Home LiteratureArticle Details
PMID: 128689 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Chloroplast genes in Chlamydomonas affecting organelle ribosomes. Genetic and biochemical analysis of analysis of antibiotic-resistant mutants at several gene loci.

Molecular & general genetics : MGG ·Vol. 140 ·No. 3 ·1975-10-03 ·Pages 183-220

Conde MF, Boynton JE, Gillham NW, Harris EH, Tingle CL, Wang WL

Abstract

Six chloroplast gene mutants of Chlamydomonas reinhardtii resistant to spectinomycin, erythromycin, or streptomycin have been assessed for antibiotic resistance of their chloroplast ribosomes. Four of these mutations clearly confer high levels of antibiotic resistance on the chloroplast ribosomes both in vivo. Although one mutant resistant to streptomycin and one resistant to spectinomycin have chloroplast ribosomes as sensitive to antibiotics as those of wild type in vivo, these mutations can be shown to alter the wildtype sensitivity of chloroplast ribosomes in polynucleotide-directed amino acid incorporation in vitro. Genetic analysis of these six chloroplast mutants and three similar mutants (Sager, 1972), two of which have been shown to affect chloroplast ribosomes (Mets and Bogorad, 1972; Schlanger and Sager, 1974), indicates that in Chlamydomonas at least three chloroplast gene loci can affect streptomycin resistance of chloroplast ribosomes and that two can affect erythromycin resistance. The three spectinomycin-resistant mutants examined appear to be alleles at a single chloroplast gene locus, but may represent mutations at two different sites within the same gene. Unlike wild type, the streptomycin and spectinomycin resistant mutants which have chloroplast ribosomes sensitive to antibiotics in vivo, grow well in the presence of antibiotic by respiring exogenously supplied acetate as a carbon source, and have normal levels of cytochrome oxidase activity and cyanide-sensitive respiration. We conclude that mitochondrial protein synthesis in these mutants is resistant to these antibiotics, whereas in wild type it is sensitive. To explain the behavior of these two chloroplast gene mutants as well as other one-step mutants which are resistant both photosynthetically and when respiring acetate in the dark, we have postulated that a mutation in a single chloroplast gene may result in alteration of both chloroplast and mitochondrial ribosomes. Mitochondrial resistance would appear to be the minimal necessary condition for survival of all such mutants, and antibiotic-resistant chloroplast ribosomes would be necessary for survival only under photosynthetic conditions.

MeSH Terms
Chlamydomonas/ultrastructure Chloroplasts Drug Resistance, Microbial/drug effects Erythromycin/pharmacology Extrachromosomal Inheritance Genetic Linkage Microscopy, Electron Mutation Ribosomes/metabolism Spectinomycin/pharmacology Streptomycin/pharmacology
Chemicals
Erythromycin Spectinomycin Streptomycin
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Conde M F
Boynton J E
Gillham N W
Harris E H
Tingle C L
Wang W L
References (70)
70 references, click to expand
  1. Formation of chloroplast membranes in Chlamydomonas reinhardi y-1. Effects of inhibitors of protein synthesis.
    J Biol Chem. 1969 May 25;244(10):2621-31 PMID: 5769994
  2. Regulation of nuclear DNA replication by thechloroplast in Chlamydomonas.
    Proc Natl Acad Sci U S A. 1974 Jul;71(7):2867-71 PMID: 4277629
  3. Isolation of cytoplasmic and chloroplast ribosomes and their dissociation into active subunits from Chlamydomonas reinhardtii.
    J Cell Biol. 1973 Jun;57(3):798-814 PMID: 4698907
  4. A major polypeptide of chloroplast membranes of Chlamydomonas reinhardi. Evidence for synthesis in the cytoplasm as a soluble component.
