• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Mar 2001; 157(3): 1293–1298.
PMCID: PMC1461554

Adaptive evolution of Cid, a centromere-specific histone in Drosophila.


Centromeric DNA is generally composed of large blocks of tandem satellite repeats that change rapidly due to loss of old arrays and expansion of new repeat classes. This extreme heterogeneity of centromeric DNA is difficult to reconcile with the conservation of the eukaryotic chromosome segregation machinery. Histone H3-like proteins, including Cid in Drosophila melanogaster, are a unique chromatin component of centromeres. In comparisons between closely related species of Drosophila, we find an excess of replacement changes that have been fixed since the separation of D. melanogaster and D. simulans, suggesting adaptive evolution. The last adaptive changes appear to have occurred recently, as evident from a reduction in polymorphism in the melanogaster lineage. Adaptive evolution has occurred both in the long N-terminal tail as well as in the histone fold of Cid. In the histone fold, the replacement changes have occurred in the region proposed to mediate binding to DNA. We propose that this rapid evolution of Cid is driven by a response to the changing satellite repeats at centromeres. Thus, centromeric H3-like proteins may act as adaptors between evolutionarily labile centromeric DNA and the conserved kinetochore machinery.

Full Text

The Full Text of this article is available as a PDF (254K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Lohe AR, Hilliker AJ, Roberts PA. Mapping simple repeated DNA sequences in heterochromatin of Drosophila melanogaster. Genetics. 1993 Aug;134(4):1149–1174. [PMC free article] [PubMed]
  • Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997 Sep 18;389(6648):251–260. [PubMed]
  • Masumoto H, Ikeno M, Nakano M, Okazaki T, Grimes B, Cooke H, Suzuki N. Assay of centromere function using a human artificial chromosome. Chromosoma. 1998 Dec;107(6-7):406–416. [PubMed]
  • McDonald JH, Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. [PubMed]
  • Murphy TD, Karpen GH. Centromeres take flight: alpha satellite and the quest for the human centromere. Cell. 1998 May 1;93(3):317–320. [PubMed]
  • Nachman MW, Brown WM, Stoneking M, Aquadro CF. Nonneutral mitochondrial DNA variation in humans and chimpanzees. Genetics. 1996 Mar;142(3):953–963. [PMC free article] [PubMed]
  • Arents G, Burlingame RW, Wang BC, Love WE, Moudrianakis EN. The nucleosomal core histone octamer at 3.1 A resolution: a tripartite protein assembly and a left-handed superhelix. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10148–10152. [PMC free article] [PubMed]
  • Palmer DK, O'Day K, Margolis RL. The centromere specific histone CENP-A is selectively retained in discrete foci in mammalian sperm nuclei. Chromosoma. 1990 Dec;100(1):32–36. [PubMed]
  • Barry AE, Bateman M, Howman EV, Cancilla MR, Tainton KM, Irvine DV, Saffery R, Choo KH. The 10q25 neocentromere and its inactive progenitor have identical primary nucleotide sequence: further evidence for epigenetic modification. Genome Res. 2000 Jun;10(6):832–838. [PMC free article] [PubMed]
  • Palmer DK, O'Day K, Trong HL, Charbonneau H, Margolis RL. Purification of the centromere-specific protein CENP-A and demonstration that it is a distinctive histone. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3734–3738. [PMC free article] [PubMed]
  • Platero JS, Ahmad K, Henikoff S. A distal heterochromatic block displays centromeric activity when detached from a natural centromere. Mol Cell. 1999 Dec;4(6):995–1004. [PubMed]
  • Round EK, Flowers SK, Richards EJ. Arabidopsis thaliana centromere regions: genetic map positions and repetitive DNA structure. Genome Res. 1997 Nov;7(11):1045–1053. [PubMed]
