Nucleotide sequence analysis of the lemur beta-globin gene family: evidence for major rate fluctuations in globin polypeptide evolution.

Lemur beta-related globin genes have been isolated and sequenced. Orthology of prosimian and human epsilon-, gamma-, and beta-related globin genes was established by dot-matrix analysis. All of these lemur globin genes potentially encode functional beta-related globin polypeptides, though precisely when the gamma-globin gene is expressed remains unknown. The organization of the 18-kb brown lemur beta-globin gene cluster (5' epsilon-gamma-[psi eta-delta]-beta 3') is consistent with its evolution by contraction via unequal crossing-over from the putative ancestral mammalian beta-globin gene cluster (5' epsilon-gamma-eta-delta-beta 3'). The dwarf lemur nonadult globin genes are arranged as in the brown lemur. Similar levels of synonymous (silent) nucleotide substitutions and noncoding DNA sequence differences have accumulated between species in all of these genes, suggesting a uniform rate of noncoding DNA divergence throughout primate beta-globin gene clusters. These differences are comparable with those observed in the nonfunctional psi eta pseudogene and have therefore accumulated at the presumably maximal neutral rate. In contrast, nonsynonymous (replacement) nucleotide substitutions show a significant heterogeneity in distribution for both the same gene in different lineages and different genes in the same lineage. These major fluctuations in replacement but not silent substitution rates cannot be attributed to changes in mutation rate, suggesting that changes in the rate of globin polypeptide evolution in primates is not governed solely by variable mutation rates.

[1]  C. Krimbas,et al.  Accuracy of phylogenetic trees estimated from DNA sequence data. , 1987, Molecular biology and evolution.

[2]  H. Bradshaw,et al.  Clustering and subfamily relationships of the Alu family in the human genome. , 1987, Molecular biology and evolution.

[3]  S. Parkhurst,et al.  The Drosophila melanogaster gypsy transposable element encodes putative gene products homologous to retroviral proteins. , 1986, Molecular and cellular biology.

[4]  P. Powers,et al.  Gene conversions and their relation to homologous chromosome pairing. , 1986, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[5]  J. Schimenti,et al.  Structure and organization of the bovine beta-globin genes. , 1985, Molecular biology and evolution.

[6]  R. Spritz,et al.  Nucleotide sequence, evolution, and expression of the fetal globin gene of the spider monkey Ateles geoffroyi. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[7]  J. Miller.  Telling a Quagga by Its Stripes , 1985 .

[8]  W. Brown,et al.  Length variation and heteroplasmy are frequent in mitochondrial DNA from parthenogenetic and bisexual lizards (genus Cnemidophorus). , 1985, Genetics.

[9]  B. Gill,et al.  Use of biotin-labeled probes to map specific DNA sequences on wheat chromosomes , 1985 .

[10]  W. Li,et al.  Evidence for higher rates of nucleotide substitution in rodents than in man. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[11]  T Darden,et al.  Evolution and extinction of transposable elements in Mendelian populations. , 1985, Genetics.

[12]  W. Ewens.  The neutral theory of molecular evolution , 1985 .

[13]  Jeffrey H. Schwartz,et al.  Evolutionary relationships of living lemurs and lorises (Mammalia, Primates) and their potential affinities with European Eocene Adapidae. Anthropological papers of the AMNH ; v. 60, pt. 1 , 1985 .

[14]  S. Karlsson,et al.  Developmental regulation of human globin genes. , 1985, Annual review of biochemistry.

[15]  M. Weiss,et al.  The η-globin gene: Its long evolutionary history in the β-globin gene family of mammals , 1984 .

[16]  A. Jeffreys,et al.  The primate ψβ1 gene: An ancient β-globin pseudogene , 1984 .

[17]  R. Jorgensen,et al.  Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[18]  A. Wilson,et al.  DNA sequences from the quagga, an extinct member of the horse family , 1984, Nature.

