.3.5.531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ferreira P., Hemerly A., de Almeida Engler J., Bergounioux C., Burssens S., Van Montagu M., Engler G., Inzé D. Three discrete classes of Arabidopsis cyclins are expressed during different intervals of the cell cycle. Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11313–11317. doi: 10.1073/pnas.91.24.11313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fobert P. R., Coen E. S., Murphy G. J., Doonan J. H. Patterns of cell division revealed by transcriptional regulation of genes during the cell cycle in plants. EMBO J. 1994 Feb 1;13(3):616–624. doi: 10.1002/j.1460-2075.1994.tb06299.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Girard F., Strausfeld U., Fernandez A., Lamb N. J. Cyclin A is required for the onset of DNA replication in mammalian fibroblasts. Cell. 1991 Dec 20;67(6):1169–1179. doi: 10.1016/0092-8674(91)90293-8. [DOI] [PubMed] [Google Scholar]
  9. Hashimoto J., Hirabayashi T., Hayano Y., Hata S., Ohashi Y., Suzuka I., Utsugi T., Toh-e A., Kikuchi Y. Isolation and characterization of cDNA clones encoding cdc2 homologues from Oryza sativa: a functional homologue and cognate variants. Mol Gen Genet. 1992 May;233(1-2):10–16. doi: 10.1007/BF00587555. [DOI] [PubMed] [Google Scholar]
  10. Hata S. cDNA cloning of a novel cdc2+/CDC28-related protein kinase from rice. FEBS Lett. 1991 Feb 11;279(1):149–152. doi: 10.1016/0014-5793(91)80271-4. [DOI] [PubMed] [Google Scholar]
  11. Hemerly A., Bergounioux C., Van Montagu M., Inzé D., Ferreira P. Genes regulating the plant cell cycle: isolation of a mitotic-like cyclin from Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3295–3299. doi: 10.1073/pnas.89.8.3295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hirayama T., Imajuku Y., Anai T., Matsui M., Oka A. Identification of two cell-cycle-controlling cdc2 gene homologs in Arabidopsis thaliana. Gene. 1991 Sep 15;105(2):159–165. doi: 10.1016/0378-1119(91)90146-3. [DOI] [PubMed] [Google Scholar]
  13. Hirt H., Mink M., Pfosser M., Bögre L., Györgyey J., Jonak C., Gartner A., Dudits D., Heberle-Bors E. Alfalfa cyclins: differential expression during the cell cycle and in plant organs. Plant Cell. 1992 Dec;4(12):1531–1538. doi: 10.1105/tpc.4.12.1531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hirt H., Páy A., Györgyey J., Bakó L., Németh K., Bögre L., Schweyen R. J., Heberle-Bors E., Dudits D. Complementation of a yeast cell cycle mutant by an alfalfa cDNA encoding a protein kinase homologous to p34cdc2. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1636–1640. doi: 10.1073/pnas.88.5.1636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. King R. W., Jackson P. K., Kirschner M. W. Mitosis in transition. Cell. 1994 Nov 18;79(4):563–571. doi: 10.1016/0092-8674(94)90542-8. [DOI] [PubMed] [Google Scholar]
  16. Kouchi H., Hata S. Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol Gen Genet. 1993 Apr;238(1-2):106–119. doi: 10.1007/BF00279537. [DOI] [PubMed] [Google Scholar]
  17. Minshull J., Blow J. J., Hunt T. Translation of cyclin mRNA is necessary for extracts of activated xenopus eggs to enter mitosis. Cell. 1989 Mar 24;56(6):947–956. doi: 10.1016/0092-8674(89)90628-4. [DOI] [PubMed] [Google Scholar]