    J Cell Biol. 1972 Jan;52(1):84-96 PMID: 5006949
  5. Antibiotic inhibitors of the bacterial ribosome.
    Bacteriol Rev. 1968 Dec;32(4 Pt 2):493-528 PMID: 4179192
  6. Altered ribosomal protein in streptomycin-dependent Escherichia coli.
    Science. 1969 Dec 5;166(3910):1282-4 PMID: 4900367
  7. Nuclear and chloroplast control of chloroplast structure and function in Chlamydomonas reinhardi.
    Symp Soc Exp Biol. 1970;24:13-37 PMID: 4252602
  8. MITOTIC REPLICATION OF DEOXYRIBONUCLEIC ACID IN CHLAMYDOMONAS REINHARDI.
    Proc Natl Acad Sci U S A. 1960 Jan;46(1):83-91 PMID: 16590601
  9. [The effect of streptomycin and neamine on the structure of chloroplast and mitochondria in Chlamydomonas reinhardii (author's transl)].
    Protoplasma. 1974;82(1):77-89 PMID: 4411142
  10. Chloroplast structure and function in ac-20, a mutant strain of Chlamydomonas reinhardi. 3. Chloroplast ribosomes and membrane organization.
    J Cell Biol. 1970 Mar;44(3):547-62 PMID: 5415236
  11. 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):223-34 PMID: 4748357
  12. Biosynthesis of mitochondrial enzymes.
    Biochim Biophys Acta. 1973 Feb 12;301(1):71-104 PMID: 4350388
  13. A microspectrophotometric method for the determination of cytochrome oxidase.
    J Biol Chem. 1951 Apr;189(2):665-70 PMID: 14832284
  14. Mapping a cluster of ribosomal genes in Escherichia coli.
    Mol Gen Genet. 1974;133(4):317-27 PMID: 4280012
  15. Comparison of the respiratory chain of Neurospora crassa wild type and the mi-mutants mi-1 and mi-3.
    Eur J Biochem. 1973 Feb 15;33(1):140-57 PMID: 4144164
  16. Cytochrome b in Neurospora crassa mitochondria. A membrane protein containing subunits of cytoplasmic and mitochondrial origin.
    Eur J Biochem. 1972 Nov 7;30(3):469-78 PMID: 4264399
  17. Cyanide-insensitive respiration. An alternative mitochondrial pathway.
    Subcell Biochem. 1975 Mar;4(1):1-65 PMID: 1091028
  18. Proteins of mitochondrial and cytoplasmic ribosomes from Neurospora crassa.
    Nature. 1969 Apr 12;222(5189):142-6 PMID: 5777034
  19. Chloroplast structure and function in ac-20, a mutant strain of Chlamydomonas reinhardi. I. CO2 fixation and ribulose-1,5-diphosphate carboxylase synthesis.
    J Cell Biol. 1970 Mar;44(3):531-9 PMID: 4984375
  20. Proteins of cytoplasmic, chloroplast, and mitochondrial ribosomes of some plants.
    Biochim Biophys Acta. 1971 Jan 28;228(2):492-502 PMID: 4993620
  21. Ribosomal proteins. XXXVII. Determination of allelle types and amino acid exchanges in protein S12 of three streptomycin-resistant mutants of Escherichia coli.
    Biochim Biophys Acta. 1972 Dec 6;287(2):282-91 PMID: 4609471
  22. Inhibitors of ribosome functions.
    Annu Rev Microbiol. 1971;25:487-562 PMID: 4949424
  23. The genetics of bacterial ribosomes.
    Annu Rev Genet. 1972;6:203-34 PMID: 4269096
  24. Biogenetic autonomy of mitochondria.
    CRC Crit Rev Biochem. 1973 Aug;1(3):381-460 PMID: 4609690
  25. Further similarities between chloroplast and bacterial ribosomes.
    Planta. 1970 Dec;91(4):329-35 PMID: 24500097
  26. Mitochondrial ribosomes.
    FEBS Lett. 1971 Feb 19;13(2):73-88 PMID: 11945636
  27. Mutations altering chloroplast ribosome phenotype in Chlamydomonas. I. Non-mendelian mutations.
    Proc Natl Acad Sci U S A. 1970 Oct;67(2):1026-33 PMID: 5289000
  28. Genetic analysis of streptomycin resistance in Escherichia coli.
    Genetics. 1970 May;65(1):9-25 PMID: 4920897
  29. Localization of extranuclear genes by investigations of the ultrastructure in Chlamydomonas reinhardii.
    Arch Mikrobiol. 1973;92(1):85-90 PMID: 4725825
  30. Studies on the structure and cellular location of various ribosome and ribosomal RNA species in the green alga Chlamydomonas reinhardi.
