Home LiteratureArticle Details
PMID: 16593592 Published · ppublish English Journal Article

Nonsense mutations in the Chlamydomonas chloroplast gene that codes for the large subunit of ribulosebisphosphate carboxylase/oxygenase.

Spreitzer RJ, Goldschmidt-Clermont M, Rahire M, Rochaix JD

Abstract

The Chlamydomonas reinhardtii chloroplast mutants 18-5B and 18-7G lack both the chloroplast-encoded large subunit and nuclear-encoded small subunit of the chloroplast enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (EC 4.1.1.39). A chloroplast intergenic-suppression model has been postulated to account for the genetic instability of 18-5B revertants. Here, we have determined the molecular basis of the 18-5B and 18-7G mutants. They contain nonsense mutations close to the 3' and 5' ends of their large-subunit genes, respectively. Pulse-chase experiments revealed that the 18-5B mutant produces a truncated large subunit that is unstable. In connection with previous experiments, this work identifies nonsense suppression in the chloroplast. Small subunits are also synthesized but then degraded in the mutants. Thus, the coordinated absence of subunits is achieved through degradation of the small subunit in the specific absence of the large subunit.

Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Spreitzer R J
Department of Molecular Biology, University of Geneva, 1211 Geneva 4, Switzerland.
Goldschmidt-Clermont M
Rahire M
Rochaix J D
References (38)
38 references, click to expand
  1. Transport of proteins into mitochondria and chloroplasts.
    J Cell Biol. 1979 Jun;81(3):461-83 PMID: 379018
  2. Interference of nonsense mutations with eukaryotic messenger RNA stability.
    Proc Natl Acad Sci U S A. 1979 Oct;76(10):5134-7 PMID: 388431
  3. Formation of the small subunit in the absence of the large subunit of ribulose 1,5-bisphosphate carboxylase in 70 S ribosome-deficient rye leaves.
    Arch Biochem Biophys. 1978 Mar;186(2):283-91 PMID: 416757
  4. Screening lambdagt recombinant clones by hybridization to single plaques in situ.
    Science. 1977 Apr 8;196(4286):180-2 PMID: 322279
  5. Translation and mRNA decay.
    Mol Gen Genet. 1978 Apr 6;160(2):121-9 PMID: 349350
  6. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease.
    Biochemistry. 1979 Nov 27;18(24):5294-9 PMID: 518835
  7. The biosynthesis of ribulose bisphosphate carboxylase. Uncoupling of the synthesis of the large and small subunits in isolated soybean leaf cells.
    Eur J Biochem. 1979 Feb 15;94(1):165-77 PMID: 571334
  8. RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination.
    Biochemistry. 1977 Oct 18;16(21):4743-51 PMID: 911786
  9. The structure of form I crystals of D-ribulose-1,5-diphosphate carboxylase.
    J Mol Biol. 1975 Feb 5;91(4):391-9 PMID: 1152035
  10. Quantitative film detection of 3H and 14C in polyacrylamide gels by fluorography.
    Eur J Biochem. 1975 Aug 15;56(2):335-41 PMID: 1175627
  11. Evidence for essential lysyl residues in ribulosebisphosphate carboxylase by use of the affinity label 3-bromo-1,4-dihydroxy-2-butanone 1,4-bisphosphate.
    J Biol Chem. 1975 Oct 25;250(20):8062-8 PMID: 1176459
  12. 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):577-91 PMID: 4350343
  13. Hyper-labile messenger RNA in polar mutants of the tryptophan operon of Escherichia coli.
    J Mol Biol. 1972 Dec 14;72(1):103-10 PMID: 4567396
  14. Calcium-dependent bacteriophage DNA infection.
    J Mol Biol. 1970 Oct 14;53(1):159-62 PMID: 4922220
  15. A membrane-filter technique for the detection of complementary DNA.
    Biochem Biophys Res Commun. 1966 Jun 13;23(5):641-6 PMID: 5963888
  16. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose.
    Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201-5 PMID: 6159641
