Birth-and-death evolution with strong purifying selection in the histone H1 multigene family and the origin of orphon H1 genes.

Histones are small basic nuclear proteins with critical structural and functional roles in eukaryotic genomes. The H1 multigene family constitutes a very interesting histone class gathering the greatest number of isoforms, with many different arrangements in the genome, including clustered and solitary genes, and showing replication-dependent (RD) or replication-independent (RI) expression patterns. The evolution of H1 histones has been classically explained by concerted evolution through a rapid process of interlocus recombination or gene conversion. Given such intriguing features, we have analyzed the long-term evolutionary pattern of the H1 multigene family through the evaluation of the relative importance of gene conversion, point mutation, and selection in generating and maintaining the different H1 subtypes. We have found the presence of an extensive silent nucleotide divergence, both within and between species, which is always significantly greater than the nonsilent variation, indicating that purifying selection is the major factor maintaining H1 protein homogeneity. The results obtained from phylogenetic analysis reveal that different H1 subtypes are no more closely related within than between species, as they cluster by type in the topologies, and that both RD and RI H1 variants follow the same evolutionary pattern. These findings suggest that H1 histones have not been subject to any significant effect of interlocus recombination or concerted evolution. However, the diversification of the H1 isoforms seems to be enhanced primarily by mutation and selection, where genes are subject to birth-and-death evolution with strong purifying selection at the protein level. This model is able to explain not only the generation and diversification of RD H1 isoforms but also the origin and long-term persistence of orphon RI H1 subtypes in the genome, something that is still unclear, assuming concerted evolution.

[1]  M. Nei,et al.  Evolution of immunoglobulin kappa chain variable region genes in vertebrates. , 1998, Molecular biology and evolution.

[2]  R. D'Andrea,et al.  Chromosomal organization of chicken histone genes: preferred associations and inverted duplications , 1985, Molecular and cellular biology.

[3]  Mark A McPeek,et al.  Estimating metazoan divergence times with a molecular clock. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[4]  V. Chapman,et al.  An interspecific linkage map of mouse chromosome 15 positioned with respect to the centromere. , 1992, Genomics.

[5]  M. Nei,et al.  A Simple Method for Estimating and Testing Minimum-Evolution Trees , 1992 .

[6]  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.

[7]  Gynheung An,et al.  Type I MADS-box genes have experienced faster birth-and-death evolution than type II MADS-box genes in angiosperms , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[8]  E. Kardalinou,et al.  Structure and expression of the human gene encoding testicular H1 histone (H1t). , 1991, Gene.

[9]  A. Poustka,et al.  Human histone gene organization: nonregular arrangement within a large cluster. , 1997, Genomics.

[10]  J. Vidal-Taboada,et al.  Evolution of the vertebrate H1 histone class: evidence for the functional differentiation of the subtypes. , 1998, Molecular biology and evolution.

[11]  J. Méndez,et al.  Molecular and Evolutionary Analysis of Mussel Histone Genes (Mytilus spp.): Possible Evidence of an "Orphon Origin" for H1 Histone Genes , 2002, Journal of Molecular Evolution.

[12]  R F Doolittle,et al.  Determining divergence times with a protein clock: update and reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

[14]  H. Robertson.  The large srh family of chemoreceptor genes in Caenorhabditis nematodes reveals processes of genome evolution involving large duplications and deletions and intron gains and losses. , 2000, Genome research.

[15]  Vladimir Brusic,et al.  Molecular Evolution and Phylogeny of Elapid Snake Venom Three-Finger Toxins , 2003, Journal of Molecular Evolution.

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

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

[18]  E. Schmidt,et al.  Divergent evolution of an "orphon" histone gene cluster in Chironomus. , 1993, Journal of molecular biology.

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

[20]  M. Birnstiel,et al.  The organization and expression of histone gene families , 1981, Cell.

[21]  A. Wolffe,et al.  Developmentally regulated expression of linker-histone variants in vertebrates. , 1994, European journal of biochemistry.

[22]  W. Albig,et al.  Characterization of the H1.5 gene completes the set of human H1 subtype genes. , 1997, Gene.

