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. 1993 Feb 1;90(3):943–947. doi: 10.1073/pnas.90.3.943

Two functional soybean genes encoding p34cdc2 protein kinases are regulated by different plant developmental pathways.

G H Miao 1, Z Hong 1, D P Verma 1
PMCID: PMC45786  PMID: 8430109

Abstract

We have isolated two cDNA clones (cdc2-S5 and cdc2-S6) encoding p34cdc2 protein kinases, homologs of yeast cdc2/CDC28 genes, from a soybean nodule cDNA library. The two sequences share 90% sequence homology in the coding regions. The 5' and 3' noncoding regions are distinct from each other, however, indicating that at least two genes encode p34cdc2 protein kinases in soybean. Both sequences can rescue the cdc28 mutation in Saccharomyces cerevisiae but rescue it with different efficiency. Genomic Southern analysis showed the existence of two copies for each of these genes, which are not closely linked and are nonallelic. The relative expression level of the two soybean p34cdc2 genes varies in different tissues. Expression of cdc2-S5 is higher in roots and root nodules, whereas cdc2-S6 is more actively expressed in aerial tissues, indicating that regulation of these two p34cdc2 genes is coupled with plant developmental pathways. Expression of cdc2-S5 is, furthermore, enhanced after Rhizobium infection, whereas cdc2-S6 fails to respond, suggesting that cdc2-S5 plays a role in nodule initiation and organogenesis. This latter gene preferentially responds to auxin (alpha-naphthaleneacetic acid) treatment, indicating that phytohormones may be involved in the control of cell division mediated by Rhizobium infection. Thus, different p34cdc2 protein kinases may control cell division in different tissues in a multicellular organism and respond to different signals--e.g., phytohormones.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Carpenter J. L., Ploense S. E., Snustad D. P., Silflow C. D. Preferential expression of an alpha-tubulin gene of Arabidopsis in pollen. Plant Cell. 1992 May;4(5):557–571. doi: 10.1105/tpc.4.5.557. [DOI] [PMC free article] [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. Delauney A. J., Verma D. P. A soybean gene encoding delta 1-pyrroline-5-carboxylate reductase was isolated by functional complementation in Escherichia coli and is found to be osmoregulated. Mol Gen Genet. 1990 May;221(3):299–305. doi: 10.1007/BF00259392. [DOI] [PubMed] [Google Scholar]
  4. Draetta G., Beach D. Activation of cdc2 protein kinase during mitosis in human cells: cell cycle-dependent phosphorylation and subunit rearrangement. Cell. 1988 Jul 1;54(1):17–26. doi: 10.1016/0092-8674(88)90175-4. [DOI] [PubMed] [Google Scholar]
  5. Edwards J. W., Walker E. L., Coruzzi G. M. Cell-specific expression in transgenic plants reveals nonoverlapping roles for chloroplast and cytosolic glutamine synthetase. Proc Natl Acad Sci U S A. 1990 May;87(9):3459–3463. doi: 10.1073/pnas.87.9.3459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Elledge S. J., Spottswood M. R. A new human p34 protein kinase, CDK2, identified by complementation of a cdc28 mutation in Saccharomyces cerevisiae, is a homolog of Xenopus Eg1. EMBO J. 1991 Sep;10(9):2653–2659. doi: 10.1002/j.1460-2075.1991.tb07808.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fang F., Newport J. W. Evidence that the G1-S and G2-M transitions are controlled by different cdc2 proteins in higher eukaryotes. Cell. 1991 Aug 23;66(4):731–742. doi: 10.1016/0092-8674(91)90117-h. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Hanks S. K., Quinn A. M., Hunter T. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science. 1988 Jul 1;241(4861):42–52. doi: 10.1126/science.3291115. [DOI] [PubMed] [Google Scholar]
  10. Hata S., Kouchi H., Suzuka I., Ishii T. Isolation and characterization of cDNA clones for plant cyclins. EMBO J. 1991 Sep;10(9):2681–2688. doi: 10.1002/j.1460-2075.1991.tb07811.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hereford L. M., Hartwell L. H. Sequential gene function in the initiation of Saccharomyces cerevisiae DNA synthesis. J Mol Biol. 1974 Apr 15;84(3):445–461. doi: 10.1016/0022-2836(74)90451-3. [DOI] [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. Hirsch A. M., Bhuvaneswari T. V., Torrey J. G., Bisseling T. Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc Natl Acad Sci U S A. 1989 Feb;86(4):1244–1248. doi: 10.1073/pnas.86.4.1244. [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. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Keith B., Dong X. N., Ausubel F. M., Fink G. R. Differential induction of 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase genes in Arabidopsis thaliana by wounding and pathogenic attack. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8821–8825. doi: 10.1073/pnas.88.19.8821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Krek W., Nigg E. A. Structure and developmental expression of the chicken CDC2 kinase. EMBO J. 1989 Oct;8(10):3071–3078. doi: 10.1002/j.1460-2075.1989.tb08458.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lee M. G., Nurse P. Complementation used to clone a human homologue of the fission yeast cell cycle control gene cdc2. Nature. 1987 May 7;327(6117):31–35. doi: 10.1038/327031a0. [DOI] [PubMed] [Google Scholar]
