Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 10 August 2001:
Vol. 293. no. 5532, pp. 1098 - 1102
DOI: 10.1126/science.1062939
Prev | Table of Contents | Next

Review

The Centromere Paradox: Stable Inheritance with Rapidly Evolving DNA

Steven Henikoff,* Kami Ahmad, Harmit S. Malik

Every eukaryotic chromosome has a centromere, the locus responsible for poleward movement at mitosis and meiosis. Although conventional loci are specified by their DNA sequences, current evidence favors a chromatin-based inheritance mechanism for centromeres. The chromosome segregation machinery is highly conserved across all eukaryotes, but the DNA and protein components specific to centromeric chromatin are evolving rapidly. Incompatibilities between rapidly evolving centromeric components may be responsible for both the organization of centromeric regions and the reproductive isolation of emerging species.

Howard Hughes Medical Institute Research Laboratories, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue North, Seattle, WA 98109, USA.
*   To whom correspondence should be addressed. E-mail: steveh{at}fhcrc.org

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Population genetic analysis of shotgun assemblies of genomic sequences from multiple individuals.
I. Hellmann, Y. Mang, Z. Gu, P. Li, F. M. de la Vega, A. G. Clark, and R. Nielsen (2008)
Genome Res. 18, 1020-1029
   Abstract »    Full Text »    PDF »
A high-resolution map of nucleosome positioning on a fission yeast centromere.
J. S. Song, X. Liu, X. S. Liu, and X. He (2008)
Genome Res. 18, 1064-1072
   Abstract »    Full Text »    PDF »
Rapid Evolution of Yeast Centromeres in the Absence of Drive.
D. Bensasson, M. Zarowiecki, A. Burt, and V. Koufopanou (2008)
Genetics 178, 2161-2167
   Abstract »    Full Text »    PDF »
Molecular Population Genetics of Drosophila Subtelomeric DNA.
J. A. Anderson, Y. S. Song, and C. H. Langley (2008)
Genetics 178, 477-487
   Abstract »    Full Text »    PDF »
Epigenetic Modification of Centromeric Chromatin: Hypomethylation of DNA Sequences in the CENH3-Associated Chromatin in Arabidopsis thaliana and Maize.
W. Zhang, H.-R. Lee, D.-H. Koo, and J. Jiang (2008)
PLANT CELL 20, 25-34
   Abstract »    Full Text »    PDF »
Genomic Instability Within Centromeres of Interspecific Marsupial Hybrids.
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 (2007)
Genetics 177, 2507-2517
   Abstract »    Full Text »    PDF »
Mitch a rapidly evolving component of the Ndc80 kinetochore complex required for correct chromosome segregation in Drosophila.
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 (2007)
J. Cell Sci. 120, 3522-3533
   Abstract »    Full Text »    PDF »
Inaugural Article: Structure, dynamics, and evolution of centromeric nucleosomes.
Y. Dalal, T. Furuyama, D. Vermaak, and S. Henikoff (2007)
PNAS 104, 15974-15981
   Abstract »    Full Text »    PDF »
Evolution of Gene Sequence in Response to Chromosomal Location.
C. Diaz-Castillo and K. G. Golic (2007)
Genetics 177, 359-374
   Abstract »    Full Text »    PDF »
A Linkage Map Reveals a Complex Basis for Segregation Distortion in an Interpopulation Cross in the Moss Ceratodon purpureus.
S. F. McDaniel, J. H. Willis, and A. J. Shaw (2007)
Genetics 176, 2489-2500
   Abstract »    Full Text »    PDF »
Functional Sequestration of Transcription Factor Activity by Repetitive DNA.
X. Liu, B. Wu, J. Szary, E. M. Kofoed, and F. Schaufele (2007)
J. Biol. Chem. 282, 20868-20876
   Abstract »    Full Text »    PDF »
Speciation in Drosophila: From Phenotypes to Molecules.
H. A. Orr, J. Masly, and N. Phadnis (2007)
J. Hered. 98, 103-110
   Abstract »    Full Text »    PDF »
Comparative Genetics of Potential Prezygotic and Postzygotic Isolating Barriers in a Lycopersicon Species Cross.
