Epigenetic silencing may aid evolution by gene duplication

S. Rodin, Arthur D. Riggs

Research output: Contribution to journalArticle

74 Citations (Scopus)

Abstract

Gene duplication is commonly regarded as the main evolutionary path toward the gain of a new function. However, even with gene duplication, there is a loss-versus-gain dilemma: most newly born duplicates degrade to pseudogenes, since degenerative mutations are much more frequent than advantageous ones. Thus, something additional seems to be needed to shift the loss versus gain equilibrium toward functional divergence. We suggest that epigenetic silencing of duplicates might play this role in evolution. This study began when we noticed in a previous publication (Lynch M, Conery JS [2000] Science 291:1151-1155) that the frequency of functional young gene duplicates is higher in organisms that have cytosine methylation (H. sapiens, M. musculus, and A. thaliana) than in organisms that do not have methylated genomes (S. cerevisiae, D. melanogaster, and C. elegans). We find that genome data analysis confirms the likelihood of much more efficient functional divergence of gene duplicates in mammals and plants than in yeast, nematode, and fly. We have also extended the classic model of gene duplication, in which newly duplicated genes have exactly the same expression pattern, to the case when they are epigenetically silenced in a tissue- and/or developmental stage-complementary manner. This exposes each of the duplicates to negative selection, thus protecting from "pseudogenization." Our analysis indicates that this kind of silencing (i) enhances evolution of duplicated genes to new functions, particularly in small populations, (ii) is quite consistent with the subfunctionalization model when degenerative but complementary mutations affect different subfunctions of the gene, and (iii) furthermore, may actually cooperate with the DDC (duplication-degeneration-complementation) process.

Original languageEnglish
Pages (from-to)718-729
Number of pages12
JournalJournal of Molecular Evolution
Volume56
Issue number6
DOIs
Publication statusPublished - Jun 1 2003

Fingerprint

Gene Duplication
gene duplication
Duplicate Genes
Epigenomics
epigenetics
duplicate genes
Genes
gene
Genome
mutation
Mutation
Pseudogenes
Melanogaster
genome
genes
pseudogenes
cytosine
Cytosine
organisms
Diptera

Keywords

  • Comparative genomics
  • Gene expression
  • Gene families
  • Imprinting
  • Methylation
  • Pseudogenes

ASJC Scopus subject areas

  • Genetics
  • Biochemistry
  • Biochemistry, Genetics and Molecular Biology(all)
  • Genetics(clinical)
  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Agricultural and Biological Sciences(all)
  • Agricultural and Biological Sciences (miscellaneous)

Cite this

Epigenetic silencing may aid evolution by gene duplication. / Rodin, S.; Riggs, Arthur D.

In: Journal of Molecular Evolution, Vol. 56, No. 6, 01.06.2003, p. 718-729.

Research output: Contribution to journalArticle

Rodin, S. ; Riggs, Arthur D. / Epigenetic silencing may aid evolution by gene duplication. In: Journal of Molecular Evolution. 2003 ; Vol. 56, No. 6. pp. 718-729.
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