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PMID: 2515110 Published · ppublish English Comparative Study Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Molecular evolution of the small subunit of ribulose bisphosphate carboxylase: nucleotide substitution and gene conversion.

Genetics ·Vol. 123 ·No. 4 ·1989-12-00 ·Pages 845-63

Meagher RB, Berry-Lowe S, Rice K

Abstract

The nucleotide sequences encoding the mature portion of 31 ribulose 1.5-bisphosphate carboxylase small subunit (SSU) genes from 17 genera of plants, green algae and cyanobacteria were examined. Among the 465 pairwise sequence comparisons, SSU multigene family members within the same species were more similar to each other in nonsynonymous or replacement nucleotide substitutions (RNS) than they were to SSU sequences in any other organism. The concerted evolution of independent SSU gene lineages within closely related plant species suggests that homogenization of RNS positions has occurred at least once in the life of each genus. The rate of expected RNS among mature SSU sequences was calculated to be 1.25 X 10(-9)/site/yr for the first 70 million years (MY) of divergence with a significant slowing to 0.13 X 10(-9)/site/yr for the next 1,400 MY. The data suggest that mature SSU sequences do not accumulate more than 20% differences in the RNS positions without compensatory changes in other components of this enzyme system. During the first 70 MY of divergence between species, the rate of expected synonymous or silent nucleotide substitutions (SNS) is approximately 6.6 X 10(-9)/site/yr. This is five times the RNS rate and is similar to the silent rate observed in animals. In striking contrast, SNS and RNS do not show this correlation among SSU gene family members within a species. A mechanism involving gene conversion within the exons followed by selection for biased gene conversion products with conservation of RNS positions and divergence of SNS positions is discussed. A SSU gene tree based on corrected RNS for 31 SSU sequences is presented and agrees well with a species tree based on morphological and cytogenetic traits for the 17 genera examined. SSU gene comparisons may be useful in predicting phylogenetic relationships and in some cases divergence times of various plant, algal and cyanobacterial species.

