The rapidly evolving field of plant centromeres

Current Opinion in Plant Biology

Volumn 7, Issue 2, 2004, Pages 108-114

  Hall, Anne E ^a   Keith, Kevin C ^a   Hall, Sarah E ^a   Copenhaver, Gregory P ^b   Preuss, Daphne ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

BAC; Bacterial artificial chromosome; CEN4; CENP A; Centromere protein A; Centromere specific retrotransposon of maize; Centromere specific retrotransposon of rice; Centromere4; CRM; CRR; FISH; Fluorescent in situ hybridization

Indexed keywords

PLANT DNA;

CENTROMERE; GENETICS; MOLECULAR EVOLUTION; PLANT CHROMOSOME; REVIEW;

CENTROMERE; CHROMOSOMES, PLANT; DNA, PLANT; EVOLUTION, MOLECULAR;

BACTERIA (MICROORGANISMS); EMBRYOPHYTA; EUKARYOTA; ZEA MAYS;

EID: 1542351285     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2004.01.008     Document Type: Review

References (54)

1. Arabidopsis Genome Initiative: Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 2000, 408:796-815.
2. 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.
3. Kumekawa N., Hosouchi T., Tsuruoka H., Kotani H. The size and sequence organization of the centromeric region of Arabidopsis thaliana chromosome 5. DNA Res. 7:2000;315-321.
4. 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.
5. Hosouchi T., Kumekawa N., Tsuruoka H., Kotani H. Physical map-based sizes of the centromeric regions of Arabidopsis thaliana chromosomes 1, 2, and 3. DNA Res. 9:2002;117-121.
6. Luo S., Preuss D. Strand-biased DNA methylation associated with centromeric regions in Arabidopsis. Proc Natl Acad Sci USA. 100:2003;11133- 11138.
7. Feng Q., Zhang Y., Hao P., Wang S., Fu G., Huang Y., Li Y., Zhu J., Liu Y., Hu X.et al. Sequence and analysis of rice chromosome 4. Nature. 420:2002;316-320.
8. Cheng Z., Dong F., Langdon T., Ouyang S., Buell C.R., Gu M., Blattner F.R., Jiang J. Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell. 14:2002;1691-1704 Using FISH analysis, the authors determine the centromeric distribution and organization of rice CentO satellites and CRR retroelements, including a quantification of the satellite arrays on all 12 chromosomes. Sequence alignments reveal homology between CentO and maize CentC, which is significant given the evolutionary separation of rice and maize. Finally, telotrisomic chromosomes derived from misdivisions indicate that chromosome breakpoints map within CentO arrays, providing strong evidence that CentO is a functional component of rice centromeres.
9. Nagaki K., Song J., Stupar R.M., Parokonny A.S., Yuan Q., Ouyang S., Liu J., Hsiao J., Jones K.M., Dawe R.K.et al. Molecular and cytological analyses of large tracks of centromeric DNA reveal the structure and evolutionary dynamics of maize centromeres. Genetics. 163:2003;759-770 CentC and a centromere-specific retrotransposon were used to identify two centromere BAC clones from a maize genomic library. Sequencing indicated that both clones consist of short CentC arrays interspersed with retrotransposons. A detailed description of the CentC and retrotransposon sequences is provided, which includes alignments and phylogenetic trees generated with centromere-specific elements from other grasses.
10. Ananiev E.V., Phillips R.L., Rines H.W. Chromosome-specific molecular organization of maize (Zea mays L.) centromeric regions. Proc Natl Acad Sci USA. 95:1998;13073-13078.
11. 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.
12. 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.
13. Kaszas E., Birchler J.A. Meiotic transmission rates correlate with physical features of rearranged centromeres in maize. Genetics. 150:1998;1683-1692.
14. Stupar R.M., Lilly J.W., Town C.D., Cheng Z., Kaul S., Buell C.R., Jiang J. Complex mtDNA constitutes an approximate 620-kb insertion on Arabidopsis thaliana chromosome 2: implication of potential sequencing errors caused by large-unit repeats. Proc Natl Acad Sci USA. 98:2001;5099-5103.
15. Fransz P.F., Armstrong S., de Jong J.H., Parnell L.D., van Drunen C., Dean C., Zabel P., Bisseling T., Jones G.H. Integrated cytogenetic map of chromosome arm 4S of A. thaliana: structural organization of heterochromatic knob and centromere region. Cell. 100:2000;367-376.
