Cell cycle stage-specific accumulation of mRNAs encoding tubulin and other polypeptides in Chlamydomonas.

Proc Natl Acad Sci U S A. 1982 September; 79(18): 5577–5581.

PMCID: PMC346947

M Ares, Jr and S H Howell

This article has been cited by other articles in PMC.

Abstract

The accumulation pattern of a number of mRNAs during the cell cycle of Chlamydomonas was examined by two-dimensional gel analysis of in vitro translation products and by RNA blot hybridization analysis. Two-dimensional gel analysis revealed that 10-15% of the 300 most abundant translation products are differentially synthesized from RNA obtained at various cell cycle stages. RNAs that direct the synthesis of alpha- and beta-tubulins and that hybridize to cloned alpha- and beta-tubulin probes accumulate coordinately during the predivision period of the cell cycle, reaching peak levels before or during division. Other RNAs represented by selected cloned cDNA probes show a number of different cell cycle patterns of accumulation. The accumulation patterns of these RNAs are not directly influenced by ongoing illumination conditions, even though alternating light-dark illumination cycles are used to synchronize Chlamydomonas cells. The results suggest that there may be a complex program of gene expression correlated with cell cycle progression in Chlamydomonas.

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Hartwell, LH. Cell division from a genetic perspective. J Cell Biol. 1978 Jun;77(3):627–637. [PubMed]
Elliott, SG; McLaughlin, CS. Rate of macromolecular synthesis through the cell cycle of the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4384–4388. [PubMed]
Bravo, R; Celis, JE. A search for differential polypeptide synthesis throughout the cell cycle of HeLa cells. J Cell Biol. 1980 Mar;84(3):795–802. [PubMed]
Hereford, LM; Osley, MA; Ludwig, TR, 2nd; McLaughlin, CS. Cell-cycle regulation of yeast histone mRNA. Cell. 1981 May;24(2):367–375. [PubMed]
Groppi, VE, Jr; Coffino, P. G1 and S phase mammalian cells synthesize histones at equivalent rates. Cell. 1980 Aug;21(1):195–204. [PubMed]
Spalding, J; Kajiwara, K; Mueller, GC. The metabolism of basic proteins in HeLa cell nuclei. Proc Natl Acad Sci U S A. 1966 Nov;56(5):1535–1542. [PubMed]
Robbins, Elliott; Borun, Thaddeus W. THE CYTOPLASMIC SYNTHESIS OF HISTONES IN HELA CELLS AND ITS TEMPORAL RELATIONSHIP TO DNA REPLICATION. Proc Natl Acad Sci U S A. 1967 Feb;57(2):409–416. [PubMed]
Stein, GS; Borun, TW. The synthesis of acidic chromosomal proteins during the cell cycle of HeLa S-3 cells. I. The accelerated accumulation of acidic residual nuclear protein before the initiation of DNA replication. J Cell Biol. 1972 Feb;52(2):292–307. [PubMed]
Delegeane, AM; Lee, AS. Coupling of histone and DNA synthesis in the somatic cell cycle. Science. 1982 Jan 1;215(4528):79–81. [PubMed]
Rickles, R; Marashi, F; Sierra, F; Clark, S; Wells, J; Stein, J; Stein, G. Analysis of histone gene expression during the cell cycle in HeLa cells by using cloned human histone genes. Proc Natl Acad Sci U S A. 1982 Feb;79(3):749–753. [PubMed]
Laffler, TG; Chang, MT; Dove, WF. Periodic synthesis of microtubular proteins in the cell cycle of Physarum. Proc Natl Acad Sci U S A. 1981 Aug;78(8):5000–5004. [PubMed]
Howell, SH; Posakony, JW; Hill, KR. The cell cycle program of polypeptide labeling in Chlamydomonas reinhardtii. J Cell Biol. 1977 Feb;72(2):223–241. [PubMed]
Weeks, DP; Collis, PS. Induction and synthesis of tubulin during the cell cycle and life cycle of Chlamydomonas reinhardi. Dev Biol. 1979 Apr;69(2):400–407. [PubMed]
Sueoka, N; Chiang, KS; Kates, JR. Deoxyribonucleic acid replication in meiosis of Chlamydomonas reinhardi. I. Isotopic transfer experiments with a strain producing eight zoospores. J Mol Biol. 1967 Apr 14;25(1):47–66. [PubMed]
Witman, GB; Carlson, K; Berliner, J; Rosenbaum, JL. Chlamydomonas flagella. I. Isolation and electrophoretic analysis of microtubules, matrix, membranes, and mastigonemes. J Cell Biol. 1972 Sep;54(3):507–539. [PubMed]