[19]  L. Ehrman,et al.  Sequences homologous to P elements occur in Drosophila paulistorum. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[20]  A. Ghent.  Examination of Five Tau Variants Suited to Ordered Contingency Tables, from the Viewpoint of Biological Research , 1984 .

[21]  R. Flavell,et al.  Molecular coevolution: DNA divergence and the maintenance of function , 1984, Cell.

[22]  G. Rubin,et al.  Effects of transposable element insertions on RNA encoded by the white gene of Drosophila , 1984, Cell.

[23]  R. Reeder.  Enhancers and ribosomal gene spacers , 1984, Cell.

[24]  P. Heath,et al.  The sequence of the gorilla fetal globin genes: evidence for multiple gene conversions in human evolution. , 1984, Molecular biology and evolution.

[25]  A. Flavell.  Role of reverse transcription in the generation of extrachromosomal copia mobile genetic elements , 1984, Nature.

[26]  R. Paro,et al.  The molecular basis of I-R hybrid Dysgenesis in drosophila melanogaster: Identification, cloning, and properties of the I factor , 1984, Cell.

[27]  R. Reeder,et al.  The mechanism of nucleolar dominance in xenopus hybrids , 1984, Cell.

[28]  M. van der Ploeg,et al.  2-Acetylaminofluorene-modified probes for the indirect hybridocytochemical detection of specific nucleic acid sequences. , 1984, Experimental cell research.

[29]  R. Hardison,et al.  Rabbit globin pseudogene psi beta 2 is a hybrid of delta- and beta-globin gene sequences. , 1984, Molecular biology and evolution.

[30]  L. Gottlieb,et al.  Phosphoglucose Isomerase Expression in Species of Clarkia with and without a Duplication of the Coding Gene. , 1984, Genetics.

[31]  C. W. Hinton.  Morphogenetically Specific Mutability in DROSOPHILA ANANASSAE. , 1984, Genetics.

[32]  C. Hutchison,et al.  Evolution of the mammalian β-globin gene cluster , 1984 .

[33]  C. Hutchison,et al.  Two mouse early embryonic beta-globin gene sequences. Evolution of the nonadult beta-globins. , 1984, The Journal of biological chemistry.

[34]  J. Lingrel,et al.  Duplication of a four-gene set during the evolution of the goat beta-globin locus produced genes now expressed differentially in development. , 1984, The Journal of biological chemistry.

[35]  C. Thomas White,et al.  The diagonal-traverse homology search algorithm for locating similarities between two sequences , 1984, Nucleic Acids Res..

[36]  D. Buth.  The Application of Electrophoretic Data in Systematic Studies , 1984 .

[37]  C. Hutchison,et al.  Two Mouse Early Embryonic &Globin Gene Sequences , 1984 .

[38]  R. Hardison,et al.  Rabbit Globin Pseudogene e/32 Is a Hybrid of 6- and @Globin Gene Sequence9 , 1984 .

[39]  M. Seashore.  Human Genetics. Part A: The Unfolding Genome , 1984, The Yale Journal of Biology and Medicine.

[40]  G. A. Watterson,et al.  On the time for gene silencing at duplicate Loci. , 1983, Genetics.

[41]  A. Wilson,et al.  Mitochondrial DNA evolution in mice. , 1983, Genetics.

[42]  T. Gilliland,et al.  Allozymes of phosphoglucoisomerase (PGI) in cultivars of barley (Hordeum vulgare L.) , 1983, The Journal of Agricultural Science.

[43]  E. Schon,et al.  Sequence and linkage of the goat εI and εII β-globin genes* , 1983 .

[44]  J. McDonald,et al.  Genetic Localization and Biochemical Characterization of a TRANS-Acting Regulatory Effect in Drosophila. , 1983, Genetics.

[45]  I. Dawid,et al.  A family of oligo-adenylate-terminated transposable sequences in Drosophila melanogaster. , 1983, Journal of molecular biology.

