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. 1981 Jul 24;9(14):3251–3270. doi: 10.1093/nar/9.14.3251

The structure of the gene for the large subunit of ribulose 1,5-bisphosphate carboxylase from spinach chloroplast DNA.

G Zurawski, B Perrot, W Bottomley, P R Whitfeld
PMCID: PMC327350  PMID: 6269077

Abstract

A cloned fragment of spinach chloroplast DNA carrying the gene for the large subunit of ribulose bisphosphate (RuBP) carboxylase has been analysed by electron microscopy of R-loops, by hybridization to Northern blots of chloroplast RNA, by S1 nuclease mapping and by DNA sequencing. The transcribed region of the gene is 1690 +/- 3 nucleotides long and co-linear with its mRNA. It comprises a 178-179 bp 5' untranslated sequence, a 1425 bp coding region and an 85-88 bp 3' untranslated region. The deduced sequence of the 475 amino acids of the spinach large subunit protein shows 10% divergence from that of the maize large subunit protein (1). The nucleotide sequence divergence between spinach and maize over the same coding region is 16% but in the transcribed flanking regions it is 35%. Features of the spinach chloroplast gene which resemble those of bacterial genes include a 5-base Shine-Dalgarno sequence complementary to a sequence near the 3' end of chloroplast and bacterial 16S rRNA, a promoter region partially homologous to a consensus sequence of bacterial promoters, and a transcription termination region capable of forming a typical stem and loop structure.