  • Copenhaver GP, Nickel K, Kuromori T, Benito MI, Kaul S, Lin X, Bevan M, Murphy G, Harris B, Parnell LD, et al. Genetic definition and sequence analysis of Arabidopsis centromeres. Science. 1999 Dec 24;286(5449):2468–2474. [PubMed]
  • Rozas J, Rozas R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics. 1999 Feb;15(2):174–175. [PubMed]
  • Csink AK, Henikoff S. Something from nothing: the evolution and utility of satellite repeats. Trends Genet. 1998 May;14(5):200–204. [PubMed]
  • Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. [PubMed]
  • Haaf T, Willard HF. Chromosome-specific alpha-satellite DNA from the centromere of chimpanzee chromosome 4. Chromosoma. 1997 Sep;106(4):226–232. [PubMed]
  • Shelby RD, Vafa O, Sullivan KF. Assembly of CENP-A into centromeric chromatin requires a cooperative array of nucleosomal DNA contact sites. J Cell Biol. 1997 Feb 10;136(3):501–513. [PMC free article] [PubMed]
  • Harrington JJ, Van Bokkelen G, Mays RW, Gustashaw K, Willard HF. Formation of de novo centromeres and construction of first-generation human artificial microchromosomes. Nat Genet. 1997 Apr;15(4):345–355. [PubMed]
  • Stoler S, Keith KC, Curnick KE, Fitzgerald-Hayes M. A mutation in CSE4, an essential gene encoding a novel chromatin-associated protein in yeast, causes chromosome nondisjunction and cell cycle arrest at mitosis. Genes Dev. 1995 Mar 1;9(5):573–586. [PubMed]
  • Hudson RR, Kreitman M, Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987 May;116(1):153–159. [PMC free article] [PubMed]
  • Takahashi K, Chen ES, Yanagida M. Requirement of Mis6 centromere connector for localizing a CENP-A-like protein in fission yeast. Science. 2000 Jun 23;288(5474):2215–2219. [PubMed]
  • Jørgensen AL, Laursen HB, Jones C, Bak AL. Evolutionarily different alphoid repeat DNA on homologous chromosomes in human and chimpanzee. Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3310–3314. [PMC free article] [PubMed]
  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997 Dec 15;25(24):4876–4882. [PMC free article] [PubMed]
  • Karpen GH, Allshire RC. The case for epigenetic effects on centromere identity and function. Trends Genet. 1997 Dec;13(12):489–496. [PubMed]
  • Wiens GR, Sorger PK. Centromeric chromatin and epigenetic effects in kinetochore assembly. Cell. 1998 May 1;93(3):313–316. [PubMed]
  • Keith KC, Baker RE, Chen Y, Harris K, Stoler S, Fitzgerald-Hayes M. Analysis of primary structural determinants that distinguish the centromere-specific function of histone variant Cse4p from histone H3. Mol Cell Biol. 1999 Sep;19(9):6130–6139. [PMC free article] [PubMed]
  • Yoda K, Ando S, Morishita S, Houmura K, Hashimoto K, Takeyasu K, Okazaki T. Human centromere protein A (CENP-A) can replace histone H3 in nucleosome reconstitution in vitro. Proc Natl Acad Sci U S A. 2000 Jun 20;97(13):7266–7271. [PMC free article] [PubMed]
  • Laurent AM, Puechberty J, Roizès G. Hypothesis: for the worst and for the best, L1Hs retrotransposons actively participate in the evolution of the human centromeric alphoid sequences. Chromosome Res. 1999;7(4):305–317. [PubMed]
  • Zwick ME, Salstrom JL, Langley CH. Genetic variation in rates of nondisjunction: association of two naturally occurring polymorphisms in the chromokinesin nod with increased rates of nondisjunction in Drosophila melanogaster. Genetics. 1999 Aug;152(4):1605–1614. [PMC free article] [PubMed]
  • Le MH, Duricka D, Karpen GH. Islands of complex DNA are widespread in Drosophila centric heterochromatin. Genetics. 1995 Sep;141(1):283–303. [PMC free article] [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...