L. C. Moyle (2007)
J. Hered. 98, 123-135
   Abstract »    Full Text »    PDF »
Cytogenetic and Molecular Characterization of Heterochromatin Gene Models in Drosophila melanogaster.
F. Rossi, R. Moschetti, R. Caizzi, N. Corradini, and P. Dimitri (2007)
Genetics 175, 595-607
   Abstract »    Full Text »    PDF »
Pervasive Adaptive Evolution among Interactors of the Drosophila Hybrid Inviability Gene, Nup96.
D. C. Presgraves and W. Stephan (2007)
Mol. Biol. Evol. 24, 306-314
   Abstract »    Full Text »    PDF »
Duplication of Centromeric Histone H3 (HTR12) Gene in Arabidopsis halleri and A. lyrata, Plant Species With Multiple Centromeric Satellite Sequences.
A. Kawabe, S. Nasuda, and D. Charlesworth (2006)
Genetics 174, 2021-2032
   Abstract »    Full Text »    PDF »
Interplay of Selective Pressure and Stochastic Events Directs Evolution of the MEL172 Satellite DNA Library in Root-Knot Nematodes.
N. Mestrovic, P. Castagnone-Sereno, and M. Plohl (2006)
Mol. Biol. Evol. 23, 2316-2325
   Abstract »    Full Text »    PDF »
Transcription and Evolutionary Dynamics of the Centromeric Satellite Repeat CentO in Rice.
H.-R. Lee, P. Neumann, J. Macas, and J. Jiang (2006)
Mol. Biol. Evol. 23, 2505-2520
   Abstract »    Full Text »    PDF »
Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila..
N. J. Brideau, H. A. Flores, J. Wang, S. Maheshwari, X. Wang, and D. A. Barbash (2006)
Science 314, 1292-1295
   Abstract »    Full Text »    PDF »
Phylogenetic Analysis of Fungal Centromere H3 Proteins.
R. E. Baker and K. Rogers (2006)
Genetics 174, 1481-1492
   Abstract »    Full Text »    PDF »
An Artificially Constructed De Novo Human Chromosome Behaves Almost Identically to Its Natural Counterpart during Metaphase and Anaphase in Living Cells..
T. Tsuduki, M. Nakano, N. Yasuoka, S. Yamazaki, T. Okada, Y. Okamoto, and H. Masumoto (2006)
Mol. Cell. Biol. 26, 7682-7695
   Abstract »    Full Text »    PDF »
Genomic and Genetic Characterization of Rice Cen3 Reveals Extensive Transcription and Evolutionary Implications of a Complex Centromere.
H. Yan, H. Ito, K. Nobuta, S. Ouyang, W. Jin, S. Tian, C. Lu, R.C. Venu, G.-l. Wang, P. J. Green, et al. (2006)
PLANT CELL 18, 2123-2133
   Abstract »    Full Text »    PDF »
Partitioning of the Maize Epigenome by the Number of Methyl Groups on Histone H3 Lysines 9 and 27.
J. Shi and R. K. Dawe (2006)
Genetics 173, 1571-1583
   Abstract »    Full Text »    PDF »
Evidence on the chromosomal location of centromeric DNA in Plasmodium falciparum from etoposide-mediated topoisomerase-II cleavage.
J. M. Kelly, L. McRobert, and D. A. Baker (2006)
PNAS 103, 6706-6711
   Abstract »    Full Text »    PDF »
Chaperone-mediated assembly of centromeric chromatin in vitro.
T. Furuyama, Y. Dalal, and S. Henikoff (2006)
PNAS 103, 6172-6177
   Abstract »    Full Text »    PDF »
Dynamic evolution at pericentromeres.
A. E. Hall, G. C. Kettler, and D. Preuss (2006)
Genome Res. 16, 355-364
   Abstract »    Full Text »    PDF »
Human centromeric alphoid domains are periodically homogenized so that they vary substantially between homologues. Mechanism and implications for centromere functioning..
