Conflict begets complexity: The evolution of centromeres

Current Opinion in Genetics and Development

Volumn 12, Issue 6, 2002, Pages 711-718

  Malik, Harmit S ^b   Henikoff, Steven ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; SATELLITE DNA;

BUDDING; CELL ACTIVITY; CELL SURVIVAL; CENTROMERE; CHROMOSOME; COMPLEX FORMATION; CONFLICT; EUKARYOTIC CELL; EVOLUTION; GENE MAPPING; GENE SEGREGATION; GENE STRUCTURE; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; YEAST; FEMALE; GENETICS; MALE; MEIOSIS; X CHROMOSOME;

EUKARYOTA; SACCHAROMYCETALES;

CENTROMERE; CHROMOSOMES, HUMAN, X; DNA, SATELLITE; EVOLUTION; FEMALE; HUMANS; MALE; MEIOSIS;

EID: 0036889219     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(02)00351-9     Document Type: Review

References (51)

1. Ng R., Carbon J. Mutational and in vitro protein-binding studies on centromere DNA from Saccharomyces cerevisiae. Mol Cell Biol. 7:1987;4522-4534.
2. Cumberledge S., Carbon J. Mutational analysis of meiotic and mitotic centromere function in Saccharomyces cerevisiae. Genetics. 117:1987;203-212.
3. Chikashige Y., Kinoshita N., Nakaseko Y., Matsumoto T., Murakami S., Niwa O., Yanagida M. Composite motifs and repeat symmetry in S. pombe centromeres: direct analysis by integration of NotI restriction sites. Cell. 57:1989;739-751.
4. Wood V., Gwilliam R., Rajandream M.A., Lyne M., Lyne R., Stewart A., Sgouros J., Peat N., Hayles J., Baker S., et al. The genome sequence of Schizosaccharomyces pombe. Nature. 415:2002;871-880.
5. Bernard P., Maure J.F., Partridge J.F., Genier S., Javerzat J.P., Allshire R.C. Requirement of heterochromatin for cohesion at centromeres. Science. 294:2001;2539-2542. See annotation [6•] .
6. Nonaka N., Kitajima T., Yokobayashi S., Xiao G., Yamamoto M., Grewal S.I., Watanabe Y. Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast. Nat Cell Biol. 4:2002;89-93. Complexcentromeres are always found surrounded by heterochromatin, but why? These reports now provide convincing evidence that pericentric heterochromatin serves to recruit cohesins specifically at centromeres, essential for proper segregation of sister centromeres.
7. Round E.K., Flowers S.K., Richards E.J. Arabidopsis thaliana centromere regions: genetic map positions and repetitive DNA structure. Genome Res. 7:1997;1045-1053.
8. Sun X., Wahlstrom J., Karpen G. Molecular structure of a functional Drosophila centromere. Cell. 91:1997;1007-1019.
9. Charlesworth B., Sniegowski P., Stephan W. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature. 371:1994;215-220.
10. Alexandrov I., Kazakov A., Tumeneva I., Shepelev V., Yurov Y. Alpha-satellite DNA of primates: old and new families. Chromosoma. 110:2001;253-266.
11. Baldini A., Miller D.A., Miller O.J., Ryder O.A., Mitchell A.R. A chimpanzee-derived chromosome-specific alpha satellite DNA sequence conserved between chimpanzee and human. Chromosoma. 100:1991;156-161.
12. Samonte R.V., Ramesh K.H., Verma R.S. Comparative mapping of human alphoid satellite DNA repeat sequences in the great apes. Genetica. 101:1997;97-104.
13. Haaf T., Willard H.F. Chromosome-specific alpha-satellite DNA from the centromere of chimpanzee chromosome 4. Chromosoma. 106:1997;226-232.
14. Jorgensen A.L., Laursen H.B., Jones C., Bak A.L. Evolutionarily different alphoid repeat DNA on homologous chromosomes in human and chimpanzee. Proc Natl Acad Sci USA. 89:1992;3310-3314.
15. Romanova L.Y., Deriagin G.V., Mashkova T.D., Tumeneva I.G., Mushegian A.R., Kisselev L.L., Alexandrov I.A. Evidence for selection in evolution of alpha satellite DNA: the central role of CENP-B/pJ alpha binding region. J Mol Biol. 261:1996;334-340.
16. Haaf T., Mater A.G., Wienberg J., Ward D.C. Presence and abundance of CENP-B box sequences in great ape subsets of primate-specific alpha-satellite DNA. J Mol Evol. 41:1995;487-491.
17. Hudson D.F., Fowler K.J., Earle E., Saffery R., Kalitsis P., Trowell H., Hill J., Wreford N.G., de Kretser D.M., Cancilla M.R., et al. Centromere protein B null mice are mitotically and meiotically normal but have lower body and testis weights. J Cell Biol. 141:1998;309-319.
18. Smit A.F., Riggs A.D. Tiggers and DNA transposon fossils in the human genome. Proc Natl Acad Sci USA. 93:1996;1443-1448.
19. Kipling D., Warburton P.E. Centromeres, CENP-B and Tigger too. Trends Genet. 13:1997;141-145.