  17. Regulation of the synthesis of ribulose-1,5-bisphosphate carboxylase and its subunits in the flagellate Chlorogonium elongatum. Different levels of translatable messenger RNAs for the large and the small subunits in autotrophic and heterotrophic cells as determined by immunological techniques.
    Eur J Biochem. 1981 May 15;116(2):261-7 PMID: 6166473
  18. Efficient isolation of genes by using antibody probes.
    Proc Natl Acad Sci U S A. 1983 Mar;80(5):1194-8 PMID: 6219389
  19. Overlap and cotranscription of the genes for the beta and epsilon subunits of tobacco chloroplast ATPase.
    Gene. 1983 Oct;24(2-3):147-55 PMID: 6227526
  20. The barley chloroplast DNA atpBE, trnM2, and trnV1 loci.
    Nucleic Acids Res. 1984 Mar 12;12(5):2549-59 PMID: 6231529
  21. Light regulation of specific mRNA species in Lemna gibba L. G-3.
    Proc Natl Acad Sci U S A. 1978 Oct;75(10):4749-53 PMID: 16592577
  22. Structures of the genes for the beta and epsilon subunits of spinach chloroplast ATPase indicate a dicistronic mRNA and an overlapping translation stop/start signal.
    Proc Natl Acad Sci U S A. 1982 Oct;79(20):6260-4 PMID: 16593238
  23. Light-dependent assembly of ribulose-1,5-bisphosphate carboxylase.
    Proc Natl Acad Sci U S A. 1983 Feb;80(4):1013-7 PMID: 16593277
  24. Rapid degradation of unassembled ribulose 1,5-bisphosphate carboxylase small subunits in chloroplasts.
    Proc Natl Acad Sci U S A. 1983 May;80(9):2632-6 PMID: 16593310
  25. Rapid recovery of chloroplast mutations affecting ribulosebisphosphate carboxylase/oxygenase in Chlamydomonas reinhardtii.
    Proc Natl Acad Sci U S A. 1983 Oct;80(20):6293-7 PMID: 16593382
  26. Regulation of Soybean Net Photosynthetic CO(2) Fixation by the Interaction of CO(2), O(2), and Ribulose 1,5-Diphosphate Carboxylase.
    Plant Physiol. 1974 Nov;54(5):678-85 PMID: 16658951
  27. Photosynthesis-deficient Mutants of Chlamydomonas reinhardii with Associated Light-sensitive Phenotypes.
    Plant Physiol. 1981 Mar;67(3):565-9 PMID: 16661715
  28. Linkage of a Known Chloroplast Gene Mutation to the Uniparental Genome of CHLAMYDOMONAS REINHARDII.
    Genetics. 1983 Nov;105(3):559-79 PMID: 17246167
  29. Sequencing end-labeled DNA with base-specific chemical cleavages.
    Methods Enzymol. 1980;65(1):499-560 PMID: 6246368
  30. Restriction fragments from Chlamydomonas chloroplast DNA.
    Methods Enzymol. 1980;65(1):785-95 PMID: 6246374
  31. Construction and characterization of new cloning vehicles. IV. Deletion derivatives of pBR322 and pBR325.
    Gene. 1980 May;9(3-4):287-305 PMID: 6248430
  32. Terminal repeats of the Drosophila transposable element copia: nucleotide sequence and genomic organization.
    Cell. 1980 Sep;21(2):581-8 PMID: 6250726
  33. The structure of the gene for the large subunit of ribulose 1,5-bisphosphate carboxylase from spinach chloroplast DNA.
    Nucleic Acids Res. 1981 Jul 24;9(14):3251-70 PMID: 6269077
  34. The maize chloroplast genes for the beta and epsilon subunits of the photosynthetic coupling factor CF1 are fused.
    Nucleic Acids Res. 1982 Aug 25;10(16):4985-5002 PMID: 6290998
  35. Sequence of the chloroplast DNA region of Chlamydomonas reinhardii containing the gene of the large subunit of ribulose bisphosphate carboxylase and parts of its flanking genes.
    J Mol Biol. 1982 Dec 25;162(4):775-93 PMID: 6302265
  36. Structure and topology of cytochrome f in pea chloroplast membranes.
    Cell. 1984 Feb;36(2):555-62 PMID: 6319031
  37. Ribulose-1,5-bisphosphate carboxylase-oxygenase.
    Annu Rev Biochem. 1983;52:507-35 PMID: 6351728
  38. First DNA sequence of a chloroplast mutation: a missense alteration in the ribulosebisphosphate carboxylase large subunit gene.
    Plasmid. 1983 May;9(3):321-4 PMID: 6867163
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1985-08-00
Pages
5460-4
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC390589
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]