Weeks, DP; Collis, P; Gealt, MA. Control of induction of tubulin synthesis in Chlamydomonas reinhardi. Nature. 1977 Aug 18;268(5621):667–668. [PubMed]
Glisin, V; Crkvenjakov, R; Byus, C. Ribonucleic acid isolated by cesium chloride centrifugation. Biochemistry. 1974 Jun 4;13(12):2633–2637. [PubMed]
Weeks, DP; Collis, PS. Induction of microtubule protein synthesis in Chlamydomonas reinhardi during flagellar regeneration. Cell. 1976 Sep;9(1):15–27. [PubMed]
Silflow, CD; Rosenbaum, JL. Multiple alpha- and beta-tubulin genes in Chlamydomonas and regulation of tubulin mRNA levels after deflagellation. Cell. 1981 Apr;24(1):81–88. [PubMed]
Lefebvre, PA; Silflow, CD; Wieben, ED; Rosenbaum, JL. Increased levels of mRNAs for tubulin and other flagellar proteins after amputation or shortening of Chlamydomonas flagella. Cell. 1980 Jun;20(2):469–477. [PubMed]
O'Farrell, PH. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PubMed]
Bonner, WM; Laskey, RA. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem. 1974 Jul 1;46(1):83–88. [PubMed]
Cleveland, DW; Lopata, MA; MacDonald, RJ; Cowan, NJ; Rutter, WJ; Kirschner, MW. Number and evolutionary conservation of alpha- and beta-tubulin and cytoplasmic beta- and gamma-actin genes using specific cloned cDNA probes. Cell. 1980 May;20(1):95–105. [PubMed]
Buell, GN; Wickens, MP; Payvar, F; Schimke, RT. Synthesis of full length cDNAs from four partially purified oviduct mRNAs. J Biol Chem. 1978 Apr 10;253(7):2471–2482. [PubMed]
Wickens, MP; Buell, GN; Schimke, RT. Synthesis of double-stranded DNA complementary to lysozyme, ovomucoid, and ovalbumin mRNAs. Optimization for full length second strand synthesis by Escherichia coli DNA polymerase I. J Biol Chem. 1978 Apr 10;253(7):2483–2495. [PubMed]
Roychoudhury, R; Jay, E; Wu, R. Terminal labeling and addition of homopolymer tracts to duplex DNA fragments by terminal deoxynucleotidyl transferase. Nucleic Acids Res. 1976 Jan;3(1):101–116. [PubMed]
Grunstein, M; Wallis, J. Colony hybridization. Methods Enzymol. 1979;68:379–389. [PubMed]
Kahn, M; Kolter, R; Thomas, C; Figurski, D; Meyer, R; Remaut, E; Helinski, DR. Plasmid cloning vehicles derived from plasmids ColE1, F, R6K, and RK2. Methods Enzymol. 1979;68:268–280. [PubMed]
Southern, EM. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. [PubMed]
Wahl, GM; Stern, M; Stark, GR. Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization by using dextran sulfate. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3683–3687. [PubMed]
Bailey, JM; Davidson, N. Methylmercury as a reversible denaturing agent for agarose gel electrophoresis. Anal Biochem. 1976 Jan;70(1):75–85. [PubMed]
Thomas, PS. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. [PubMed]
Rigby, PW; Dieckmann, M; Rhodes, C; Berg, P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. [PubMed]
Herrmann, R; Neugebauer, K; Pirkl, E; Zentgraf, H; Schaller, H. Conversion of bacteriophage fd into an efficient single-stranded DNA vector system. Mol Gen Genet. 1980 Jan;177(2):231–242. [PubMed]
Cavalier-Smith, T. Basal body and flagellar development during the vegetative cell cycle and the sexual cycle of Chlamydomonas reinhardii. J Cell Sci. 1974 Dec;16(3):529–556. [PubMed]
Rosenbaum, JL; Moulder, JE; Ringo, DL. Flagellar elongation and shortening in Chlamydomonas. The use of cycloheximide and colchicine to study the synthesis and assembly of flagellar proteins. J Cell Biol. 1969 May;41(2):600–619. [PubMed]
Lefebvre, PA; Nordstrom, SA; Moulder, JE; Rosenbaum, JL. Flagellar elongation and shortening in Chlamydomonas. IV. Effects of flagellar detachment, regeneration, and resorption on the induction of flagellar protein synthesis. J Cell Biol. 1978 Jul;78(1):8–27. [PubMed]
Minami, SA; Collis, PS; Young, EE; Weeks, DP. Tubulin induction in C. reinhardii: requirement for tubulin mRNA synthesis. Cell. 1981 Apr;24(1):89–95. [PubMed]