20. Pelissier T., Tutois S., Tourmente S., Deragon J.M., Picard G. DNA regions flanking the major Arabidopsis thaliana satellite are principally enriched in Athila retroelement sequences. Genetica. 97:1996;141-151.
21. Kumekawa N., Hosouchi T., Tsuruoka H., Kotani H. The size and sequence organization of the centromeric region of Arabidopsis thaliana chromosome 4. DNA Res. 8:2001;285-290. The authors used refined restriction mapping to re-size the centromeres to increase estimates by >2 Mb! Although the authors still do not have a sequence consensus of the central core, they highlight the gradient of sequence heterogeneity that steadily decreases as they approach the 'core', allowing them to propose what it probably looks like: a combination of 180 bp repeats and Athila retrotransposons in a regular array.
22. Agudo M., Losada A., Abad J.P., Pimpinelli S., Ripoll P., Villasante A. Centromeres from telomeres? The centromeric region of the Y chromosome of Drosophila melanogaster contains a tandem array of telomeric HeT-A- and TART-related sequences. Nucleic Acids Res. 27:1999;3318-3324.
23. Schueler M.G., Higgins A.W., Rudd M.K., Gustashaw K., Willard H.F. Genomic and genetic definition of a functional human centromere. Science. 294:2001;109-115. A tour de force, not only for successfully assembling the sequence of a complex centromere but also for elucidating the evolutionary landscape at the human X centromere. The study provides the closest look at the evolutionary forces that constantly shape centromeric regions.
24. McAllister B.F., Werren J.H. Evolution of tandemly repeated sequences: What happens at the end of an array? J Mol Evol. 48:1999;469-481.
25. Csink A.K., Henikoff S. Something from nothing, the evolution and utility of satellite repeats. Trends Genet. 14:1998;200-204.
26. Copenhaver G.P., Nickel K., Kuromori T., Benito M.I., Kaul S., Lin X., Bevan M., Murphy G., Harris B., Parnell L.D., et al. Genetic definition and sequence analysis of Arabidopsis centromeres. Science. 286:1999;2468-2474.
27. Haupt W., Fischer T.C., Winderl S., Fransz P., Torres-Ruiz R.A. The centromere1 (CEN1) region of Arabidopsis thaliana: architecture and functional impact of chromatin. Plant J. 27:2001;285-296. The CEN1 core is defined as being separate from the pericentric regions based on recombination rates, sequence properties and in situ hybridization. The authors make use of a lethal mutation tightly linked to CEN1 to map the centromere. This study reveals sharp thresholds for drop in recombination frequencies between pericentric heterochromatin and centromere 'core' regions.
28. Lo A.W., Craig J.M., Saffery R., Kalitsis P., Irvine D.V., Earle E., Magliano D.J., Choo K.H. A 330 kb CENP-A binding domain and altered replication timing at a human neocentromere. EMBO J. 20:2001;2087-2096. The authors amend the boundaries of the mardel(10) neocentromere from earlier reports. They find altered replication timing as well as a distinctive pattern of repetitive elements distinguishes the neocentromere from surrounding regions.
29. Palmer D.K., O'Day K., Trong H.L., Charbonneau H., Margolis R.L. Purification of the centromere-specific protein CENP-A and demonstration that it is a distinctive histone. Proc Natl Acad Sci USA. 88:1991;3734-3738.
30. Henikoff S., Ahmad K., Malik H.S. The centromere paradox: stable inheritance with rapidly evolving DNA. Science. 293:2001;1098-1102. We summarize evidence for the 'centromere paradox' and present an evolutionary model to explain it. Rapid divergence of centromeric DNA and CenH3s is also expected to contribute to fitness consequences in the heterogametic sex, suggesting centromere-drive as a novel means to mediate postzygotic isolation between species.
31. Satinover D.L., Vance G.H., Van Dyke D.L., Schwartz S. Cytogenetic analysis and construction of a BAC contig across a common neocentromeric region from 9p. Chromosoma. 110:2001;275-283.
32. Warburton P.E., Dolled M., Mahmood R., Alonso A., Li S., Naritomi K., Tohma T., Nagai T., Hasegawa T., Ohashi H., et al. Molecular cytogenetic analysis of eight inversion duplications of human chromosome 13q that each contain a neocentromere. Am J Hum Genet. 66:2000;1794-1806.
33. Ventura M., Archidiacono N., Rocchi M. Centromere emergence in evolution. Genome Res. 11:2001;595-599. In comparing three primate X chromosomes, marker order is found to be perfectly conserved whereas centromere position is not. Having ruled out the trivial and much less parsimonious explanation of many pericentric inversions, the authors point to centromere emergence as the most likely explanation for centromere repositioning.