G. Roizes (2006)
Nucleic Acids Res. 34, 1912-1924
   Abstract »    Full Text »    PDF »
The CNA1 Histone of the Ciliate Tetrahymena thermophila Is Essential for Chromosome Segregation in the Germline Micronucleus.
M. D. Cervantes, X. Xi, D. Vermaak, M.-C. Yao, and H. S. Malik (2006)
Mol. Biol. Cell 17, 485-497
   Abstract »    Full Text »    PDF »
Assembly of additional heterochromatin distinct from centromere-kinetochore chromatin is required for de novo formation of human artificial chromosome.
H. Nakashima, M. Nakano, R. Ohnishi, Y. Hiraoka, Y. Kaneda, A. Sugino, and H. Masumoto (2005)
J. Cell Sci. 118, 5885-5898
   Abstract »    Full Text »    PDF »
Genetic interactions of separase regulatory subunits reveal the diverged Drosophila Cenp-C homolog.
S. Heeger, O. Leismann, R. Schittenhelm, O. Schraidt, S. Heidmann, and C. F. Lehner (2005)
Genes & Dev. 19, 2041-2053
   Abstract »    Full Text »    PDF »
The Transcribed 165-bp CentO Satellite Is the Major Functional Centromeric Element in the Wild Rice Species Oryza punctata.
W. Zhang, C. Yi, W. Bao, B. Liu, J. Cui, H. Yu, X. Cao, M. Gu, M. Liu, and Z. Cheng (2005)
Plant Physiology 139, 306-315
   Abstract »    Full Text »    PDF »
Centromere renewal and replacement in the plant kingdom.
R. K. Dawe (2005)
PNAS 102, 11573-11574
   Full Text »    PDF »
From The Cover: Chromatin immunoprecipitation cloning reveals rapid evolutionary patterns of centromeric DNA in Oryza species.
H.-R. Lee, W. Zhang, T. Langdon, W. Jin, H. Yan, Z. Cheng, and J. Jiang (2005)
PNAS 102, 11793-11798
   Abstract »    Full Text »    PDF »
Differential Rates of Local and Global Homogenization in Centromere Satellites From Arabidopsis Relatives.
S. E. Hall, S. Luo, A. E. Hall, and D. Preuss (2005)
Genetics 170, 1913-1927
   Abstract »    Full Text »    PDF »
Progressive proximal expansion of the primate X chromosome centromere.
M. G. Schueler, J. M. Dunn, C. P. Bird, M. T. Ross, L. Viggiano, NISC Comparative Sequencing Program, M. Rocchi, H. F. Willard, and E. D. Green (2005)
PNAS 102, 10563-10568
   Abstract »    Full Text »    PDF »
Visualization of Diffuse Centromeres with Centromere-Specific Histone H3 in the Holocentric Plant Luzula nivea.
K. Nagaki, K. Kashihara, and M. Murata (2005)
PLANT CELL 17, 1886-1893
   Abstract »    Full Text »    PDF »
Sobo, a Recently Amplified Satellite Repeat of Potato, and Its Implications for the Origin of Tandemly Repeated Sequences.
A. L. Tek, J. Song, J. Macas, and J. Jiang (2005)
Genetics 170, 1231-1238
   Abstract »    Full Text »    PDF »
The genetic basis of reproductive isolation: Insights from Drosophila.
H. A. Orr (2005)
PNAS 102, 6522-6526
   Abstract »    Full Text »    PDF »
Retention of Latent Centromeres in the Mammalian Genome.
G. C. Ferreri, D. M. Liscinsky, J. A. Mack, M. D. B. Eldridge, and R. J. O'Neill (2005)
J. Hered. 96, 217-224
   Abstract »    Full Text »    PDF »
Molecular and Functional Dissection of the Maize B Chromosome Centromere.
W. Jin, J. C. Lamb, J. M. Vega, R. K. Dawe, J. A. Birchler, and J. Jiang (2005)
PLANT CELL 17, 1412-1423
   Abstract »    Full Text »    PDF »
Structure, Divergence, and Distribution of the CRR Centromeric Retrotransposon Family in Rice.
