Genetics, Vol. 157, 1293-1298, March 2001, Copyright © 2001

Adaptive Evolution of Cid, a Centromere-Specific Histone in Drosophila

Harmit S. Malikb and Steven Henikoffb,a
a Howard Hughes Medical Institute, Seattle, Washington 98109
b Fred Hutchinson Cancer Research Center, Seattle, Washington 98109

Corresponding author: Steven Henikoff, 1100 Fairview Ave. N., A1-162, Seattle, WA 98109., steveh{at}fhcrc.org (E-mail)

Communicating editor: J. A. BIRCHLER

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.




This article has been cited by other articles:


Home page
 GeneticsHome page
C. J. Metcalfe, K. V. Bulazel, G. C. Ferreri, E. Schroeder-Reiter, G. Wanner, W. Rens, C. Obergfell, M. D. B. Eldridge, and R. J. O'Neill
Genomic Instability Within Centromeres of Interspecific Marsupial Hybrids
Genetics, December 1, 2007; 177(4): 2507 - 2517.
[Abstract] [Full Text] [PDF]

Home page
 J. Cell Sci.Home page
B. Williams, G. Leung, H. Maiato, A. Wong, Z. Li, E. V. Williams, C. Kirkpatrick, C. F. Aquadro, C. L. Rieder, and M. L. Goldberg
Mitch a rapidly evolving component of the Ndc80 kinetochore complex required for correct chromosome segregation in Drosophila
J. Cell Sci., October 15, 2007; 120(20): 3522 - 3533.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
Y. Dalal, T. Furuyama, D. Vermaak, and S. Henikoff
Inaugural Article: Structure, dynamics, and evolution of centromeric nucleosomes
PNAS, October 9, 2007; 104(41): 15974 - 15981.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
M. A. Rodriguez, D. Vermaak, J. J. Bayes, and H. S. Malik
Species-specific positive selection of the male-specific lethal complex that participates in dosage compensation in Drosophila
PNAS, September 25, 2007; 104(39): 15412 - 15417.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
A. Villasante, J. P. Abad, and M. Mendez-Lago
Centromeres were derived from telomeres during the evolution of the eukaryotic chromosome
PNAS, June 19, 2007; 104(25): 10542 - 10547.
[Abstract] [Full Text] [PDF]

Home page
 J HeredHome page
H. A. Orr, J. Masly, and N. Phadnis
Speciation in Drosophila: From Phenotypes to Molecules
J. Hered., March 1, 2007; 98(2): 103 - 110.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
D. C. Presgraves and W. Stephan
Pervasive Adaptive Evolution among Interactors of the Drosophila Hybrid Inviability Gene, Nup96
Mol. Biol. Evol., January 1, 2007; 24(1): 306 - 314.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
A. Kawabe, S. Nasuda, and D. Charlesworth
Duplication of Centromeric Histone H3 (HTR12) Gene in Arabidopsis halleri and A. lyrata, Plant Species With Multiple Centromeric Satellite Sequences
Genetics, December 1, 2006; 174(4): 2021 - 2032.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
H.-R. Lee, P. Neumann, J. Macas, and J. Jiang
Transcription and Evolutionary Dynamics of the Centromeric Satellite Repeat CentO in Rice
Mol. Biol. Evol., December 1, 2006; 23(12): 2505 - 2520.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
R. E. Baker and K. Rogers
Phylogenetic Analysis of Fungal Centromere H3 Proteins
Genetics, November 1, 2006; 174(3): 1481 - 1492.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
G. Roizes
Human centromeric alphoid domains are periodically homogenized so that they vary substantially between homologues. Mechanism and implications for centromere functioning.
Nucleic Acids Res., January 1, 2006; 34(6): 1912 - 1924.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Biol. CellHome page
M. D. Cervantes, X. Xi, D. Vermaak, M.-C. Yao, and H. S. Malik
The CNA1 Histone of the Ciliate Tetrahymena thermophila Is Essential for Chromosome Segregation in the Germline Micronucleus
Mol. Biol. Cell, January 1, 2006; 17(1): 485 - 497.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
R. E. Baker and K. Rogers
Genetic and Genomic Analysis of the AT-Rich Centromere DNA Element II of Saccharomyces cerevisiae
Genetics, December 1, 2005; 171(4): 1463 - 1475.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
H.-R. Lee, W. Zhang, T. Langdon, W. Jin, H. Yan, Z. Cheng, and J. Jiang
From The Cover: Chromatin immunoprecipitation cloning reveals rapid evolutionary patterns of centromeric DNA in Oryza species
PNAS, August 16, 2005; 102(33): 11793 - 11798.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
S. E. Hall, S. Luo, A. E. Hall, and D. Preuss
Differential Rates of Local and Global Homogenization in Centromere Satellites From Arabidopsis Relatives
Genetics, August 1, 2005; 170(4): 1913 - 1927.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Biol. CellHome page
N. S. Edwards and A. W. Murray
Identification of Xenopus CENP-A and an Associated Centromeric DNA Repeat
Mol. Biol. Cell, April 1, 2005; 16(4): 1800 - 1810.
[Abstract] [Full Text] [PDF]