MeSH Terms
Amino Acid Sequence Base Sequence Biological Evolution Cyanobacteria/genetics Eukaryota/genetics Gene Conversion Genes, Plant Molecular Sequence Data Mutation Phylogeny Plants/genetics Ribulose-Bisphosphate Carboxylase/genetics
Chemicals
Ribulose-Bisphosphate Carboxylase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Meagher R B
Department of Genetics, University of Georgia, Athens 30602.
Berry-Lowe S
Rice K
References (55)
55 references, click to expand
  1. Expression dynamics of the pea rbcS multigene family and organ distribution of the transcripts.
    EMBO J. 1986 Sep;5(9):2063-2071 PMID: 16453702
  2. Nucleotide sequence of a cDNA encoding rbcS from the desert plant Mesembryanthemum crystallinum.
    Nucleic Acids Res. 1987 Aug 11;15(15):6301 PMID: 3627990
  3. Complete sequence of one of the mRNAs coding for the small subunit of ribulose bisphosphate carboxylase of Nicotiana sylvestris.
    Biochimie. 1984 Jul-Aug;66(7-8):539-45 PMID: 6549380
  4. Genomic organization, sequence analysis and expression of all five genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase from tomato.
    Mol Gen Genet. 1987 Sep;209(2):247-56 PMID: 3478552
  5. Nucleotide sequence and molecular evolution of two tomato genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase.
    Gene. 1986;48(1):23-32 PMID: 3557127
  6. Mitochondrial DNA sequences of primates: tempo and mode of evolution.
    J Mol Evol. 1982;18(4):225-39 PMID: 6284948
  7. Nucleotide sequence of a gene encoding sunflower ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit (rbcs).
    Nucleic Acids Res. 1987 Sep 11;15(17):7181 PMID: 3658679
  8. The evolution of genes: the chicken preproinsulin gene.
    Cell. 1980 Jun;20(2):555-66 PMID: 7388949
  9. Evidence for selection as a mechanism in the concerted evolution of Lycopersicon esculentum (tomato) genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase.
    Proc Natl Acad Sci U S A. 1986 Jun;83(11):3880-4 PMID: 3012537
  10. Nucleotide sequence of cDNA encoding the small subunit of ribulose-1,5-bisphosphate carboxylase from maize.
    J Biochem. 1987 Oct;102(4):673-6 PMID: 3436948
  11. Sequence of a genomic DNA clone for the small subunit of ribulose bis-phosphate carboxylase-oxygenase from tobacco.
    Nucleic Acids Res. 1985 Apr 11;13(7):2373-86 PMID: 4000958
  12. Sequence of a ribulose 1,5-bisphosphate carboxylase/oxygenase cDNA from the C4 dicot Flaveria trinervia.
    Nucleic Acids Res. 1987 Feb 25;15(4):1875 PMID: 3822845
  13. Sequence, evolution and differential expression of the two genes encoding variant small subunits of ribulose bisphosphate carboxylase/oxygenase in Chlamydomonas reinhardtii.
    J Mol Biol. 1986 Oct 5;191(3):421-32 PMID: 3820291
  14. Ubiquitin genes as a paradigm of concerted evolution of tandem repeats.
    J Mol Evol. 1987;25(1):58-64 PMID: 3041010
  15. Recent divergence from a common ancestor of human IFN-alpha genes.
    Nature. 1982 Jan 14;295(5845):165-8 PMID: 6173759
  16. The sequence of the gorilla fetal globin genes: evidence for multiple gene conversions in human evolution.
    Mol Biol Evol. 1984 Sep;1(5):371-89 PMID: 6599972
  17. The nucleotide sequence, expression, and evolution of one member of a multigene family encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in soybean.
    J Mol Appl Genet. 1982;1(6):483-98 PMID: 7153686
  18. Chromosomal translocations generated by high-frequency meiotic recombination between repeated yeast genes.
    Genetics. 1986 Nov;114(3):731-52 PMID: 3539696
  19. Tertiary structure of plant RuBisCO: domains and their contacts.
    Science. 1988 Jul 1;241(4861):71-4 PMID: 3133767
  20. Developmentally regulated genes in silkmoths.
    Annu Rev Genet. 1984;18:443-87 PMID: 6397124
  21. A chloroplast DNA inversion marks an ancient evolutionary split in the sunflower family (Asteraceae).
    Proc Natl Acad Sci U S A. 1987 Aug;84(16):5818-22 PMID: 16593871
  22. Isolation of tobacco SSU genes: characterization of a transcriptionally active pseudogene.
    Nucleic Acids Res. 1987 Nov 11;15(21):8661-77 PMID: 3684569
  23. The diversification of the leguminosae: first fossil evidence of the mimosoideae and papilionoideae.
    Science. 1985 May 31;228(4703):1087-9 PMID: 17737903
  24. Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes.
    Proc Natl Acad Sci U S A. 1980 Dec;77(12):7323-7 PMID: 6261251
  25. Genes encoding actin in higher plants: intron positions are highly conserved but the coding sequences are not.
    J Mol Appl Genet. 1983;2(1):111-26 PMID: 6842118
  26. Codon substitution in evolution and the "saturation" of synonymous changes.
    Genetics. 1983 Dec;105(4):1011-27 PMID: 6642197
  27. Functional determinants in transit sequences: import and partial maturation by vascular plant chloroplasts of the ribulose-1,5-bisphosphate carboxylase small subunit of Chlamydomonas.