K. Nagaki, P. Neumann, D. Zhang, S. Ouyang, C. R. Buell, Z. Cheng, and J. Jiang (2005)
Mol. Biol. Evol. 22, 845-855
   Abstract »    Full Text »    PDF »
Identification of Xenopus CENP-A and an Associated Centromeric DNA Repeat.
N. S. Edwards and A. W. Murray (2005)
Mol. Biol. Cell 16, 1800-1810
   Abstract »    Full Text »    PDF »
Histone variants: deviants?.
R. T. Kamakaka and S. Biggins (2005)
Genes & Dev. 19, 295-316
   Abstract »    Full Text »    PDF »
Segregation Distortion in Hybrids Between the Bogota and USA Subspecies of Drosophila pseudoobscura.
H. A. Orr and S. Irving (2005)
Genetics 169, 671-682
   Abstract »    Full Text »    PDF »
Functional mapping of a trypanosome centromere by chromosome fragmentation identifies a 16-kb GC-rich transcriptional "strand-switch" domain as a major feature.
S. O. Obado, M. C. Taylor, S. R. Wilkinson, E. V. Bromley, and J. M. Kelly (2005)
Genome Res. 15, 36-43
   Abstract »    Full Text »    PDF »
Satellite DNA From the Y Chromosome of the Malaria Vector Anopheles gambiae.
J. Krzywinski, D. Sangare, and N. J. Besansky (2005)
Genetics 169, 185-196
   Abstract »    Full Text »    PDF »
A Novel Meiotic Drive Locus Almost Completely Distorts Segregation in Mimulus (Monkeyflower) Hybrids.
L. Fishman and J. H. Willis (2005)
Genetics 169, 347-353
   Abstract »    Full Text »    PDF »
A variant histone H3 is enriched at telomeres in Trypanosoma brucei.
J. E. Lowell and G. A. M. Cross (2004)
J. Cell Sci. 117, 5937-5947
   Abstract »    Full Text »    PDF »
Centromere-encoded RNAs are integral components of the maize kinetochore.
C. N. Topp, C. X. Zhong, and R. K. Dawe (2004)
PNAS 101, 15986-15991
   Abstract »    Full Text »    PDF »
Human, Mouse, and Rat Genome Large-Scale Rearrangements: Stability Versus Speciation.
S. Zhao, J. Shetty, L. Hou, A. Delcher, B. Zhu, K. Osoegawa, P. de Jong, W. C. Nierman, R. L. Strausberg, and C. M. Fraser (2004)
Genome Res. 14, 1851-1860
   Abstract »    Full Text »    PDF »
Centromere Dynamics and Chromosome Evolution in Marsupials.
R. J. O'Neill, M. D. B. Eldridge, and C. J. Metcalfe (2004)
J. Hered. 95, 375-381
   Abstract »    Full Text »    PDF »
Adaptive Evolution of the Histone Fold Domain in Centromeric Histones.
J. L. Cooper and S. Henikoff (2004)
Mol. Biol. Evol. 21, 1712-1718
   Abstract »    Full Text »    PDF »
Centromeric DNA sequences in the pathogenic yeast Candida albicans are all different and unique.
K. Sanyal, M. Baum, and J. Carbon (2004)
PNAS 101, 11374-11379
   Abstract »    Full Text »    PDF »
Functional Complementation of Human Centromere Protein A (CENP-A) by Cse4p from Saccharomyces cerevisiae.
G. Wieland, S. Orthaus, S. Ohndorf, S. Diekmann, and P. Hemmerich (2004)
Mol. Cell. Biol. 24, 6620-6630
   Abstract »    Full Text »    PDF »
The Small Chromosomes of Trypanosoma brucei Involved in Antigenic Variation Are Constructed Around Repetitive Palindromes.
B. Wickstead, K. Ersfeld, and K. Gull (2004)
Genome Res. 14, 1014-1024
   Abstract »    Full Text »    PDF »
Human centromere repositioning "in progress".