[46]  R. Hardison.  The nucleotide sequence of the rabbit embryonic globin gene beta 4. , 1983, The Journal of biological chemistry.

[47]  G. Hong,et al.  Buffer gradient gels and 35S label as an aid to rapid DNA sequence determination. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Y. Takagi,et al.  A frameshift addition causes silencing of the δ-gtobin gene in an old world monkey, an anubis(Papio doguera) , 1983 .

[49]  T. Jones.  Instability during storage of phosphogluco-isomerase isoenzymes from ryegrasses (Lolium spp.) , 1983 .

[50]  T. Miyata,et al.  Unusual evolutionary conservation and frequent DNA segment exchange in class I genes of the major histocompatibility complex. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[51]  T. Moss.  A transcriptional function for the repetitive ribosomal spacer in Xenopus laevis , 1983, Nature.

[52]  A. Wilson,et al.  Rise and fall of the delta globin gene. , 1983, Journal of molecular biology.

[53]  J. Reiser,et al.  Three regions upstream from the cap site are required for efficient and accurate transcription of the rabbit β-globin gene in mouse 3T6 cells , 1983, Cell.

[54]  A. R. Templeton,et al.  PHYLOGENETIC INFERENCE FROM RESTRICTION ENDONUCLEASE CLEAVAGE SITE MAPS WITH PARTICULAR REFERENCE TO THE EVOLUTION OF HUMANS AND THE APES , 1983, Evolution; international journal of organic evolution.

[55]  J. Modolell,et al.  Drosophila melanogaster mutations suppressible by the suppressor of Hairy-wing are insertions of a 7.3-kilobase mobile element. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[56]  J. D. Dixon,et al.  Prosimian hemoglobins I. The primary structure of the beta-globin chain of Lemur catta. , 1983, Hemoglobin.

[57]  W. Engels.  The P family of transposable elements in Drosophila. , 1983, Annual review of genetics.

[58]  M. Gale,et al.  Genetic control of glucose phosphate isomerase in wheat and related species , 1982, Heredity.

[59]  C. Langley,et al.  Restriction map variation in the Adh region of Drosophila. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[60]  M. W. Young,et al.  Differing levels of dispersed repetitive DNA among closely related species of Drosophila. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[61]  G. Rubin,et al.  The molecular basis of P-M hybrid dysgenesis: The nature of induced mutations , 1982, Cell.

[62]  G. Rubin,et al.  The molecular basis of P-M hybrid dysgenesis: The role of the P element, a P-strain-specific transposon family , 1982, Cell.

[63]  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.

[64]  L. Gottlieb.  Conservation and Duplication of Isozymes in Plants , 1982, Science.

[65]  A. Jeffreys,et al.  Isolation and sequence analysis of a hybrid δ-globin pseudogene from the brown lemur , 1982 .

[66]  R. Flavell,et al.  The DNA sequence of the 5' flanking region of the human beta-globin gene: evolutionary conservation and polymorphic differences. , 1982, Nucleic acids research.

[67]  A. Jeffreys,et al.  Processes of gene duplication , 1982, Nature.

[68]  E. Schon,et al.  Structure and evolution of goat γ-, β C- and β A-globin genes: Three developmentally regulated genes contain inserted elements , 1981, Cell.

[69]  W. Brown,et al.  Extensive polymorphism in the mitochondrial DNA of apes. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[70]  J. Slightom,et al.  A history of the human fetal globin gene duplication , 1981, Cell.

[71]  N. Weeden,et al.  CORRELATION BETWEEN SUBCELLULAR LOCATION AND PHOSPHOGLUCOSE ISOMERASE VARIABILITY , 1981, Evolution; international journal of organic evolution.

[72]  T. Miyata,et al.  Extraordinarily high evolutionary rate of pseudogenes: evidence for the presence of selective pressure against changes between synonymous codons. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[73]  M. Nei,et al.  Pseudogenes as a paradigm of neutral evolution , 1981, Nature.