Home page
 Eukaryot CellHome page
L. Morey, K. Barnes, Y. Chen, M. Fitzgerald-Hayes, and R. E. Baker
The Histone Fold Domain of Cse4 Is Sufficient for CEN Targeting and Propagation of Active Centromeres in Budding Yeast
Eukaryot. Cell, December 1, 2004; 3(6): 1533 - 1543.
[Abstract] [Full Text] [PDF]

Home page
 J. Cell Sci.Home page
J. E. Lowell and G. A. M. Cross
A variant histone H3 is enriched at telomeres in Trypanosoma brucei
J. Cell Sci., November 15, 2004; 117(24): 5937 - 5947.
[Abstract] [Full Text] [PDF]

Home page
 J. Cell Sci.Home page
K. L. Arney and A. G. Fisher
Epigenetic aspects of differentiation
J. Cell Sci., September 1, 2004; 117(19): 4355 - 4363.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
J. L. Cooper and S. Henikoff
Adaptive Evolution of the Histone Fold Domain in Centromeric Histones
Mol. Biol. Evol., September 1, 2004; 21(9): 1712 - 1718.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Cell. Biol.Home page
G. Wieland, S. Orthaus, S. Ohndorf, S. Diekmann, and P. Hemmerich
Functional Complementation of Human Centromere Protein A (CENP-A) by Cse4p from Saccharomyces cerevisiae
Mol. Cell. Biol., August 1, 2004; 24(15): 6620 - 6630.
[Abstract] [Full Text] [PDF]

Home page
 Plant CellHome page
W. Jin, J. R. Melo, K. Nagaki, P. B. Talbert, S. Henikoff, R. K. Dawe, and J. Jiang
Maize Centromeres: Organization and Functional Adaptation in the Genetic Background of Oat
PLANT CELL, March 1, 2004; 16(3): 571 - 581.
[Abstract] [Full Text] [PDF]

Home page
 Genome ResHome page
S. E. Hall, G. Kettler, and D. Preuss
Centromere Satellites From Arabidopsis Populations: Maintenance of Conserved and Variable Domains
Genome Res., February 1, 2003; 13(2): 195 - 205.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Cell. Biol.Home page
D. Vermaak, H. S. Hayden, and S. Henikoff
Centromere Targeting Element within the Histone Fold Domain of Cid
Mol. Cell. Biol., November 1, 2002; 22(21): 7553 - 7561.
[Abstract] [Full Text] [PDF]

Home page
 Plant CellHome page
C. X. Zhong, J. B. Marshall, C. Topp, R. Mroczek, A. Kato, K. Nagaki, J. A. Birchler, J. Jiang, and R. K. Dawe
Centromeric Retroelements and Satellites Interact with Maize Kinetochore Protein CENH3
PLANT CELL, November 1, 2002; 14(11): 2825 - 2836.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
K. Sanyal and J. Carbon
The CENP-A homolog CaCse4p in the pathogenic yeast Candida albicans is a centromere protein essential for chromosome transmission
PNAS, October 1, 2002; 99(20): 12969 - 12974.
[Abstract] [Full Text] [PDF]

Home page
 Plant CellHome page
P. B. Talbert, R. Masuelli, A. P. Tyagi, L. Comai, and S. Henikoff
Centromeric Localization and Adaptive Evolution of an Arabidopsis Histone H3 Variant
PLANT CELL, May 1, 2002; 14(5): 1053 - 1066.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
G. A. Maston and M. Ruvolo
Chorionic Gonadotropin Has a Recent Origin Within Primates and an Evolutionary History of Selection
Mol. Biol. Evol., March 1, 2002; 19(3): 320 - 335.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
H. S. Malik, D. Vermaak, and S. Henikoff
Recurrent evolution of DNA-binding motifs in the Drosophila centromeric histone
PNAS, January 17, 2002; (2002) 32664299.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
F. Pardo-Manuel de Villena and C. Sapienza
Female Meiosis Drives Karyotypic Evolution in Mammals
Genetics, November 1, 2001; 159(3): 1179 - 1189.
[Abstract] [Full Text] [PDF]

Home page
 ScienceHome page
S. Henikoff, K. Ahmad, and H. S. Malik
The Centromere Paradox: Stable Inheritance with Rapidly Evolving DNA
Science, August 10, 2001; 293(5532): 1098 - 1102.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
H. S. Malik, D. Vermaak, and S. Henikoff
Recurrent evolution of DNA-binding motifs in the Drosophila centromeric histone
PNAS, February 5, 2002; 99(3): 1449 - 1454.
[Abstract] [Full Text] [PDF]

Home page
 Plant CellHome page
E. N. Hiatt, E. K. Kentner, and R. K. Dawe
Independently Regulated Neocentromere Activity of Two Classes of Tandem Repeat Arrays
PLANT CELL, February 1, 2002; 14(2): 407 - 420.
[Abstract] [Full Text] [PDF]