34. Malik H.S., Henikoff S. Adaptive evolution of Cid, a centromere-specific histone in Drosophila. Genetics. 157:2001;1293-1298. Comparison of Cid (CenH3) sequences from different strains of D. melanogaster and D. simulans provide evidence of positive selection. One of the positively selected regions corresponds to the Loop I region of the histone-fold domain that is believed to make specific contacts with the DNA, suggesting altered DNA-binding as the reason behind adaptive evolution.
35. Talbert P.B., Masuelli R., Tyagi A.P., Comai L., Henikoff S. Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell. 14:2002;1053-1066.
36. Henikoff S., Malik H.S. Centromeres, selfish drivers. Nature. 417:2002;227.
37. Pardo-Manuel de Villena F., Sapienza C. Transmission ratio distortion in offspring of heterozygous female carriers of Robertsonian translocations. Hum Genet. 108:2001;31-36.
38. Pardo-Manuel de Villena F., Sapienza C. Female meiosis drives karyotypic evolution in mammals. Genetics. 159:2001;1179-1189. The authors expand on earlier work studying the transmission advantage of Robertsonian fusions in female meiosis. They collate karyotype data from different mammalian orders to argue in favor of the model in which asymmetries in female meiosis will lead to directional adjustment of the karyotype either toward or away from a particular chromosome form, rapidly bringing about karyotypic changes.
39. Petrie M., Schwabl H., Brande-Lavridsen N., Burke T. Maternal investment. Sex differences in avian yolk hormone levels. Nature. 412:2001;498-499.
40. Sheldon B.C., Andersson S., Griffith S.C., Ornborg J., Sendecka J. Ultraviolet colour variation influences blue tit sex ratios. Nature. 402:1999;874-877.
41. Rhoades M.M. Preferential segregation in maize. Genetics. 27:1942;395-407.
42. Dawe R.K., Cande W.Z. Induction of centromeric activity in maize by suppressor of meiotic drive 1. Proc Natl Acad Sci USA. 93:1996;8512-8517.
43. Buckler E.S. iv, Phelps-Durr T.L., Buckler C.S., Dawe R.K., Doebley J.F., Holtsford T.P. Meiotic drive of chromosomal knobs reshaped the maize genome. Genetics. 153:1999;415-426.
44. Alfenito M.R., Birchler J.A. Molecular characterization of a maize B chromosome centric sequence. Genetics. 135:1993;589-597.
45. Hiatt E.N., Kentner E.K., Dawe R.K. Independently regulated neocentromere activity of two classes of tandem repeat arrays. Plant Cell. 14:2002;407-420. Two different repeat classes are found in maize knobs. This study reveals that both of these, together with their respective binding proteins, constitute independent drive systems. Experiments with drugs that arrest microtubule dynamics but do not affect knob neocentromeric activity also suggest that the binding proteins are most likely responsible for motor activity.
46. Kaszas E., Birchler J.A. Meiotic transmission rates correlate with physical features of rearranged centromeres in maize. Genetics. 150:1998;1683-1692.
47. Page B.T., Wanous M.K., Birchler J.A. Characterization of a maize chromosome 4 centromeric sequence: evidence for an evolutionary relationship with the B chromosome centromere. Genetics. 159:2001;291-302. This study shows that the primary constriction of chromosome 4 has a major representation of a repeat that is related to the B-specific centromere sequence, confirming the evolutionary relationship between the centromeres of chromosome 4 and the B chromosome. It also discusses alternative models for the origin of B chromosomes in maize.
48. Daniel A., Hook E.B., Wulf G. Risks of unbalanced progeny at amniocentesis to carriers of chromosome rearrangements: data from United States and Canadian laboratories. Am J Med Genet. 33:1989;14-53.
49. Daniel A. Distortion of female meiotic segregation and reduced male fertility in human Robertsonian translocations: consistent with the centromere model of co-evolving centromere DNA/centromeric histone (CENP-A). Am J Med Genet. 111:2002;450-452.
50. Heus J.J., Zonneveld B.J., Steensma H.Y., Van den Berg J.A. Centromeric DNA of Kluyveromyces lactis. Curr Genet. 18:1990;517-522.
51. Baum M., Ngan V.K., Clarke L. The centromeric K-type repeat and the central core are together sufficient to establish a functional Schizosaccharomyces pombe centromere. Mol Biol Cell. 5:1994;747-761.