16. Arabidopsis Sequencing Consortium: The complete sequence of a heterochromatic island from a higher eukaryote. Cell 2000, 100:377-386.
17. Fransz P., Armstrong S., Alonso-Blanco C., Fischer T.C., Torres-Ruiz R.A., Jones G. Cytogenetics for the model system Arabidopsis thaliana. Plant J. 13:1998;867-876.
18. Hall S.E., Kettler G., Preuss D. Centromere satellites from Arabidopsis populations: maintenance of conserved and variable domains. Genome Res. 13:2003;195-205 The authors of this paper describe the evolution of centromere satellite repeats in Arabidopsis thaliana ecotypes. Consensus sequences were derived for each of the ecotypes and the species, and the conserved and variable regions determined. The results presented here are indicative of the functionality of satellites and their rapid evolution even within a species.
19. Heslop-Harrison J.S., Brandes A., Schwarzacher T. Tandemly repeated DNA sequences and centromeric chromosomal regions of Arabidopsis species. Chromosome Res. 11:2003;241-253.
20. Wolfe K.H., Gouy M., Yang Y.W., Sharp P.M., Li W.H. Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci USA. 86:1989;6201-6205.
21. Schindelhauer D., Schwarz T. Evidence for a fast, intrachromosomal conversion mechanism from mapping of nucleotide variants within a homogeneous alpha-satellite DNA array. Genome Res. 12:2002;1815-1826.
22. Ugarkovic D., Plohl M. Variation in satellite DNA profiles - causes and effects. EMBO J. 21:2002;5955-5959 This review describes recent advances in studies of satellite sequence evolution and satellite copy number. The authors discuss current hypotheses regarding satellite evolution and their relevance to speciation events.
23. Smith G.P. Evolution of repeated DNA sequences by unequal crossover. Science. 191:1976;528-535.
24. Dover G. Molecular drive: a cohesive mode of species evolution. Nature. 299:1982;111-117.
25. Ohta T., Dover G.A. The cohesive population genetics of molecular drive. Genetics. 108:1984;501-521.
26. Elder J.F. Jr., Turner B.J. Concerted evolution of repetitive DNA sequences in eukaryotes. Q Rev Biol. 70:1995;297-320.
27. Nijman I.J., Lenstra J.A. Mutation and recombination in cattle satellite DNA: a feedback model for the evolution of satellite DNA repeats. J Mol Evol. 52:2001;361-371.
28. Sullivan K.F. A solid foundation: functional specialization of centromeric chromatin. Curr Opin Genet Dev. 11:2001;182-188.
29. Malik H.S., Vermaak D., Henikoff S. Recurrent evolution of DNA-binding motifs in the Drosophila centromeric histone. Proc Natl Acad Sci USA. 99:2002;1449-1454.
30. 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 The authors of this paper identify and analyze the A. thaliana homolog of CENP-A (HTR12). Sequencing of this gene in other Arabidopsis species showed that although the protein core is conserved, the tail has undergone more nonsynonymous changes than expected. The authors present a model for how satellite evolution is driven by the evolution of CENP-A.
31. Charlesworth B., Sniegowski P., Stephan W. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature. 371:1994;215-220.
32. Stephan W. Recombination and the evolution of satellite DNA. Genet Res. 47:1986;167-174.
33. Wright S.I., Agrawal N., Bureau T.E. Effects of recombination rate and gene density on transposable element distributions in Arabidopsis thaliana. Genome Res. 13:2003;1897-1903.
34. Eichler E.E., Sankoff D. Structural dynamics of eukaryotic chromosome evolution. Science. 301:2003;793-797.
35. Akhunov E.D., Akhunova A.R., Linkiewicz A.M., Dubcovsky J., Hummel D., Lazo G., Chao S., Anderson O.D., David J., Qi L.et al. Synteny perturbations between wheat homoeologous chromosomes caused by locus duplications and deletions correlate with recombination rates. Proc Natl Acad Sci USA. 100:2003;10836-10841.
36. Ventura M., Archidiacono N., Rocchi M. Centromere emergence in evolution. Genome Res. 11:2001;595-599.