    J Cell Sci. 1971 Jan;8(1):153-83 PMID: 5552399
  31. Sites of synthesis of chloroplast membrane polypeptides in Chlamydomonas reinhardi y-1.
    J Biol Chem. 1970 Sep 10;245(17):4327-34 PMID: 5498419
  32. Organelle mutations and their expression in Chlamydomonas reinhardi.
    Proc Natl Acad Sci U S A. 1971 Jun;68(6):1301-6 PMID: 5288379
  33. Protein synthesis in Chlamydomonas reinhardi. Evidence for synthesis of proteins of chloroplastic ribosomes on cytoplasmic ribosomes.
    J Biol Chem. 1973 Sep 10;248(17):6145-53 PMID: 4726301
  34. [Localization of a non-Mendelian gene in Chlamydomonas reinhardii].
    Mol Gen Genet. 1972;114(3):266-72 PMID: 5015428
  35. Induction of cyanide-insensitive respiration in Neurospora crassa.
    J Biol Chem. 1974 Jun 10;249(11):3551-6 PMID: 4275427
  36. Differential synthesis of ribulosediphosphate carboxylase subunits.
    Biochem Biophys Res Commun. 1970 Nov 9;41(3):621-7 PMID: 5479291
  37. [The number of copies of an extranuclear gene in Chlamydomonas reinhardii].
    Mol Gen Genet. 1970;107(4):366-71 PMID: 5519982
  38. Attachment of chloroplast polysomes to thylakoid membranes in Chlamydomonas reinhardtii.
    Proc Natl Acad Sci U S A. 1973 May;70(5):1554-8 PMID: 4514325
  39. [Segregation and re-segregation of an extranuclear gene in Chlamydomonas reinhardii].
    Mol Gen Genet. 1970;108(1):33-40 PMID: 5472936
  40. Genetic analysis of the chloroplast and mitochondrial genomes.
    Annu Rev Genet. 1974;8:347-91 PMID: 4613261
  41. Recombination of nonchromosomal mutations: a 3-point cross in the green alga Chlamydomonas reinhardi.
    Science. 1968 Nov 8;162(3854):683-4 PMID: 5693897
  42. The intracellular site of synthesis of mitochndrial ribosomal proteins in Neurospora crassa.
    J Cell Biol. 1972 Jul;54(1):56-74 PMID: 4261038
  43. The attachment site of streptomycin to the 30S ribosomal subunit.
    Proc Natl Acad Sci U S A. 1972 Aug;69(8):2141-4 PMID: 4559597
  44. Segregation and recombination of non-Mendellan genes in Chlamydomonas.
    Genetics. 1974 Sep;78(1):439-57 PMID: 4442714
  45. Characterization of the chloroplastic and cytoplasmic ribosomes of Chlamydomonas reinhardi.
    J Mol Biol. 1969 Apr 14;41(1):121-38 PMID: 5803285
  46. Genetic transcription and translation specifying chloroplast components in Chlamydomonas reinhardi.
    Biochemistry. 1971 Feb 16;10(4):692-701 PMID: 5544660
  47. Nondroplet ultrastructural demonstration of cytochrome oxidase activity with a polymerizing osmiophilic reagent, diaminobenzidine (DAB).
    J Cell Biol. 1968 Jul;38(1):1-14 PMID: 4300067
  48. Can a non-Mendelian mutation affect both chloroplast and mithchondrial ribosomes?
    Proc Natl Acad Sci U S A. 1973 Dec;70(12):3463-7 PMID: 4271684
  49. Identification and functional characterization of the protein controlled by the streptomycin-resistant locus in E. coli.
    Nature. 1969 Apr 26;222(5191):333-9 PMID: 4181187
  50. A one-step method for the isolation and determination of leaf ribulose-1,5-diphosphate carboxylase.
    Anal Biochem. 1971 May;41(1):57-66 PMID: 5578554
  51. STREPTOMYCIN, SUPPRESSION, AND THE CODE.
    Proc Natl Acad Sci U S A. 1964 May;51:883-90 PMID: 14173007
  52. 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):42-9 PMID: 5017708
  53. Chloroplast ribosome biogenesis in Chlamydomonas. Selection and characterization of mutants blocked in ribosome formation.