  19. Lehner C. F., O'Farrell P. H. Drosophila cdc2 homologs: a functional homolog is coexpressed with a cognate variant. EMBO J. 1990 Nov;9(11):3573–3581. doi: 10.1002/j.1460-2075.1990.tb07568.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lewin B. Driving the cell cycle: M phase kinase, its partners, and substrates. Cell. 1990 Jun 1;61(5):743–752. doi: 10.1016/0092-8674(90)90181-d. [DOI] [PubMed] [Google Scholar]
  21. Lörincz A. T., Reed S. I. Primary structure homology between the product of yeast cell division control gene CDC28 and vertebrate oncogenes. Nature. 1984 Jan 12;307(5947):183–185. doi: 10.1038/307183a0. [DOI] [PubMed] [Google Scholar]
  22. MacNeill S. A., Creanor J., Nurse P. Isolation, characterisation and molecular cloning of new mutant alleles of the fission yeast p34cdc2+ protein kinase gene: identification of temperature-sensitive G2-arresting alleles. Mol Gen Genet. 1991 Sep;229(1):109–118. doi: 10.1007/BF00264219. [DOI] [PubMed] [Google Scholar]
  23. Mahmoudi M., Lin V. K. Comparison of two different hybridization systems in northern transfer analysis. Biotechniques. 1989 Apr;7(4):331-2, 334. [PubMed] [Google Scholar]
  24. Martinez M. C., Jørgensen J. E., Lawton M. A., Lamb C. J., Doerner P. W. Spatial pattern of cdc2 expression in relation to meristem activity and cell proliferation during plant development. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7360–7364. doi: 10.1073/pnas.89.16.7360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nurse P., Bissett Y. Gene required in G1 for commitment to cell cycle and in G2 for control of mitosis in fission yeast. Nature. 1981 Aug 6;292(5823):558–560. doi: 10.1038/292558a0. [DOI] [PubMed] [Google Scholar]
  26. Nurse P. Universal control mechanism regulating onset of M-phase. Nature. 1990 Apr 5;344(6266):503–508. doi: 10.1038/344503a0. [DOI] [PubMed] [Google Scholar]
  27. Olson D. C., White J. A., Edelman L., Harkins R. N., Kende H. Differential expression of two genes for 1-aminocyclopropane-1-carboxylate synthase in tomato fruits. Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5340–5344. doi: 10.1073/pnas.88.12.5340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Reed S. I., Hadwiger J. A., Lörincz A. T. Protein kinase activity associated with the product of the yeast cell division cycle gene CDC28. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4055–4059. doi: 10.1073/pnas.82.12.4055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Reed S. I., Wittenberg C. Mitotic role for the Cdc28 protein kinase of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5697–5701. doi: 10.1073/pnas.87.15.5697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Stein G. H., Drullinger L. F., Robetorye R. S., Pereira-Smith O. M., Smith J. R. Senescent cells fail to express cdc2, cycA, and cycB in response to mitogen stimulation. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11012–11016. doi: 10.1073/pnas.88.24.11012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Surana U., Robitsch H., Price C., Schuster T., Fitch I., Futcher A. B., Nasmyth K. The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae. Cell. 1991 Apr 5;65(1):145–161. doi: 10.1016/0092-8674(91)90416-v. [DOI] [PubMed] [Google Scholar]
  32. Verma DPS. Signals in Root Nodule Organogenesis and Endocytosis of Rhizobium. Plant Cell. 1992 Apr;4(4):373–382. doi: 10.1105/tpc.4.4.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Wang A. M., Doyle M. V., Mark D. F. Quantitation of mRNA by the polymerase chain reaction. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9717–9721. doi: 10.1073/pnas.86.24.9717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Yip W. K., Moore T., Yang S. F. Differential accumulation of transcripts for four tomato 1-aminocyclopropane-1-carboxylate synthase homologs under various conditions. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2475–2479. doi: 10.1073/pnas.89.6.2475. [DOI] [PMC free article] [PubMed] [Google Scholar]

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