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Selected References

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

  1. Alwine J. C., Kemp D. J., Stark G. R. Method for detection of specific RNAs in agarose gels by transfer to diazobenzyloxymethyl-paper and hybridization with DNA probes. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5350–5354. doi: 10.1073/pnas.74.12.5350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bailey J. M., Davidson N. Methylmercury as a reversible denaturing agent for agarose gel electrophoresis. Anal Biochem. 1976 Jan;70(1):75–85. doi: 10.1016/s0003-2697(76)80049-8. [DOI] [PubMed] [Google Scholar]
  3. Bedbrook J. R., Coen D. M., Beaton A. R., Bogorad L., Rich A. Location of the single gene for the large subunit of ribulosebisphosphate carboxylase on the maize chloroplast chromosome. J Biol Chem. 1979 Feb 10;254(3):905–910. [PubMed] [Google Scholar]
  4. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  5. Blair G. E., Ellis R. J. Protein synthesis in chloroplasts. I. Light-driven synthesis of the large subunit of fraction I protein by isolated pea chloroplasts. Biochim Biophys Acta. 1973 Aug 24;319(2):223–234. doi: 10.1016/0005-2787(73)90013-0. [DOI] [PubMed] [Google Scholar]
  6. Borer P. N., Dengler B., Tinoco I., Jr, Uhlenbeck O. C. Stability of ribonucleic acid double-stranded helices. J Mol Biol. 1974 Jul 15;86(4):843–853. doi: 10.1016/0022-2836(74)90357-x. [DOI] [PubMed] [Google Scholar]
  7. Bottomley W., Whitfeld P. R. Cell-free transcription and translation of total spinach chloroplast DNA. Eur J Biochem. 1979 Jan 2;93(1):31–39. doi: 10.1111/j.1432-1033.1979.tb12791.x. [DOI] [PubMed] [Google Scholar]
  8. Chan P. H., Wildman S. G. Chloroplast DNA codes for the primary structure of the large subunit of fraction I protein. Biochim Biophys Acta. 1972 Sep 14;277(3):677–680. doi: 10.1016/0005-2787(72)90115-3. [DOI] [PubMed] [Google Scholar]
  9. Chua N. H., Schmidt G. W. Post-translational transport into intact chloroplasts of a precursor to the small subunit of ribulose-1,5-bisphosphate carboxylase. Proc Natl Acad Sci U S A. 1978 Dec;75(12):6110–6114. doi: 10.1073/pnas.75.12.6110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Coen D. M., Bedbrook J. R., Bogorad L., Rich A. Maize chloroplast DNA fragment encoding the large subunit of ribulosebisphosphate carboxylase. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5487–5491. doi: 10.1073/pnas.74.12.5487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Crick F. H. Codon--anticodon pairing: the wobble hypothesis. J Mol Biol. 1966 Aug;19(2):548–555. doi: 10.1016/s0022-2836(66)80022-0. [DOI] [PubMed] [Google Scholar]
  12. Dobberstein B., Blobel G., Chua N. H. In vitro synthesis and processing of a putative precursor for the small subunit of ribulose-1,5-bisphosphate carboxylase of Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A. 1977 Mar;74(3):1082–1085. doi: 10.1073/pnas.74.3.1082. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Driesel A. J., Crouse E. J., Gordon K., Bohnert H. J., Herrmann R. G., Steinmetz A., Mubumbila M., Keller M., Burkard G., Weil J. H. Fractionation and identification of spinach chloroplast transfer RNAs and mapping of their genes on the restriction map of chloroplast DNA. Gene. 1979 Aug;6(4):285–306. doi: 10.1016/0378-1119(79)90070-2. [DOI] [PubMed] [Google Scholar]
  14. Gerlach W. L., Dyer T. A. Sequence organization of the repeating units in the nucleus of wheat which contain 5S rRNA genes. Nucleic Acids Res. 1980 Nov 11;8(21):4851–4865. doi: 10.1093/nar/8.21.4851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gray J. C., Kekwick R. G. Synthesis of the small subunit of ribulose 1,5-diphosphate carboxylase on cytoplasmic ribosomes from greening bean leaves. FEBS Lett. 1973 Dec 15;38(1):67–69. doi: 10.1016/0014-5793(73)80515-0. [DOI] [PubMed] [Google Scholar]
  16. Katz L., Kingsbury D. T., Helinski D. R. Stimulation by cyclic adenosine monophosphate of plasmid deoxyribonucleic acid replication and catabolite repression of the plasmid deoxyribonucleic acid-protein relaxation complex. J Bacteriol. 1973 May;114(2):577–591. doi: 10.1128/jb.114.2.577-591.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kawashima N., Wildman S. G. Studies on fraction I protein. IV. Mode of inheritance of primary structure in relation to whether chloroplast or nuclear DNA contains the code for a chloroplast protein. Biochim Biophys Acta. 1972 Feb 23;262(1):42–49. doi: 10.1016/0005-2787(72)90217-1. [DOI] [PubMed] [Google Scholar]
  18. Korn L. J., Brown D. D. Nucleotide sequence of Xenopus borealis oocyte 5S DNA: comparison of sequences that flank several related eucaryotic genes. Cell. 1978 Dec;15(4):1145–1156. doi: 10.1016/0092-8674(78)90042-9. [DOI] [PubMed] [Google Scholar]