37. Eder V., Ventura M., Ianigro M., Teti M., Rocchi M., Archidiacono N. Chromosome 6 phylogeny in primates and centromere repositioning. Mol Biol Evol. 20:2003;1506-1512 The authors use comparative FISH mapping in primates to document a centromere-repositioning event on chromosome 6. They propose this centromere-repositioning occurred because of an emergence event, rather than a transposition or inversion event, that relocated the endogenous centromere. They conclude that centromere emergence is actually fairly frequent in primates and, surprisingly, find that the repositioning process does not affect neighboring chromosomal sequences.
38. du Sart D., Cancilla M.R., Earle E., Mao J.I., Saffery R., Tainton K.M., Kalitsis P., Martyn J., Barry A.E., Choo K.H. A functional neo-centromere formed through activation of a latent human centromere and consisting of non-alpha-satellite DNA. Nat Genet. 16:1997;144-153.
39. Hiatt E.N., Dawe R.K. Four loci on abnormal chromosome 10 contribute to meiotic drive in maize. Genetics. 164:2003;699-709.
40. Maggert K.A., Karpen G.H. The activation of a neocentromere in Drosophila requires proximity to an endogenous centromere. Genetics. 158:2001;1615-1628.
41. Thomas J.W., Schueler M.G., Summers T.J., Blakesley R.W., McDowell J.C., Thomas P.J., Idol J.R., Maduro V.V., Lee-Lin S.Q., Touchman J.W.et al. Pericentromeric duplications in the laboratory mouse. Genome Res. 13:2003;55-63 Comparative mapping in humans, mice and rats identifies regions on several mouse chromosomes that contain pericentromeric duplications (duplicons), which appear to flank an ancient chromosome breakpoint. This is significant because sequence comparisons indicate that the pericentromeric duplicons are hot-spots for rearrangements and duplications. The authors propose these regions are crucial for genome evolution.
42. Nagaki K., Talbert P.B., Zhong C.X., Dawe R.K., Henikoff S., Jiang J. Chromatin immunoprecipitation reveals that the 180-bp satellite repeat is the key functional DNA element of Arabidopsis thaliana centromeres. Genetics. 163:2003;1221-1225.
43. Zhong C.X., Marshall J.B., Topp C., Mroczek R., Kato A., Nagaki K., Birchler J.A., Jiang J., Dawe R.K. Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell. 14:2002;2825-2836 This group demonstrates that antibodies to maize CENH3, a centromere-specific histone that marks functional centromeres, co-immunoprecipitate both CentC satellite and CRM retroelements. This work is significant because it suggests that, in addition to satellite DNA, a conserved retroelement may be a component of the functional maize centromere.
44. Grimes B.R., Rhoades A.A., Willard H.F. Alpha-satellite DNA and vector composition influence rates of human artificial chromosome formation. Mol Ther. 5:2002;798-805.
45. 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.
46. Sun X., Le H.D., Wahlstrom J.M., Karpen G.H. Sequence analysis of a functional Drosophila centromere. Genome Res. 13:2003;182-194.
47. Comai L., Tyagi A.P., Lysak M.A. FISH analysis of meiosis in Arabidopsis allopolyploids. Chromosome Res. 11:2003;217-226.
48. Xia X., Selvaraj G., Bertrand H. Structure and evolution of a highly repetitive DNA sequence from Brassica napus. Plant Mol Biol. 21:1993;213-224.
49. Hudakova S., Michalek W., Presting G.G., ten Hoopen R., dos Santos K., Jasencakova Z., Schubert I. Sequence organization of barley centromeres. Nucleic Acids Res. 29:2001;5029-5035.
50. Gindullis F., Desel C., Galasso I., Schmidt T. The large-scale organization of the centromeric region in Beta species. Genome Res. 11:2001;253-265.
51. Morgante M., Jurman I., Shi L., Zhu T., Keim P., Rafalski J.A. The STR120 satellite DNA of soybean: organization, evolution and chromosomal specificity. Chromosome Res. 5:1997;363-373.
52. Zwick M.S., Islam-Faridi M.N., Zhang H.B., Hodnett G.L., Gomez M.I., Kim J.S., Price H.J., Stelly D.M. Distribution and sequence analysis of the centromere-associated repetitive element CEN38 of Sorghum bicolor (Poaceae). Am J Bot. 87:2000;1757-1764.
53. Grellet F., Delcasso D., Panabieres F., Delseny M. Organization and evolution of a higher plant alphoid-like satellite DNA sequence. J Mol Biol. 187:1986;495-507.
54. Kishii M., Nagaki K., Tsujimoto H. A tandem repetitive sequence located in the centromeric region of common wheat (Triticum aestivum) chromosomes. Chromosome Res. 9:2001;417-428.