D. J. Amor, K. Bentley, J. Ryan, J. Perry, L. Wong, H. Slater, and K. H. A. Choo (2004)
PNAS 101, 6542-6547
   Abstract »    Full Text »    PDF »
Structural features of the rice chromosome 4 centromere.
Y. Zhang, Y. Huang, L. Zhang, Y. Li, T. Lu, Y. Lu, Q. Feng, Q. Zhao, Z. Cheng, Y. Xue, et al. (2004)
Nucleic Acids Res. 32, 2023-2030
   Abstract »    Full Text »    PDF »
Lessons from the Genome Sequence of Neurospora crassa: Tracing the Path from Genomic Blueprint to Multicellular Organism.
K. A. Borkovich, L. A. Alex, O. Yarden, M. Freitag, G. E. Turner, N. D. Read, S. Seiler, D. Bell-Pedersen, J. Paietta, N. Plesofsky, et al. (2004)
Microbiol. Mol. Biol. Rev. 68, 1-108
   Abstract »    Full Text »    PDF »
Maize Centromeres: Organization and Functional Adaptation in the Genetic Background of Oat.
W. Jin, J. R. Melo, K. Nagaki, P. B. Talbert, S. Henikoff, R. K. Dawe, and J. Jiang (2004)
PLANT CELL 16, 571-581
   Abstract »    Full Text »    PDF »
Histone H3 lysine 9 methylation is required for DNA elimination in developing macronuclei in Tetrahymena.
Y. Liu, K. Mochizuki, and M. A. Gorovsky (2004)
PNAS 101, 1679-1684
   Abstract »    Full Text »    PDF »
Human Artificial Chromosomes with Alpha Satellite-Based De Novo Centromeres Show Increased Frequency of Nondisjunction and Anaphase Lag.
M. K. Rudd, R. W. Mays, S. Schwartz, and H. F. Willard (2003)
Mol. Cell. Biol. 23, 7689-7697
   Abstract »    Full Text »    PDF »
Epigenetic assembly of centromeric chromatin at ectopic {alpha}-satellite sites on human chromosomes.
M. Nakano, Y. Okamoto, J.-i. Ohzeki, and H. Masumoto (2003)
J. Cell Sci. 116, 4021-4034
   Abstract »    Full Text »    PDF »
KNL-1 directs assembly of the microtubule-binding interface of the kinetochore in C. elegans.
A. Desai, S. Rybina, T. Muller-Reichert, A. Shevchenko, A. Shevchenko, A. Hyman, and K. Oegema (2003)
Genes & Dev. 17, 2421-2435
   Abstract »    Full Text »    PDF »
Marcus Rhoades, Preferential Segregation and Meiotic Drive.
J. A. Birchler, R. K. Dawe, and J. F. Doebley (2003)
Genetics 164, 835-841
   Full Text »    PDF »
Chromatin Immunoprecipitation Reveals That the 180-bp Satellite Repeat Is the Key Functional DNA Element of Arabidopsis thaliana Centromeres.
K. Nagaki, P. B. Talbert, C. X. Zhong, R. K. Dawe, S. Henikoff, and J. Jiang (2003)
Genetics 163, 1221-1225
   Abstract »    Full Text »    PDF »
The Neurobiology of Rett Syndrome.
S. Akbarian (2003)
Neuroscientist 9, 57-63
   Abstract »    PDF »
RNA Interference, Transposons, and the Centromere.
R. K. Dawe (2003)
PLANT CELL 15, 297-301
   Full Text »    PDF »
Centromere Satellites From Arabidopsis Populations: Maintenance of Conserved and Variable Domains.
S. E. Hall, G. Kettler, and D. Preuss (2003)
Genome Res. 13, 195-205
   Abstract »    Full Text »    PDF »
CENP-B box is required for de novo centromere chromatin assembly on human alphoid DNA.
J.-i. Ohzeki, M. Nakano, T. Okada, and H. Masumoto (2002)
J. Cell Biol. 159, 765-775
   Abstract »    Full Text »    PDF »
Genome Organization and Reorganization in Evolution: Formatting for Computation and Function.
