Dosage Compensation Mechanisms: Evolution

Abstract

Degeneration of sex‐limited chromosomes favours the emergence of dosage compensation mechanisms able to equalize in both sexes the amount of products derived from sex‐linked genes. These mechanisms are understood in detail in the fly Drosophila melanogaster, the nematode Caenorhabditis elegans and in eutherian mammals. The three systems, biochemically and evolutionarily unrelated, share a common logic.

Keywords: chromosome degeneration; sex chromosomes; chromatin; transcription regulation; evolution

References

Alekseyenko AA, Larschan E, Lai WR, Park PJ and Kuroda MI (2006) High‐resolution ChIP‐chip analysis reveals that the Drosophila MSL complex selectively identifies active genes on the male X chromosome. Genes and Development 20: 848–857.

Bernstein E and Allis CD (2005) RNA meets chromatin. Genes and Development 19: 1635–1655.

Carrel L, Park C, Tyekucheva S et al. (2006) Genomic environment predicts expression patterns on the human inactive X chromosome. PLoS Genetics 2: e151.

Charlesworth D, Charlesworth B and Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95: 118–128.

Csankovszki G, McDonel P and Meyer BJ (2004) Recruitment and spreading of the C. elegans dosage compensation complex along X chromosomes. Science 303: 1182–1185.

Demakova OV, Kotlikova IV, Gordadze PR et al. (2003) The MSL complex levels are critical for its correct targeting to the chromosomes in Drosophila melanogaster. Chromosoma 112: 103–115.

Duret L, Chureau C, Samain S, Weissenbach J and Avner P (2006 Jun 16) The Xist RNA gene evolved in eutherians by pseudogenization of a protein‐coding gene. Science 312(5780): 1653–1655.

Ercan S, Giresi PG, Whittle CM et al. (2007) X chromosome repression by localization of the C. elegans dosage compensation machinery to sites of transcription initiation. Nature Genetics 39: 403–408.

Fagegaltier D and Baker BS (2004) X chromosome sites autonomously recruit the dosage compensation complex in Drosophila males. PLoS Biology 2: e341.

Gilfillan GD, König C, Dahlsveen IK et al. (2007) Cumulative contributions of weak DNA determinants to targeting the Drosophila dosage compensation complex. Nucleic Acids Research 35: 3561–3572.

Gilfillan GD, Straub T, de Wit E et al. (2006) Chromosome‐wide gene‐specific targeting of the Drosophila dosage compensation complex. Genes and Development 20: 858–870.

Goldsmith MR, Shimada T and Abe H (2005) The genetics and genomics of the silkworm, Bombyx mori. Annual Review of Entomology 50: 71–100.

Gupta V, Parisi M, Sturgill D et al. (2006) Global analysis of X‐chromosome dosage compensation. Journal of Biology 5: 3.

Heard E and Disteche CM (2006) Dosage compensation in mammals: fine‐tuning the expression of the X chromosome. Genes and Development 20: 1848–1867.

Hore TA, Koina E, Wakefield MJ and Marshall Graves JA (2007) The region homologous to the X‐chromosome inactivation centre has been disrupted in marsupial and monotreme mammals. Chromosome Research 15: 147–161.

Itoh Y, Melamed E, Yang X et al. (2007) Dosage compensation is less effective in birds than in mammals. Journal of Biology 6: 2.

Kind J and Akhtar A (2007) Cotranscriptional recruitment of the dosage compensation complex to X‐linked target genes. Genes and Development 21: 2030–2040.

Legube G, McWeeney SK, Lercher MJ and Akhtar A (2006) X‐chromosome‐wide profiling of MSL‐1 distribution and dosage compensation in Drosophila. Genes and Development 20: 871–883.

Lucchesi JC, Kelly WG and Panning B (2005) Chromatin remodeling in dosage compensation. Annual Review of Genetics 39: 615–651.

Marín I (2003) Evolution of chromatin‐remodeling complexes: comparative genomics reveals the ancient origin of “novel” compensasome genes. Journal of Molecular Evolution 56: 527–539.

Marín I, Franke A, Bashaw GJ and Baker BS (1996) The dosage compensation system of Drosophila is co‐opted by newly evolved X chromosomes. Nature 383: 160–163.

Marín I, Siegal ML and Baker BS (2000) The evolution of dosage‐compensation mechanisms. BioEssays 22: 1106–1114.

McDonel P, Jans J, Peterson BK and Meyer BJ (2006) Clustered DNA motifs mark X chromosomes for repression by a dosage compensation complex. Nature 444: 614–618.

McNeil JA, Smith KP, Hall LL and Lawrence JB (2006) Word frequency analysis reveals enrichment of dinucleotide repeats on the human X chromosome and [GATA]n in the X escape region. Genome Research 16: 477–484.

Mendjan S and Akhtar A (2007) The right dose for every sex. Chromosoma 116: 95–106.

Meyer BJ (2005) X‐chromosome dosage compensation. The C. elegans Research Community, WormBook edition, doi/10.1895/wormbook.1.8.1, http://www.wormbook.org.

Nguyen DK and Disteche CM (2006) Dosage compensation of the active X chromosome in mammals. Nature Genetics 38: 47–53.

Ruiz MF, Esteban MR, Doñoro C, Goday C and Sánchez L (2000) Evolution of dosage compensation in Diptera: the gene maleless implements dosage compensation in Drosophila (Brachycera suborder) but its homolog in Sciara (Nematocera suborder) appears to play no role in dosage compensation. Genetics 156: 1853–1865.

Smith ER, Cayrou C, Huang R et al. (2005) A human protein complex homologous to the Drosophila MSL complex is responsible for the majority of histone H4 acetylation at lysine 16. Molecular and Cellular Biology 25: 9175–9188.

Straub T and Becker PB (2007) Dosage compensation: the beginning and end of generalization. Nature Reviews Genetics 8: 47–57.

Wang Z, Willard HF, Mukherjee S and Furey TS (2006) Evidence of influence of genomic DNA sequence on human X chromosome inactivation. PLoS Computational Biology 2: e113.

Further Reading

Akhtar A and Gasser SM (2007) The nuclear envelope and transcriptional control. Nature Reviews Genetics 8: 507–517.

Graves JA (2006) Sex chromosome specialization and degeneration in mammals. Cell 124: 901–914.

Zaratiegui M, Irvine DV and Martienssen RA (2007) Noncoding RNAs and gene silencing. Cell 128: 763–776.

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How to Cite close
Marín, Ignacio(Mar 2008) Dosage Compensation Mechanisms: Evolution. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0006128.pub2]