    J Cell Biol. 1974 Oct;63(1):160-79 PMID: 4423964
  54. An altered chloroplast ribosomal protein in ery-M1 mutants of Chlamydomonas reinhardi.
    Mol Gen Genet. 1974;132(2):119-29 PMID: 4421915
  55. Concerning the sites of synthesis of proteins of chloroplast ribosomes and of fraction I protein (ribulose-1,5-diphosphate carboxylase).
    Biochem Biophys Res Commun. 1971 Aug 6;44(3):539-45 PMID: 4256445
  56. Induction of chromosomal and nonchromosomal mutations in Chlamydomonas reinhardi with N-methyl-N'-nitro-N-nitrosoguanidine.
    Genetics. 1965 Sep;52(3):529-37 PMID: 5863904
  57. Ribosomal proteins. 33. Location of amino-acid replacements in protein S12 isolated from Escherichia coli mutants resistant to streptomycin.
    J Mol Biol. 1972 Jul 28;68(3):547-50 PMID: 4560854
  58. Localization of five antibiotic resistances at the subunit level in chloroplast ribosomes of Chlamydomonas.
    Proc Natl Acad Sci U S A. 1974 May;71(5):1715-9 PMID: 4275942
  59. [On the different genetic constitution of the chloroplast and mitochondria in antibiotic dependent mutants of Chlamydomonas reinhardii (author's transl)].
    Protoplasma. 1974;82(1):91-101 PMID: 4410265
  60. Altered chlorplast ribosomal proteins associated with erythromycin-resistant mutants in two genetic systems of Chlamydomonas reinhardi.
    Proc Natl Acad Sci U S A. 1972 Dec;69(12):3779-83 PMID: 4509340
  61. The effects of erythromycin and chloramphenicol on the ultrastructure of mitochondria in sensitive and resistant strains of Paramecium.
    J Cell Biol. 1972 Jul;54(1):8-19 PMID: 5038875
  62. Identification of a chloroplast ribosomal protein altered by a chloroplast mutation in Chlamydomonas.
    J Biol Chem. 1975 May 25;250(10):3655-9 PMID: 1126932
  63. Dissociation of mammalian polyribosomes into subunits by puromycin.
    Proc Natl Acad Sci U S A. 1971 Feb;68(2):390-4 PMID: 5277091
  64. Cyanide-resistant respiration in Neurospora crassa.
    J Bacteriol. 1971 Dec;108(3):1087-96 PMID: 4333318
  65. Mutation of a cytoplasmic gene in Chlamydomonas alters chlorplast ribosome function.
    Proc Natl Acad Sci U S A. 1972 Dec;69(12):3551-5 PMID: 4509313
  66. Mendelian and uniparental alterations in erythromycin binding by plastid ribosomes.
    Science. 1971 Nov 12;174(4010):707-9 PMID: 5123420
  67. Studies on the origin of streptomycin resistant mutants in Chlamydomonas reinhardi.
    Genetics. 1962 Nov;47:1463-74 PMID: 13947923
  68. Chloroplast ribosome deficient mutants in the green alga Chlamydomonas reinhardi and the question of chloroplast ribosome function.
    J Cell Sci. 1972 Mar;10(2):267-305 PMID: 5018026
  69. Terminal Respiration of Vegetative Cells and Zygospores in Chlamydomonas reinhardi.
    Plant Physiol. 1965 Nov;40(6):1220-7 PMID: 16656207
  70. Inhibition of the assembly of cytochrome oxidase in Neurospora crassa by chloramphenicol.
    Eur J Biochem. 1972 Nov 7;30(3):413-7 PMID: 4344826
Article Info
Journal
Molecular & general genetics : MGG
Abbr.
Mol Gen Genet
ISSN
0026-8925
DOI
10.1007/BF00334266
Published
1975-10-03
Pages
183-220
Language
English
Region
Germany
NLM ID
0125036
Subset
IM
External Links
PubMed source DOI: 10.1007/BF00334266
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: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2