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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 Mar 28;92(7):2607–2611. doi: 10.1073/pnas.92.7.2607

Fate of a redundant gamma-globin gene in the atelid clade of New World monkeys: implications concerning fetal globin gene expression.

C M Meireles 1, M P Schneider 1, M I Sampaio 1, H Schneider 1, J L Slightom 1, C H Chiu 1, K Neiswanger 1, D L Gumucio 1, J Czelusniak 1, M Goodman 1
PMCID: PMC42267  PMID: 7535927

Abstract

Conclusive evidence was provided that gamma 1, the upstream of the two linked simian gamma-globin loci (5'-gamma 1-gamma 2-3'), is a pseudogene in a major group of New World monkeys. Sequence analysis of PCR-amplified genomic fragments of predicted sizes revealed that all extant genera of the platyrrhine family Atelidae [Lagothrix (woolly monkeys), Brachyteles (woolly spider monkeys), Ateles (spider monkeys), and Alouatta (howler monkeys)] share a large deletion that removed most of exon 2, all of intron 2 and exon 3, and much of the 3' flanking sequence of gamma 1. The fact that two functional gamma-globin genes were not present in early ancestors of the Atelidae (and that gamma 1 was the dispensible gene) suggests that for much or even all of their evolution, platyrrhines have had gamma 2 as the primary fetally expressed gamma-globin gene, in contrast to catarrhines (e.g., humans and chimpanzees) that have gamma 1 as the primary fetally expressed gamma-globin gene. Results from promoter sequences further suggest that all three platyrrhine families (Atelidae, Cebidae, and Pitheciidae) have gamma 2 rather than gamma 1 as their primary fetally expressed gamma-globin gene. The implications of this suggestion were explored in terms of how gene redundancy, regulatory mutations, and distance of each gamma-globin gene from the locus control region were possibly involved in the acquisition and maintenance of fetal, rather than embryonic, expression.

