Molecular evolution of the nontandemly repeated genes of the histone 3 multigene family.

In some species, histone gene clusters consist of tandem arrays of each type of histone gene, whereas in other species the genes may be clustered but not arranged in tandem. In certain species, however, histone genes are found scattered across several different chromosomes. This study examines the evolution of histone 3 (H3) genes that are not arranged in large clusters of tandem repeats. Although H3 amino acid sequences are highly conserved both within and between species, we found that the nucleotide sequence divergence at synonymous sites is high, indicating that purifying selection is the major force for maintaining H3 amino acid sequence homogeneity over long-term evolution. In cases where synonymous-site divergence was low, recent gene duplication appeared to be a better explanation than gene conversion. These results, and other observations on gene inactivation, organization, and phylogeny, indicated that these H3 genes evolve according to a birth-and-death process under strong purifying selection. Thus, we found little evidence to support previous claims that all H3 proteins, regardless of their genome organization, undergo concerted evolution. Further analyses of the structure of H3 proteins revealed that the histones of higher eukaryotes might have evolved from a replication-independent-like H3 gene.

[1]  M. Chabouté,et al.  Genomic organization and nucleotide sequences of two histone H3 and two histone H4 genes of Arabidopsis thaliana , 1987, Plant Molecular Biology.

[2]  M. Chabouté,et al.  Nucleotide sequences of two corn histone H3 genes. Genomic organization of the corn histone H3 and H4 genes , 1986, Plant Molecular Biology.

[3]  Sudhir Kumar,et al.  MEGA2: molecular evolutionary genetics analysis software , 2001, Bioinform..

[4]  M. Nei,et al.  Purifying selection and birth-and-death evolution in the ubiquitin gene family. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[5]  Jianzhi Zhang,et al.  Evolution of the rodent eosinophil-associated RNase gene family by rapid gene sorting and positive selection. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[6]  P. Preiser,et al.  Malaria multigene families: the price of chronicity. , 2000, Parasitology today.

[7]  J. Pérez-Ortín,et al.  News & Notes: Stochastic Nucleosome Positioning in a Yeast Chromatin Region Is Not Dependent on Histone H1 , 1999, Current Microbiology.

[8]  Andrew Smith Genome sequence of the nematode C-elegans: A platform for investigating biology , 1998 .

[9]  H. Robertson Two large families of chemoreceptor genes in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae reveal extensive gene duplication, diversification, movement, and intron loss. , 1998, Genome research.

[10]  N. M. Brooke,et al.  A molecular timescale for vertebrate evolution , 1998, Nature.

[11]  M. Nei,et al.  Positive Darwinian selection after gene duplication in primate ribonuclease genes. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[12]  R. Debry Comparative Analysis of Evolution in a Rodent Histone H2a Pseudogene , 1998, Journal of Molecular Evolution.

[13]  M. Sogin,et al.  A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[14]  J. Berg Genome sequence of the nematode C. elegans: a platform for investigating biology. , 1998, Science.

[15]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[16]  M. Nei,et al.  Evolution by the birth-and-death process in multigene families of the vertebrate immune system. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[17]  J. Craig Venter,et al.  The first genome from the third domain of life , 1997, Nature.

[18]  H. Bussey,et al.  Histone H1 in Saccharomyces cerevisiae , 1997, Yeast.

[19]  O. Witt,et al.  Histones: genetic diversity and tissue-specific gene expression , 1997, Histochemistry and Cell Biology.

[20]  W. Wheeler,et al.  Molecular evolution and phylogenetic utility of the polyubiquitin locus in mammals and higher vertebrates. , 1996, Molecular phylogenetics and evolution.

[21]  J. M. Requena,et al.  Organization, transcription and regulation of the Leishmania infantum histone H3 genes. , 1996, The Biochemical journal.

[22]  W. Marzluff,et al.  Characterization of the mouse histone gene cluster on chromosome 13: 45 histone genes in three patches spread over 1Mb. , 1996, Genome research.

[23]  W. Marzluff,et al.  Characterization of the 55-kb mouse histone gene cluster on chromosome 3. , 1996, Genome research.

[24]  W. Marzluff,et al.  Structure of a cluster of mouse histone genes. , 1996, Biochimica et biophysica acta.

[25]  G. J. Graham,et al.  Tandem genes and clustered genes. , 1995, Journal of theoretical biology.

[26]  W. Marzluff,et al.  Selection on silent sites in the rodent H3 histone gene family. , 1994, Genetics.

[27]  Paul M. Sharp,et al.  Codon usage in Caenorhabditis elegans: delineation of translational selection and mutational biases , 1994, Nucleic Acids Res..

[28]  M. Nei,et al.  Divergent evolution and evolution by the birth-and-death process in the immunoglobulin VH gene family. , 1994, Molecular biology and evolution.

[29]  T. Thatcher,et al.  Phylogenetic analysis of the core histones H2A, H2B, H3, and H4. , 1994, Nucleic acids research.

[30]  M. Riley,et al.  Ubiquitins revisited: further examples of within- and between-locus concerted evolution. , 1993, Molecular phylogenetics and evolution.

[31]  T. Ohta An examination of the generation-time effect on molecular evolution. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[32]  T. Nakayama,et al.  The chicken histone gene family. , 1993, Comparative biochemistry and physiology. B, Comparative biochemistry.

[33]  Y. Matsuo,et al.  Nucleotide variation and divergence in the histone multigene family in Drosophila melanogaster. , 1989, Genetics.

[34]  Wen-Hsiung Li,et al.  Molecular evolution of ubiquitin genes. , 1987, Trends in ecology & evolution.

[35]  S. W. Emmons,et al.  Molecular characterization of the histone gene family of Caenorhabditis elegans. , 1987, Journal of molecular biology.

[36]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[37]  W. Bonner,et al.  Histones and their modifications. , 1986, CRC critical reviews in biochemistry.

[38]  J. Felsenstein CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[39]  C. Holt,et al.  A new family of tandem repetitive early histone genes in the sea urchin Lytechinus pictus: evidence for concerted evolution within tandem arrays. , 1984, Nucleic acids research.

[40]  G. Stein,et al.  Histone genes: Structure, organization, and regulation , 1984 .

[41]  R A Graves,et al.  Structure of a cluster of mouse histone genes. , 1983, Nucleic acids research.

[42]  T. Ohta On the evolution of multigene families. , 1983, Theoretical population biology.

[43]  R. Graves,et al.  Histone mRNA concentrations are regulated at the level of transcription and mRNA degradation. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[44]  L. Kedes,et al.  Expression and organization of histone genes. , 1983, Annual review of genetics.

[45]  G. Dover,et al.  Molecular drive: a cohesive mode of species evolution , 1982, Nature.

[46]  T. Strachan,et al.  Dynamics of concerted evolution of ribosomal DNA and histone gene families in the melanogaster species subgroup of Drosophila. , 1982, Journal of molecular biology.

[47]  Y. Kan,et al.  Rapid duplication and loss of genes coding for the alpha chains of hemoglobin. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[48]  L. Kedes,et al.  Histone genes and histone messengers. , 1979, Annual review of biochemistry.

[49]  L. Kedes Histone messengers and histone genes , 1976, Cell.

[50]  G. P. Smith,et al.  Unequal crossover and the evolution of multigene families. , 1974, Cold Spring Harbor symposia on quantitative biology.