J. A. SHAPIRO (2002)
Ann. N.Y. Acad. Sci. 981, 111-134
   Abstract »    Full Text »    PDF »
On the Roles of Repetitive DNA Elements in the Context of a Unified Genomic-Epigenetic System.
R. v. STERNBERG (2002)
Ann. N.Y. Acad. Sci. 981, 154-188
   Abstract »    Full Text »    PDF »
Evidence for a Fast, Intrachromosomal Conversion Mechanism From Mapping of Nucleotide Variants Within a Homogeneous alpha -Satellite DNA Array.
D. Schindelhauer and T. Schwarz (2002)
Genome Res. 12, 1815-1826
   Abstract »    Full Text »    PDF »
Centromere Targeting Element within the Histone Fold Domain of Cid.
D. Vermaak, H. S. Hayden, and S. Henikoff (2002)
Mol. Cell. Biol. 22, 7553-7561
   Abstract »    Full Text »    PDF »
Centromeric Retroelements and Satellites Interact with Maize Kinetochore Protein CENH3.
C. X. Zhong, J. B. Marshall, C. Topp, R. Mroczek, A. Kato, K. Nagaki, J. A. Birchler, J. Jiang, and R. K. Dawe (2002)
PLANT CELL 14, 2825-2836
   Abstract »    Full Text »    PDF »
The CENP-A homolog CaCse4p in the pathogenic yeast Candida albicans is a centromere protein essential for chromosome transmission.
K. Sanyal and J. Carbon (2002)
PNAS 99, 12969-12974
   Abstract »    Full Text »    PDF »
Archaeal Histone Tetramerization Determines DNA Affinity and the Direction of DNA Supercoiling.
F. Marc, K. Sandman, R. Lurz, and J. N. Reeve (2002)
J. Biol. Chem. 277, 30879-30886
   Abstract »    Full Text »    PDF »
Functional Rice Centromeres Are Marked by a Satellite Repeat and a Centromere-Specific Retrotransposon.
Z. Cheng, F. Dong, T. Langdon, S. Ouyang, C. R. Buell, M. Gu, F. R. Blattner, and J. Jiang (2002)
PLANT CELL 14, 1691-1704
   Abstract »    Full Text »    PDF »
Evolution of Genome Size in Drosophila. Is the Invader's Genome Being Invaded by Transposable Elements?.
C. Vieira, C. Nardon, C. Arpin, D. Lepetit, and C. Biemont (2002)
Mol. Biol. Evol. 19, 1154-1161
   Abstract »    Full Text »    PDF »
The Unique Centromeric Chromatin Structure of Schizosaccharomyces pombe Is Maintained during Meiosis.
J. B. Smirnova and R. J. McFarlane (2002)
J. Biol. Chem. 277, 19817-19822
   Abstract »    Full Text »    PDF »
Heterochromatin in Animals and Plants. Similarities and Differences.
Z. V. Avramova (2002)
Plant Physiology 129, 40-49
   Full Text »    PDF »
Centromeric Localization and Adaptive Evolution of an Arabidopsis Histone H3 Variant.
P. B. Talbert, R. Masuelli, A. P. Tyagi, L. Comai, and S. Henikoff (2002)
PLANT CELL 14, 1053-1066
   Abstract »    Full Text »    PDF »
Recurrent evolution of DNA-binding motifs in the Drosophila centromeric histone.
H. S. Malik, D. Vermaak, and S. Henikoff (2002)
PNAS
   Abstract »    Full Text »    PDF »
Genomic and Genetic Definition of a Functional Human Centromere.
M. G. Schueler, A. W. Higgins, M. K. Rudd, K. Gustashaw, H. F. Willard, and H. F. Willard (2001)
Science 294, 109-115
   Abstract »    Full Text »    PDF »
Recurrent evolution of DNA-binding motifs in the Drosophila centromeric histone.
H. S. Malik, D. Vermaak, and S. Henikoff (2002)
PNAS 99, 1449-1454
   Abstract »    Full Text »    PDF »