[74]  A. Jeffreys,et al.  Evolution of the β-globin gene cluster in man and the primates , 1981 .

[75]  E. Coen,et al.  Springcleaning ribosomal DNA: a model for multigene evolution? , 1981, Nature.

[76]  W. Brown,et al.  Evolutionary tree for apes and humans based on cleavage maps of mitochondrial DNA. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[77]  C. Groves,et al.  Studies on the taxonomy and phylogeny of the genus Equus. 1. Subgeneric classification of the recent species , 1981 .

[78]  G. Brown,et al.  Intra- and interspecific variation of the mitochondrial genome in Rattus norvegicus and Rattus rattus: restriction enzyme analysis of variant mitochondrial DNA molecules and their evolutionary relationships. , 1981, Genetics.

[79]  P. A. Biro,et al.  Structural features of the DNA flanking the human non-alpha globin genes: implications in the control of fetal hemoglobin switching. , 1981, Transactions of the Association of American Physicians.

[80]  M. Goodman,et al.  Decoding the pattern of protein evolution. , 1981, Progress in biophysics and molecular biology.

[81]  H. Cann,et al.  Maternal inheritance of human mitochondrial DNA. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[82]  A. Jeffreys,et al.  The 5' flanking region of human epsilon-globin gene. , 1980, Nucleic acids research.

[83]  Ann E. Blechl,et al.  Human fetal g γ- and A γ-globin genes: Complete nucleotide sequences suggest that DNA can be exchanged between these duplicated genes , 1980, Cell.

[84]  Tom Maniatis,et al.  The structure and evolution of the human β-globin gene family , 1980, Cell.

[85]  C. Shoulders,et al.  The primary structure of the human ϵ-globin gene , 1980, Cell.

[86]  G. Rubin,et al.  Terminal repeats of the drosophila transposable element copia: Nucleotide sequence and genomic organization , 1980, Cell.

[87]  N. Opdyke,et al.  Pliocene dispersal of the horse Equus and late Cenozoic mammalian dispersal events , 1980, Nature.

[88]  Debra K. Bennett,et al.  STRIPES DO NOT A ZEBRA MAKE, PART I: A CLADISTIC ANALYSIS OF EQUUS , 1980 .

[89]  R. Staden.  A new computer method for the storage and manipulation of DNA gel reading data. , 1980, Nucleic acids research.

[90]  W. J. Brammar,et al.  A bacteriophage lambda vector for cloning large DNA fragments made with several restriction enzymes. , 1980, Gene.

[91]  T. Bonner,et al.  Evolution of DNA sequences has been retarded in Malagasy primates , 1980, Nature.

[92]  S. Tanksley.  PGI-1, A SINGLE GENE IN TOMATO RESPONSIBLE FOR A VARIABLE NUMBER OF ISOZYMES , 1980 .

[93]  W. Brown.  Polymorphism in mitochondrial DNA of humans as revealed by restriction endonuclease analysis. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[94]  F. Crick,et al.  Selfish DNA: the ultimate parasite , 1980, Nature.

[95]  J. Szostak,et al.  Unequal crossing over in the ribosomal DNA of Saccharomyces cerevisiae , 1980, Nature.

[96]  T. Maniatis,et al.  Molecular cloning and characterization of the human β-like globin gene cluster , 1980, Cell.

[97]  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.

[98]  A. Harris,et al.  Late Pleistocene Horses of Dry Cave, Eddy County, New Mexico , 1980 .

[99]  H. Bunn.  Regulation of Hemoglobin Function in Mammals , 1980 .

[100]  D. Sherratt,et al.  Trans-complementable copy-number mutants of plasmid ColE1 , 1980, Nature.

[101]  V. Eisenmann.  Les chevaux (Equus sensu lato) fossiles et actuels : crânes et dents jugales supérieures , 1980 .

[102]  T. Maniatis,et al.  The molecular genetics of human hemoglobins. , 1980, Annual review of genetics.

