Evolution of closely linked gene pairs in vertebrate genomes

E. Franck, T. Hulsen, M.A. Huynen, W.W. de Jong, N.H. Lunsen, O. Madsen

Research output: Contribution to journalArticleAcademicpeer-review

9 Citations (Scopus)

Abstract

The orientation of closely linked genes in mammalian genomes is not random: there are more head-to-head (h2h) gene pairs than expected. To understand the origin of this enrichment in h2h gene pairs, we have analyzed the phylogenetic distribution of gene pairs separated by less than 600 bp of intergenic DNA (gene duos). We show here that a lack of head-to-tail (h2t) gene duos is an even more distinctive characteristic of mammalian genomes, with the platypus genome as the only exception. In nonmammalian vertebrate and in nonvertebrate genomes, the frequency of h2h, h2t, and tail-to-tail (t2t) gene duos is close to random. In tetrapod genomes, the h2t and t2t gene duos are more likely to be part of a larger gene cluster of closely spaced genes than h2h gene duos; in fish and urochordate genomes, the reverse is seen. In human and mouse tissues, the expression profiles of gene duos were skewed toward positive coexpression, irrespective of orientation. The organization of orthologs of both members of about 40% of the human gene duos could be traced in other species, enabling a prediction of the organization at the branch points of gnathostomes, tetrapods, amniotes, and euarchontoglires. The accumulation of h2h gene duos started in tetrapods, whereas that of h2t and t2t gene duos only started in amniotes. The apparent lack of evolutionary conservation of h2t and t2t gene duos relative to that of h2h gene duos is thus a result of their relatively late origin in the lineage leading to mammals; we show that once they are formed h2t and t2t gene duos are as stable as h2h gene duos.
LanguageEnglish
Pages1909-1921
JournalMolecular Biology and Evolution
Volume25
Issue number9
DOIs
Publication statusPublished - 2008

Fingerprint

Vertebrates
vertebrate
genome
vertebrates
Genome
gene
Genes
genes
tetrapod
Tail
Platypus
tail
Urochordata
Intergenic DNA
Tunicata
Multigene Family
Transcriptome
intergenic DNA
multigene family
Mammals

Keywords

  • head-to-head
  • bidirectional promoters
  • transcriptional interference
  • antisense transcription
  • organization
  • conservation
  • elongation
  • expression
  • mammals
  • origin

Cite this

Franck, E., Hulsen, T., Huynen, M. A., de Jong, W. W., Lunsen, N. H., & Madsen, O. (2008). Evolution of closely linked gene pairs in vertebrate genomes. Molecular Biology and Evolution, 25(9), 1909-1921. https://doi.org/10.1093/molbev/msn136
Franck, E. ; Hulsen, T. ; Huynen, M.A. ; de Jong, W.W. ; Lunsen, N.H. ; Madsen, O. / Evolution of closely linked gene pairs in vertebrate genomes. In: Molecular Biology and Evolution. 2008 ; Vol. 25, No. 9. pp. 1909-1921.
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Franck, E, Hulsen, T, Huynen, MA, de Jong, WW, Lunsen, NH & Madsen, O 2008, 'Evolution of closely linked gene pairs in vertebrate genomes', Molecular Biology and Evolution, vol. 25, no. 9, pp. 1909-1921. https://doi.org/10.1093/molbev/msn136

Evolution of closely linked gene pairs in vertebrate genomes. / Franck, E.; Hulsen, T.; Huynen, M.A.; de Jong, W.W.; Lunsen, N.H.; Madsen, O.

In: Molecular Biology and Evolution, Vol. 25, No. 9, 2008, p. 1909-1921.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Evolution of closely linked gene pairs in vertebrate genomes

AU - Franck, E.

AU - Hulsen, T.

AU - Huynen, M.A.

AU - de Jong, W.W.

AU - Lunsen, N.H.

AU - Madsen, O.

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N2 - The orientation of closely linked genes in mammalian genomes is not random: there are more head-to-head (h2h) gene pairs than expected. To understand the origin of this enrichment in h2h gene pairs, we have analyzed the phylogenetic distribution of gene pairs separated by less than 600 bp of intergenic DNA (gene duos). We show here that a lack of head-to-tail (h2t) gene duos is an even more distinctive characteristic of mammalian genomes, with the platypus genome as the only exception. In nonmammalian vertebrate and in nonvertebrate genomes, the frequency of h2h, h2t, and tail-to-tail (t2t) gene duos is close to random. In tetrapod genomes, the h2t and t2t gene duos are more likely to be part of a larger gene cluster of closely spaced genes than h2h gene duos; in fish and urochordate genomes, the reverse is seen. In human and mouse tissues, the expression profiles of gene duos were skewed toward positive coexpression, irrespective of orientation. The organization of orthologs of both members of about 40% of the human gene duos could be traced in other species, enabling a prediction of the organization at the branch points of gnathostomes, tetrapods, amniotes, and euarchontoglires. The accumulation of h2h gene duos started in tetrapods, whereas that of h2t and t2t gene duos only started in amniotes. The apparent lack of evolutionary conservation of h2t and t2t gene duos relative to that of h2h gene duos is thus a result of their relatively late origin in the lineage leading to mammals; we show that once they are formed h2t and t2t gene duos are as stable as h2h gene duos.

AB - The orientation of closely linked genes in mammalian genomes is not random: there are more head-to-head (h2h) gene pairs than expected. To understand the origin of this enrichment in h2h gene pairs, we have analyzed the phylogenetic distribution of gene pairs separated by less than 600 bp of intergenic DNA (gene duos). We show here that a lack of head-to-tail (h2t) gene duos is an even more distinctive characteristic of mammalian genomes, with the platypus genome as the only exception. In nonmammalian vertebrate and in nonvertebrate genomes, the frequency of h2h, h2t, and tail-to-tail (t2t) gene duos is close to random. In tetrapod genomes, the h2t and t2t gene duos are more likely to be part of a larger gene cluster of closely spaced genes than h2h gene duos; in fish and urochordate genomes, the reverse is seen. In human and mouse tissues, the expression profiles of gene duos were skewed toward positive coexpression, irrespective of orientation. The organization of orthologs of both members of about 40% of the human gene duos could be traced in other species, enabling a prediction of the organization at the branch points of gnathostomes, tetrapods, amniotes, and euarchontoglires. The accumulation of h2h gene duos started in tetrapods, whereas that of h2t and t2t gene duos only started in amniotes. The apparent lack of evolutionary conservation of h2t and t2t gene duos relative to that of h2h gene duos is thus a result of their relatively late origin in the lineage leading to mammals; we show that once they are formed h2t and t2t gene duos are as stable as h2h gene duos.

KW - head-to-head

KW - bidirectional promoters

KW - transcriptional interference

KW - antisense transcription

KW - organization

KW - conservation

KW - elongation

KW - expression

KW - mammals

KW - origin

U2 - 10.1093/molbev/msn136

DO - 10.1093/molbev/msn136

M3 - Article

VL - 25

SP - 1909

EP - 1921

JO - Molecular Biology and Evolution

T2 - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

SN - 0737-4038

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ER -