  19. Link G., Coen D. M., Bogorad L. Differential expression of the gene for the large subunit of ribulose bisphosphate carboxylase in maize leaf cell types. Cell. 1978 Nov;15(3):725–731. doi: 10.1016/0092-8674(78)90258-1. [DOI] [PubMed] [Google Scholar]
  20. Malnoë P., Rochaix J. D., Chua N. H., Spahr P. F. Characterization of the gene and messenger RNA of the large subunit of ribulose 1,5-diphosphate carboxylase in Chlamydomonas reinhardii. J Mol Biol. 1979 Sep 25;133(3):417–434. doi: 10.1016/0022-2836(79)90401-7. [DOI] [PubMed] [Google Scholar]
  21. Maniatis T., Kee S. G., Efstratiadis A., Kafatos F. C. Amplification and characterization of a beta-globin gene synthesized in vitro. Cell. 1976 Jun;8(2):163–182. doi: 10.1016/0092-8674(76)90001-5. [DOI] [PubMed] [Google Scholar]
  22. Maxam A. M., Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. doi: 10.1073/pnas.74.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  24. Nishimura M., Akazawa T. Further proof for the catalytic role of the larger subunit in the spinach leaf ribulose-1,5-diphosphate carboxylase. Biochem Biophys Res Commun. 1973 Oct 1;54(3):842–848. doi: 10.1016/0006-291x(73)90770-5. [DOI] [PubMed] [Google Scholar]
  25. Rosenberg M., Court D. Regulatory sequences involved in the promotion and termination of RNA transcription. Annu Rev Genet. 1979;13:319–353. doi: 10.1146/annurev.ge.13.120179.001535. [DOI] [PubMed] [Google Scholar]
  26. Sanger F., Coulson A. R. A rapid method for determining sequences in DNA by primed synthesis with DNA polymerase. J Mol Biol. 1975 May 25;94(3):441–448. doi: 10.1016/0022-2836(75)90213-2. [DOI] [PubMed] [Google Scholar]
  27. Scherer G. F., Walkinshaw M. D., Arnott S., Morré D. J. The ribosome binding sites recognized by E. coli ribosomes have regions with signal character in both the leader and protein coding segments. Nucleic Acids Res. 1980 Sep 11;8(17):3895–3907. doi: 10.1093/nar/8.17.3895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Shine J., Dalgarno L. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1342–1346. doi: 10.1073/pnas.71.4.1342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Siebenlist U. Nucleotide sequence of the three major early promoters of bacteriophage T7. Nucleic Acids Res. 1979;6(5):1895–1907. doi: 10.1093/nar/6.5.1895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Stringer C. D., Hartman F. C. Sequences of two active-site peptides from spinach ribulosebisphosphate carboxylase/oxygenase. Biochem Biophys Res Commun. 1978 Feb 28;80(4):1043–1048. doi: 10.1016/0006-291x(78)91351-7. [DOI] [PubMed] [Google Scholar]
  31. Sugiyama T., Akazawa T. Subunit structure of spinach leaf ribulose 1,5-diphosphate carboxylase. Biochemistry. 1970 Nov 10;9(23):4499–4504. doi: 10.1021/bi00825a006. [DOI] [PubMed] [Google Scholar]
  32. Thomas M., White R. L., Davis R. W. Hybridization of RNA to double-stranded DNA: formation of R-loops. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2294–2298. doi: 10.1073/pnas.73.7.2294. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tinoco I., Jr, Borer P. N., Dengler B., Levin M. D., Uhlenbeck O. C., Crothers D. M., Bralla J. Improved estimation of secondary structure in ribonucleic acids. Nat New Biol. 1973 Nov 14;246(150):40–41. doi: 10.1038/newbio246040a0. [DOI] [PubMed] [Google Scholar]
  34. Whitfeld P. R., Herrmann R. G., Bottomley W. Mapping of the ribosomal RNA genes on spinach chloroplast DNA. Nucleic Acids Res. 1978 Jun;5(6):1741–1751. doi: 10.1093/nar/5.6.1741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Whitfeld P. R., Spencer D. Buoyant density of tobacco and spinach chloroplast DNA. Biochim Biophys Acta. 1968 Apr 22;157(2):333–343. doi: 10.1016/0005-2787(68)90087-7. [DOI] [PubMed] [Google Scholar]
  36. Wienand U., Schwarz Z., Feix G. Electrophoretic elution of nucleic acids from gels adapted for subsequent biological tests. Application for analysis of mRNAs from maize endosperm. FEBS Lett. 1979 Feb 15;98(2):319–323. doi: 10.1016/0014-5793(79)80208-2. [DOI] [PubMed] [Google Scholar]
  37. Wu R. Nucleotide sequence analysis of DNA. I. Partial sequence of the cohesive ends of bacteriophage lambda and 186 DNA. J Mol Biol. 1970 Aug;51(3):501–521. doi: 10.1016/0022-2836(70)90004-5. [DOI] [PubMed] [Google Scholar]
  38. Zurawski G., Yanofsky C. Escherichia coli tryptophan operon leader mutations, which relieve transcription termination, are cis-dominant to trp leader mutations, which increase transcription termination. J Mol Biol. 1980 Sep 5;142(1):123–129. doi: 10.1016/0022-2836(80)90210-7. [DOI] [PubMed] [Google Scholar]

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