  18. Minshull J., Golsteyn R., Hill C. S., Hunt T. The A- and B-type cyclin associated cdc2 kinases in Xenopus turn on and off at different times in the cell cycle. EMBO J. 1990 Sep;9(9):2865–2875. doi: 10.1002/j.1460-2075.1990.tb07476.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nash R., Tokiwa G., Anand S., Erickson K., Futcher A. B. The WHI1+ gene of Saccharomyces cerevisiae tethers cell division to cell size and is a cyclin homolog. EMBO J. 1988 Dec 20;7(13):4335–4346. doi: 10.1002/j.1460-2075.1988.tb03332.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Norbury C., Nurse P. Animal cell cycles and their control. Annu Rev Biochem. 1992;61:441–470. doi: 10.1146/annurev.bi.61.070192.002301. [DOI] [PubMed] [Google Scholar]
  21. Peeper D. S., Parker L. L., Ewen M. E., Toebes M., Hall F. L., Xu M., Zantema A., van der Eb A. J., Piwnica-Worms H. A- and B-type cyclins differentially modulate substrate specificity of cyclin-cdk complexes. EMBO J. 1993 May;12(5):1947–1954. doi: 10.1002/j.1460-2075.1993.tb05844.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pines J. Cyclins and cyclin-dependent kinases: take your partners. Trends Biochem Sci. 1993 Jun;18(6):195–197. doi: 10.1016/0968-0004(93)90185-p. [DOI] [PubMed] [Google Scholar]
  23. Pines J., Hunter T. Human cyclin A is adenovirus E1A-associated protein p60 and behaves differently from cyclin B. Nature. 1990 Aug 23;346(6286):760–763. doi: 10.1038/346760a0. [DOI] [PubMed] [Google Scholar]
  24. Reed S. I. G1-specific cyclins: in search of an S-phase-promoting factor. Trends Genet. 1991 Mar;7(3):95–99. doi: 10.1016/0168-9525(91)90279-Y. [DOI] [PubMed] [Google Scholar]
  25. Renaudin J. P., 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 U S A. 1994 Jul 19;91(15):7375–7379. doi: 10.1073/pnas.91.15.7375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Schwob E., Nasmyth K. CLB5 and CLB6, a new pair of B cyclins involved in DNA replication in Saccharomyces cerevisiae. Genes Dev. 1993 Jul;7(7A):1160–1175. doi: 10.1101/gad.7.7a.1160. [DOI] [PubMed] [Google Scholar]
  27. Sherr C. J. Mammalian G1 cyclins. Cell. 1993 Jun 18;73(6):1059–1065. doi: 10.1016/0092-8674(93)90636-5. [DOI] [PubMed] [Google Scholar]
  28. Soni R., Carmichael J. P., Shah Z. H., Murray J. A. A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell. 1995 Jan;7(1):85–103. doi: 10.1105/tpc.7.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Surana U., Amon A., Dowzer C., McGrew J., Byers B., Nasmyth K. 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):1969–1978. doi: 10.1002/j.1460-2075.1993.tb05846.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Swenson K. I., Farrell K. M., Ruderman J. V. The clam embryo protein cyclin A induces entry into M phase and the resumption of meiosis in Xenopus oocytes. Cell. 1986 Dec 26;47(6):861–870. doi: 10.1016/0092-8674(86)90801-9. [DOI] [PubMed] [Google Scholar]
  31. Yang W. C., de Blank C., Meskiene I., Hirt H., Bakker J., van Kammen A., Franssen H., Bisseling T. Rhizobium nod factors reactivate the cell cycle during infection and nodule primordium formation, but the cycle is only completed in primordium formation. Plant Cell. 1994 Oct;6(10):1415–1426. doi: 10.1105/tpc.6.10.1415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Zindy F., Lamas E., Chenivesse X., Sobczak J., Wang J., Fesquet D., Henglein B., Bréchot C. Cyclin A is required in S phase in normal epithelial cells. Biochem Biophys Res Commun. 1992 Feb 14;182(3):1144–1154. doi: 10.1016/0006-291x(92)91851-g. [DOI] [PubMed] [Google Scholar]

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