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Selected References

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  1. Bailey W. J., Hayasaka K., Skinner C. G., Kehoe S., Sieu L. C., Slightom J. L., Goodman M. Reexamination of the African hominoid trichotomy with additional sequences from the primate beta-globin gene cluster. Mol Phylogenet Evol. 1992 Jun;1(2):97–135. doi: 10.1016/1055-7903(92)90024-b. [DOI] [PubMed] [Google Scholar]
  2. Barrie P. A., Jeffreys A. J., Scott A. F. Evolution of the beta-globin gene cluster in man and the primates. J Mol Biol. 1981 Jul 5;149(3):319–336. doi: 10.1016/0022-2836(81)90476-9. [DOI] [PubMed] [Google Scholar]
  3. Bell G. I., Karam J. H., Rutter W. J. Polymorphic DNA region adjacent to the 5' end of the human insulin gene. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5759–5763. doi: 10.1073/pnas.78.9.5759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cabot E. L., Beckenbach A. T. Simultaneous editing of multiple nucleic acid and protein sequences with ESEE. Comput Appl Biosci. 1989 Jul;5(3):233–234. doi: 10.1093/bioinformatics/5.3.233. [DOI] [PubMed] [Google Scholar]
  5. Collins F. S., Weissman S. M. The molecular genetics of human hemoglobin. Prog Nucleic Acid Res Mol Biol. 1984;31:315–462. doi: 10.1016/s0079-6603(08)60382-7. [DOI] [PubMed] [Google Scholar]
  6. Cooper S. J., Hope R. M. Evolution and expression of a beta-like globin gene of the Australian marsupial Sminthopsis crassicaudata. Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11777–11781. doi: 10.1073/pnas.90.24.11777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Engel J. D. Developmental regulation of human beta-globin gene transcription: a switch of loyalties? Trends Genet. 1993 Sep;9(9):304–309. doi: 10.1016/0168-9525(93)90248-g. [DOI] [PubMed] [Google Scholar]
  8. Fitch D. H., Bailey W. J., Tagle D. A., Goodman M., Sieu L., Slightom J. L. Duplication of the gamma-globin gene mediated by L1 long interspersed repetitive elements in an early ancestor of simian primates. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7396–7400. doi: 10.1073/pnas.88.16.7396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Giebel L. B., van Santen V. L., Slightom J. L., Spritz R. A. Nucleotide sequence, evolution, and expression of the fetal globin gene of the spider monkey Ateles geoffroyi. Proc Natl Acad Sci U S A. 1985 Oct;82(20):6985–6989. doi: 10.1073/pnas.82.20.6985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Goodman M., Czelusniak J., Koop B. F., Tagle D. A., Slightom J. L. Globins: a case study in molecular phylogeny. Cold Spring Harb Symp Quant Biol. 1987;52:875–890. doi: 10.1101/sqb.1987.052.01.096. [DOI] [PubMed] [Google Scholar]
  11. Goodman M., Koop B. F., Czelusniak J., Weiss M. L. The eta-globin gene. Its long evolutionary history in the beta-globin gene family of mammals. J Mol Biol. 1984 Dec 25;180(4):803–823. doi: 10.1016/0022-2836(84)90258-4. [DOI] [PubMed] [Google Scholar]
  12. Gumucio D. L., Shelton D. A., Blanchard-McQuate K., Gray T., Tarle S., Heilstedt-Williamson H., Slightom J. L., Collins F., Goodman M. Differential phylogenetic footprinting as a means to identify base changes responsible for recruitment of the anthropoid gamma gene to a fetal expression pattern. J Biol Chem. 1994 May 27;269(21):15371–15380. [PubMed] [Google Scholar]
  13. Hanscombe O., Whyatt D., Fraser P., Yannoutsos N., Greaves D., Dillon N., Grosveld F. Importance of globin gene order for correct developmental expression. Genes Dev. 1991 Aug;5(8):1387–1394. doi: 10.1101/gad.5.8.1387. [DOI] [PubMed] [Google Scholar]
  14. Hardison R. C. Comparison of the beta-like globin gene families of rabbits and humans indicates that the gene cluster 5'-epsilon-gamma-delta-beta-3' predates the mammalian radiation. Mol Biol Evol. 1984 Sep;1(5):390–410. doi: 10.1093/oxfordjournals.molbev.a040326. [DOI] [PubMed] [Google Scholar]
  15. Hardison R. C. The nucleotide sequence of rabbit embryonic globin gene beta 3. J Biol Chem. 1981 Nov 25;256(22):11780–11786. [PubMed] [Google Scholar]
  16. Harris S., Barrie P. A., Weiss M. L., Jeffreys A. J. The primate psi beta 1 gene. An ancient beta-globin pseudogene. J Mol Biol. 1984 Dec 25;180(4):785–801. doi: 10.1016/0022-2836(84)90257-2. [DOI] [PubMed] [Google Scholar]
  17. Hayasaka K., Fitch D. H., Slightom J. L., Goodman M. Fetal recruitment of anthropoid gamma-globin genes. Findings from phylogenetic analyses involving the 5'-flanking sequences of the psi gamma 1 globin gene of spider monkey Ateles geoffroyi. J Mol Biol. 1992 Apr 5;224(3):875–881. doi: 10.1016/0022-2836(92)90568-5. [DOI] [PubMed] [Google Scholar]
  18. Hayasaka K., Skinner C. G., Goodman M., Slightom J. L. The gamma-globin genes and their flanking sequences in primates: findings with nucleotide sequences of capuchin monkey and tarsier. Genomics. 1993 Oct;18(1):20–28. doi: 10.1006/geno.1993.1422. [DOI] [PubMed] [Google Scholar]
  19. Hill A., Hardies S. C., Phillips S. J., Davis M. G., Hutchison C. A., 3rd, Edgell M. H. Two mouse early embryonic beta-globin gene sequences. Evolution of the nonadult beta-globins. J Biol Chem. 1984 Mar 25;259(6):3739–3747. [PubMed] [Google Scholar]
  20. Huisman T. H., Schroeder W. A., Keeling M. E., Gengozian N., Miller A., Brodie A. R., Shelton J. R., Shelton J. B., Apell G. Search for nonallelic structural genes for gamma-chains of fetal hemoglobin in some primates. Biochem Genet. 1973 Nov;10(3):309–318. doi: 10.1007/BF00485708. [DOI] [PubMed] [Google Scholar]
  21. Jurka J., Milosavljevic A. Reconstruction and analysis of human Alu genes. J Mol Evol. 1991 Feb;32(2):105–121. doi: 10.1007/BF02515383. [DOI] [PubMed] [Google Scholar]
  22. Koop B. F., Goodman M. Evolutionary and developmental aspects of two hemoglobin beta-chain genes (epsilon M and beta M) of opossum. Proc Natl Acad Sci U S A. 1988 Jun;85(11):3893–3897. doi: 10.1073/pnas.85.11.3893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Koop B. F., Tagle D. A., Goodman M., Slightom J. L. A molecular view of primate phylogeny and important systematic and evolutionary questions. Mol Biol Evol. 1989 Nov;6(6):580–612. doi: 10.1093/oxfordjournals.molbev.a040574. [DOI] [PubMed] [Google Scholar]
  24. Myers R. M., Tilly K., Maniatis T. Fine structure genetic analysis of a beta-globin promoter. Science. 1986 May 2;232(4750):613–618. doi: 10.1126/science.3457470. [DOI] [PubMed] [Google Scholar]
  25. Rogan P. K., Pan J., Weissman S. M. L1 repeat elements in the human epsilon-G gamma-globin gene intergenic region: sequence analysis and concerted evolution within this family. Mol Biol Evol. 1987 Jul;4(4):327–342. doi: 10.1093/oxfordjournals.molbev.a040448. [DOI] [PubMed] [Google Scholar]
  26. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schneider H., Schneider M. P., Sampaio I., Harada M. L., Stanhope M., Czelusniak J., Goodman M. Molecular phylogeny of the New World monkeys (Platyrrhini, primates). Mol Phylogenet Evol. 1993 Sep;2(3):225–242. doi: 10.1006/mpev.1993.1022. [DOI] [PubMed] [Google Scholar]
  28. Shen S. H., Slightom J. L., Smithies O. A history of the human fetal globin gene duplication. Cell. 1981 Oct;26(2 Pt 2):191–203. doi: 10.1016/0092-8674(81)90302-0. [DOI] [PubMed] [Google Scholar]
  29. Tagle D. A., Koop B. F., Goodman M., Slightom J. L., Hess D. L., Jones R. T. Embryonic epsilon and gamma globin genes of a prosimian primate (Galago crassicaudatus). Nucleotide and amino acid sequences, developmental regulation and phylogenetic footprints. J Mol Biol. 1988 Sep 20;203(2):439–455. doi: 10.1016/0022-2836(88)90011-3. [DOI] [PubMed] [Google Scholar]
  30. Tagle D. A., Stanhope M. J., Siemieniak D. R., Benson P., Goodman M., Slightom J. L. The beta globin gene cluster of the prosimian primate Galago crassicaudatus: nucleotide sequence determination of the 41-kb cluster and comparative sequence analyses. Genomics. 1992 Jul;13(3):741–760. doi: 10.1016/0888-7543(92)90150-q. [DOI] [PubMed] [Google Scholar]

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