    J Cell Biol. 1985 Jan;100(1):226-34 PMID: 3965471
  28. Tandem genetic duplications in phage and bacteria.
    Annu Rev Microbiol. 1977;31:473-505 PMID: 334045
  29. The molecular evolution of actin.
    Genetics. 1986 Sep;114(1):315-32 PMID: 3770469
  30. Endosymbiotic origin and codon bias of the nuclear gene for chloroplast glyceraldehyde-3-phosphate dehydrogenase from maize.
    J Mol Evol. 1987;26(4):320-8 PMID: 3131533
  31. Tissue-specific and light-regulated expression of a pea nuclear gene encoding the small subunit of ribulose-1,5-bisphosphate carboxylase.
    EMBO J. 1984 Aug;3(8):1671-9 PMID: 6479146
  32. Ribulose-1,5-bisphosphate carboxylase-oxygenase.
    Annu Rev Biochem. 1983;52:507-35 PMID: 6351728
  33. A potential donor gene for the bm1 gene conversion event in the C57BL mouse.
    Nature. 1983 Dec 22-1984 Jan 4;306(5945):792-5 PMID: 6656881
  34. Developmental cell interactions in Myxococcus xanthus and the spoC locus.
    Proc Natl Acad Sci U S A. 1983 Mar;80(5):1406-10 PMID: 16593290
  35. Human fetal G gamma- and A gamma-globin genes: complete nucleotide sequences suggest that DNA can be exchanged between these duplicated genes.
    Cell. 1980 Oct;21(3):627-38 PMID: 7438203
  36. The genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase are expressed differentially in petunia leaves.
    Nucleic Acids Res. 1986 Apr 25;14(8):3325-42 PMID: 3010233
  37. Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia.
    Science. 1989 Jan 6;243(4887):75-7 PMID: 2911720
  38. Polypeptide composition of fraction I protein from Nicotiana glauca and from cultivars of Nicotiana tabacum, including a male sterile line.
    Biochem Genet. 1975 Dec;13(11-12):771-8 PMID: 1200977
  39. The glycosylated seed storage proteins of Glycine max and Phaseolus vulgaris. Structural homologies of genes and proteins.
    J Biol Chem. 1986 Jul 15;261(20):9228-38 PMID: 3013879
  40. 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
  41. Chimpanzee fetal G gamma and A gamma globin gene nucleotide sequences provide further evidence of gene conversions in hominine evolution.
    Mol Biol Evol. 1985 Sep;2(5):370-89 PMID: 3870867
  42. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions.
    Mol Biol Evol. 1986 Sep;3(5):418-26 PMID: 3444411
  43. Intrachromosomal gene conversion and the maintenance of sequence homogeneity among repeated genes.
    Genetics. 1982 Feb;100(2):315-37 PMID: 7106560
  44. Expansions and contractions of the genetic map relative to the physical map of yeast chromosome III.
    Mol Cell Biol. 1988 Feb;8(2):595-604 PMID: 2832729
  45. Gene conversion, linkage, and the evolution of multigene families.
    Genetics. 1988 Sep;120(1):291-301 PMID: 3220252
  46. Cotranscription of genes encoding the small and large subunits of ribulose-1,5-bisphosphate carboxylase in the cyanobacterium Anabaena 7120.
    Proc Natl Acad Sci U S A. 1984 Oct;81(19):5961-5 PMID: 6091125
  47. Localization in the Tomato Genome of DNA Restriction Fragments Containing Sequences Homologous to the rRNA (45s), the Major Chlorophyll a/b Binding Polypeptide and the Ribulose Bisphosphate Carboxylase Genes.
    Genetics. 1986 Jan;112(1):93-105 PMID: 17246311
  48. Biochemical evolution.
    Annu Rev Biochem. 1977;46:573-639 PMID: 409339
  49. rbcS genes in Solanum tuberosum: conservation of transit peptide and exon shuffling during evolution.
    Proc Natl Acad Sci U S A. 1988 Feb;85(3):846-50 PMID: 3422467
  50. A number of different nuclear genes for the small subunit of RuBPCase are transcribed in petunia.
    Nucleic Acids Res. 1983 Jun 25;11(12):4177-83 PMID: 6688128
  51. Identification of common molecular subsequences.
    J Mol Biol. 1981 Mar 25;147(1):195-7 PMID: 7265238
  52. Nucleotide sequence of a gene encoding corn ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit (rbcs).
    Nucleic Acids Res. 1987 May 26;15(10):4360 PMID: 3588298
  53. Nucleotide sequence encoding the precursor of the small subunit of ribulose 1,5-bisphosphate carboxylase from Lemna gibba L.G-3.
    Nucleic Acids Res. 1983 Nov 25;11(22):8051-61 PMID: 6316282
  54. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection.
    Nature. 1988 Sep 8;335(6186):167-70 PMID: 3412472
  55. Physical lengths of meiotic and mitotic gene conversion tracts in Saccharomyces cerevisiae.
    Genetics. 1988 Mar;118(3):401-10 PMID: 2835285
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
DOI
10.1093/genetics/123.4.845
Published
1989-12-00
Pages
845-63
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1203894
Subset
IM
External Links
PubMed source DOI: 10.1093/genetics/123.4.845 PMC Full Text View journal details
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