[103]  N. Rosenthal,et al.  The structure and transcription of four linked rabbit β-like globin genes , 1979, Cell.

[104]  J. Maizel,et al.  The evolution and sequence comparison of two recently diverged mouse chromosomal β-globin genes , 1979, Cell.

[105]  M. Nei,et al.  Mathematical model for studying genetic variation in terms of restriction endonucleases. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[106]  A. Jeffreys.  DNA sequence variants in the G γ-, A γ-, δ- and β-globin genes of man , 1979, Cell.

[107]  J. L. King,et al.  Fixation of a deleterious allele at one of two "duplicate" loci by mutation pressure and random drift. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[108]  W. Brown,et al.  Rapid evolution of animal mitochondrial DNA. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[109]  M. Goodman,et al.  Amino acid sequences of the alpha and beta chains of adult hemoglobin of the brown lemur, Lemur fulvus fulvus. , 1979, Journal of biochemistry.

[110]  L. A. Goodman,et al.  Measures of association for cross classifications , 1979 .

[111]  O. Ryder,et al.  Hemoglobin polymorphism in Equus przewalskii and E. caballus analyzed by isoelectric focusing. , 1979, Comparative biochemistry and physiology. B, Comparative biochemistry.

[112]  M. Kaminski.  The biochemical evolution of the horse. , 1979, Comparative biochemistry and physiology. B, Comparative biochemistry.

[113]  Bart Barrell,et al.  The nucleotide sequence of bacteriophage φX174 , 1978 .

[114]  M. Goodman,et al.  Amino acid sequences of the alpha and beta chains of adult hemoglobin of the slender loris, Loris tardigradus. , 1978, Journal of biochemistry.

[115]  M. Nei,et al.  Estimation of average heterozygosity and genetic distance from a small number of individuals. , 1978, Genetics.

[116]  G. Rubin,et al.  Repeated gene families in Drosophila melanogaster. , 1978, Cold Spring Harbor symposia on quantitative biology.

[117]  K. Benirschke,et al.  Chromosome banding studies of the Equidae. , 1978, Cytogenetics and cell genetics.

[118]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[119]  A. Wilson,et al.  Rapid speciation and chromosomal evolution in mammals. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[120]  L. Gottlieb.  Evidence for duplication and divergence of the structural gene for phosphoglucoisomerase in diploid species of clarkia. , 1977, Genetics.

[121]  R. Watson,et al.  Mapping of closed circular DNAs by cleavage with restriction endonucleases and calibration by agarose gel electrophoresis. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[122]  G. S. Whitt,et al.  Loss of duplicate gene expression after polyploidisation , 1977, Nature.

[123]  Hamilton O. Smith,et al.  A simple method for DNA restriction site mapping. , 1976, Nucleic acids research.

[124]  T. Maniatis,et al.  Amplification and characterization of a β-globin gene synthesized in vitro , 1976, Cell.

[125]  G. P. Smith,et al.  Evolution of repeated DNA sequences by unequal crossover. , 1976, Science.

[126]  C. Schnarrenberger,et al.  Development and intracellular distribution of enzymes of the oxidative pentose phosphate cycle in radish cotyledons. , 1975, Plant physiology.

[127]  E. Southern.  Detection of specific sequences among DNA fragments separated by gel electrophoresis. , 1975, Journal of molecular biology.

[128]  M. King,et al.  Evolution at two levels in humans and chimpanzees. , 1975, Science.

[129]  R. W. Davis,et al.  Studies on the cleavage of bacteriophage lambda DNA with EcoRI Restriction endonuclease. , 1975, Journal of molecular biology.

[130]  L. H. Throckmorton.  The Phylogeny, Ecology, and Geography of Drosophila , 1975 .

[131]  T. Dobzhansky.  Genetic analysis of hybrid sterility within the species Drosophila pseudoobscura. , 2009, Hereditas.

[132]  J. Clegg.  HORSE HEMOGLOBIN POLYMORPHISM , 1974, Annals of the New York Academy of Sciences.