[23]  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.

[24]  M. Chiusano,et al.  Organization and Nucleotide Sequence of the Cluster of Five Histone Genes in the Polichaete Worm Chaetopterus variopedatus: First Record of a H1 Histone Gene in the Phylum Annelida , 1998, Journal of Molecular Evolution.

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

[26]  Masatoshi Nei,et al.  Molecular evolution of the nontandemly repeated genes of the histone 3 multigene family. , 2002, Molecular biology and evolution.

[27]  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.

[28]  G Philipps,et al.  Histones and histone genes in higher plants: structure and genomic organization. , 1993, Biochimie.

[29]  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.

[30]  H. Woodland,et al.  Nucleotide sequences of H1 histone genes from Xenopus laevis. A recently diverged pair of H1 genes and an unusual H1 pseudogene. , 1983, Nucleic acids research.

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

[32]  K. Ohsumi,et al.  Occurrence of H1 subtypes specific to pronuclei and cleavage-stage cell nuclei of anuran amphibians. , 1991, Developmental biology.

[33]  S. Khochbin,et al.  The Evolution of the Differentiation-Specific Histone H1 Gene Basal Promoter , 1997, Journal of Molecular Evolution.

[34]  M. Nei,et al.  Evolutionary dynamics of the T-cell receptor VB gene family as inferred from the human and mouse genomic sequences. , 2001, Molecular biology and evolution.

[35]  J. Dacks,et al.  Origin of H1 linker histones , 2001, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

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

[37]  Masatoshi Nei,et al.  Purifying selection and birth-and-death evolution in the histone H4 gene family. , 2002, Molecular biology and evolution.

[38]  E. Lozovskaya,et al.  Drosophila virilis has atypical kinds and arrangements of histone repeats , 1998, Chromosoma.

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

[40]  E. Schulze,et al.  The Vertebrate Linker Histones H10, H5, and H1M Are Descendants of Invertebrate ``Orphon'' Histone H1 Genes , 1995, Journal of Molecular Evolution.

[41]  R. Angerer,et al.  A histone H1 protein in sea urchins is encoded by a poly(A)+ mRNA. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

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

[43]  A Rzhetsky,et al.  Interior-branch and bootstrap tests of phylogenetic trees. , 1995, Molecular biology and evolution.

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

[45]  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.

[46]  E. Adashi,et al.  A mammalian oocyte-specific linker histone gene H1oo: homology with the genes for the oocyte-specific cleavage stage histone (cs-H1) of sea urchin and the B4/H1M histone of the frog. , 2001, Development.

[47]  T. Sitnikova,et al.  Bootstrap method of interior-branch test for phylogenetic trees. , 1996, Molecular biology and evolution.

[48]  A. Wolffe,et al.  Chromatin transitions during early Xenopus embryogenesis: changes in histone H4 acetylation and in linker histone type. , 1993, Developmental biology.

[49]  David Landsman,et al.  The Histone Database , 2002, Nucleic Acids Res..

[50]  Masatoshi Nei,et al.  Concerted and nonconcerted evolution of the Hsp70 gene superfamily in two sibling species of nematodes. , 2004, Molecular biology and evolution.

[51]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

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

[53]  A. Skoultchi,et al.  The mouse histone H1 genes: gene organization and differential regulation. , 1997, Journal of molecular biology.

[54]  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.

[55]  M. Nei,et al.  Locus specificity of polymorphic alleles and evolution by a birth-and-death process in mammalian MHC genes. , 1999, Molecular biology and evolution.

[56]  L. Sánchez,et al.  Molecular Evolutionary Characterization of the Mussel Mytilus Histone Multigene Family: First Record of a Tandemly Repeated Unit of Five Histone Genes Containing an H1 Subtype with “Orphon” Features , 2004, Journal of Molecular Evolution.

[57]  T. A. Hall,et al.  BIOEDIT: A USER-FRIENDLY BIOLOGICAL SEQUENCE ALIGNMENT EDITOR AND ANALYSIS PROGRAM FOR WINDOWS 95/98/ NT , 1999 .