Hemoglobins from bacteria to man: Evolution of different patterns of gene expression

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Abstract

The discovery of hemoglobins in virtually all kingdoms of organisms has shown (1) that the ancestral gene for hemoglobin is ancient, and (2) that hemoglobins can serve additional functions besides transport of oxygen between tissues, ranging from intracellular oxygen transport to catalysis of redox reactions. These different functions of the hemoglobins illustrate the acquisition of new roles by a preexisting structural gene, which requires changes not only in the coding regions but also in the regulatory elements of the genes. The evolution of different regulated functions within an ancient gene family allows an examination of the types of biosequence data that are informative for various types of issues. Alignment of amino acid sequences is informative for the phylogenetic relationships among the hemoglobins in bacteria, fungi, protists, plants and animals. Although many of these diverse hemoglobins are induced by low oxygen concentrations, to date none of the molecular mechanisms for their hypoxic induction shows common regulatory proteins; hence, a search for matches in non-coding DNA sequences would not be expected to be fruitful. Indeed, alignments of non-coding DNA sequences do not reveal significant matches even between mammalian α- and β-globin gene clusters, which diverged approximately 450 million years ago and are still expressed in a coordinated and balanced manner. They are in very different genomic contexts that show pronounced differences in regulatory mechanisms. The α-globin gene is in constitutively active chromatin and is encompassed by a CpG island, which is a dominant determinant of its regulation, whereas the β-globin gene is in A+T-rich genomic DNA. Non-coding sequence matches are not seen between avian and mammalian β-globin gene clusters, which diverged approximately 250 million years ago, despite the fact that regulation of both gene clusters requires tissue-specific activation of a chromatin domain regulated by a locus control region. The cis-regulatory sequences needed for domain opening and enhancement do show common binding sites for transcription factors. In contrast, alignments of non-coding sequences from species representing multiple eutherian mammalian orders, some of which diverged as long as 135 million years ago, are reliable predictors of novel cis-regulatory elements, both proximal and distal to the genes. Examples include a potential target for the hematopoietic transcription factor TAL1.

Original languageEnglish (US)
Pages (from-to)1099-1117
Number of pages19
JournalJournal of Experimental Biology
Volume201
Issue number8
StatePublished - Apr 1 1998

Fingerprint

hemoglobin
gene expression
Hemoglobins
Globins
Bacteria
Gene Expression
bacterium
gene
bacteria
Multigene Family
multigene family
Genes
regulatory sequences
genes
Oxygen
intergenic DNA
oxygen
Chromatin
chromatin
Transcription Factors

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Physiology
  • Aquatic Science
  • Animal Science and Zoology
  • Molecular Biology
  • Insect Science

Cite this

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title = "Hemoglobins from bacteria to man: Evolution of different patterns of gene expression",
abstract = "The discovery of hemoglobins in virtually all kingdoms of organisms has shown (1) that the ancestral gene for hemoglobin is ancient, and (2) that hemoglobins can serve additional functions besides transport of oxygen between tissues, ranging from intracellular oxygen transport to catalysis of redox reactions. These different functions of the hemoglobins illustrate the acquisition of new roles by a preexisting structural gene, which requires changes not only in the coding regions but also in the regulatory elements of the genes. The evolution of different regulated functions within an ancient gene family allows an examination of the types of biosequence data that are informative for various types of issues. Alignment of amino acid sequences is informative for the phylogenetic relationships among the hemoglobins in bacteria, fungi, protists, plants and animals. Although many of these diverse hemoglobins are induced by low oxygen concentrations, to date none of the molecular mechanisms for their hypoxic induction shows common regulatory proteins; hence, a search for matches in non-coding DNA sequences would not be expected to be fruitful. Indeed, alignments of non-coding DNA sequences do not reveal significant matches even between mammalian α- and β-globin gene clusters, which diverged approximately 450 million years ago and are still expressed in a coordinated and balanced manner. They are in very different genomic contexts that show pronounced differences in regulatory mechanisms. The α-globin gene is in constitutively active chromatin and is encompassed by a CpG island, which is a dominant determinant of its regulation, whereas the β-globin gene is in A+T-rich genomic DNA. Non-coding sequence matches are not seen between avian and mammalian β-globin gene clusters, which diverged approximately 250 million years ago, despite the fact that regulation of both gene clusters requires tissue-specific activation of a chromatin domain regulated by a locus control region. The cis-regulatory sequences needed for domain opening and enhancement do show common binding sites for transcription factors. In contrast, alignments of non-coding sequences from species representing multiple eutherian mammalian orders, some of which diverged as long as 135 million years ago, are reliable predictors of novel cis-regulatory elements, both proximal and distal to the genes. Examples include a potential target for the hematopoietic transcription factor TAL1.",
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Hemoglobins from bacteria to man : Evolution of different patterns of gene expression. / Hardison, Ross.

In: Journal of Experimental Biology, Vol. 201, No. 8, 01.04.1998, p. 1099-1117.

Research output: Contribution to journalArticle

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