[133]  C. Hutchison,et al.  Maternal inheritance of mammalian mitochondrial DNA , 1974, Nature.

[134]  C. Schnarrenberger,et al.  Two isoenzymes of glucosephosphate isomerase from spinach leaves and their intracellular compartmentation. , 1974, European journal of biochemistry.

[135]  C. Groves.  Horses, asses and zebras in the wild , 1974 .

[136]  R. Britten,et al.  Reduction in the rate of DNA reassociation by sequence divergence. , 1973, Journal of molecular biology.

[137]  I. Dawid.  Evolution of mitochondrial DNA sequences in Xenopus. , 1972, Developmental biology.

[138]  I. Dawid,et al.  Maternal and cytoplasmic inheritance of mitochondrial DNA in Xenopus. , 1972, Developmental biology.

[139]  J. Farris.  Estimating Phylogenetic Trees from Distance Matrices , 1972, The American Naturalist.

[140]  S. Prakash,et al.  Origin of reproductive isolation in the absence of apparent genic differentiation in a geographic isolate of Drosophila pseudoobscura. , 1972, Genetics.

[141]  R. D. Martín,et al.  Adaptive radiation and behaviour of the Malagasy lemurs. , 1972, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[142]  G. Nelson.  Cephalic sensory canals, pitlines, and the classification of esocoid fishes, with notes on galaxiids and other teleosts. American Museum novitates ; no. 2492 , 1972 .

[143]  J. B. Spofford.  A heterotic model for the evolution of duplications. , 1972, Brookhaven symposia in biology.

[144]  J. Buettner‐Janusch,et al.  Properties of the hemoglobins of newborn and adult prosimians (Prosimii: Lemuriformes and Lorisiformes). , 1972, Folia primatologica; international journal of primatology.

[145]  R. Lindner,et al.  DIPLOID-TETRAPLOID SYMPATRY IN DACTYLIS(GRAMINEAE) , 1971 .

[146]  S. Boyer,et al.  Hemoglobins A and A2 in New World Primates: Comparative Variation and Its Evolutionary Implications , 1969, Science.

[147]  C. W. Easley,et al.  Structural comparison of the hemoglobins of the genus Equus with those of ruminants. , 1969, The Journal of biological chemistry.

[148]  R. K. Koehn.  Esterase Heterogeneity: Dynamics of a Polymorphism , 1969, Science.

[149]  T. Cavender.  An Oligocene mudminnow (family Umbridae) from Oregon with remarks on relationships within the Esocoidei , 1969 .

[150]  C. Groves,et al.  On some taxonomic problems of Asiatic wild assess with the description of a new subspecies lPerissodactylas Equidaer , 1967 .

[151]  A. Dillmann.  Enzyme Nomenclature , 1965, Nature.

[152]  R. Hill,et al.  EVOLUTION OF HEMOGLOBIN. , 1964, Federation proceedings.

[153]  O. J. Dunn.  Multiple Comparisons Using Rank Sums , 1964 .

[154]  N. Davidson,et al.  Cation effects on the denaturation of DNA , 1962 .

[155]  P. Doty,et al.  Determination of the base composition of deoxyribonucleic acid from its thermal denaturation temperature. , 1962, Journal of molecular biology.

[156]  K. Jones,et al.  Hexaploid Dactylis , 1961, Nature.

[157]  M. Chadefaud,et al.  Traité de botanique : systématique , 1960 .

[158]  G. Stebbins,et al.  Morphology, distribution, and interrelationships of the diploid subspecies , 1959 .

[159]  D. Poulson,et al.  Evolution in the Genus Drosophila , 1954, The Yale Journal of Biology and Medicine.

[160]  D. Newman,et al.  THE DISTRIBUTION OF RANGE IN SAMPLES FROM A NORMAL POPULATION, EXPRESSED IN TERMS OF AN INDEPENDENT ESTIMATE OF STANDARD DEVIATION , 1939 .