Centromere location in Arabidopsis is unaltered by extreme divergence in CENH3 protein sequence

Genome Research

Volumn 27, Issue 3, 2017, Pages 471-478

  Maheshwari, Shamoni ^a   Ishii, Takayoshi ^b   Brown, C Titus ^a   Houben, Andreas ^b   Comai, Luca ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; CENH3 PROTEIN; UNCLASSIFIED DRUG; CENTROMERE PROTEIN A;

AMINO ACID SEQUENCE; ARABIDOPSIS THALIANA; ARTICLE; CENTROMERE; CONTROLLED STUDY; DNA BINDING; DNA SEQUENCE; EPIGENETICS; GENE LOCATION; GENETIC BACKGROUND; GENETIC VARIABILITY; HAPLOIDY; LEPIDIUM; LEPIDIUM OLERACEUM; MAIZE; NONHUMAN; NUCLEOSOME; OUTCROSSING; PLANT GENOME; PRIORITY JOURNAL; PROTEIN INTERACTION; ARABIDOPSIS; CHEMISTRY; GENETIC POLYMORPHISM; GENETICS; METABOLISM; MOLECULAR EVOLUTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CENTROMERE; CENTROMERE PROTEIN A; EVOLUTION, MOLECULAR; NUCLEOSOMES; POLYMORPHISM, GENETIC;

EID: 85016501045     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.214619.116     Document Type: Article

References (57)

1. Allshire RC, Karpen GH. 2008. Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat Rev Genet 9: 923-937.
2. Birchler JA, Gao Z, Sharma A, Presting GG, Han F. 2011. Epigenetic aspects of centromere function in plants. Curr Opin Plant Biol 14: 217-222.
3. Cerutti F, Gamba R, Mazzagatti A, Piras FM, Cappelletti E, Belloni E, Nergadze SG, Raimondi E, Giulotto E. 2016. The major horse satellite DNA family is associated with centromere competence. Mol Cytogenet 9: 35.
4. Chen WC. 2011. "Overlapping codon model, phylogenetic clustering, and alternative partial expectation conditional maximization algorithm. " PhD thesis, Iowa State University, Ames, IA.
5. Chmátal L, Gabriel SI, Mitsainas GP, Martínez-Vargas J, Ventura J, Searle JB, Schultz RM, Lampson MA. 2014. Centromere strength provides the cell biological basis for meiotic drive and karyotype evolution in mice. Curr Biol 24: 2295-2300.
6. Cooper JL, Henikoff S. 2004. Adaptive evolution of the histone fold domain in centromeric histones. Mol Biol Evol 21: 1712-1718.
7. Copenhaver GP. 2003. Using Arabidopsis to understand centromere function: progress and prospects. Chromosome Res 11: 255-262.
8. Copenhaver GP, Nickel K, Kuromori T, Benito MI, Kaul S, Lin X, Bevan M, Murphy G, Harris B, Parnell LD, et al. 1999. Genetic definition and sequence analysis of Arabidopsis centromeres. Science 286: 2468-2474.
9. Drinnenberg IA, Henikoff S, Malik HS. 2016. Evolutionary turnover of kinetochore proteins: a ship of theseus? Trends Cell Biol 26: 498-510.
10. Fishman L, Saunders A. 2008. Centromere-associated female meiotic drive entails male fitness costs in monkeyflowers. Science 322: 1559-1562.
11. Fransz PF, Armstrong S, de Jong JH, Parnell LD, van Drunen C, Dean C, Zabel P, Bisseling T, Jones GH. 2000. Integrated cytogenetic map of chromosome arm 4S of A. thaliana: structural organization of heterochromatic knob and centromere region. Cell 100: 367-376.
12. Gong Z, Wu Y, Koblizkova A, Torres GA, Wang K, Iovene M, Neumann P, Zhang W, Novak P, Buell CR, et al. 2012. Repeatless and repeat-based centromeres in potato: implications for centromere evolution. Plant Cell 24: 3559-3574.
13. Hall SE, Luo S, Hall AE, Preuss D. 2005. Differential rates of local and global homogenization in centromere satellites from Arabidopsis relatives. Genetics 170: 1913-1927.
14. Harris RS. 2007. "Improved pairwise alignment of genomic DNA. " PhD thesis, Pennsylvania State University, State College, PA.
15. Henikoff S, Ahmad K, Malik HS. 2001. The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293: 1098-1102.
16. Henikoff JG, Thakur J, Kasinathan S, Henikoff S. 2015. A unique chromatin complex occupies young a-satellite arrays of human centromeres. Sci Adv 1: e1400234.
17. Heslop-Harrison JS, Murata M, Ogura Y, Schwarzacher T, Motoyoshi F. 1999. Polymorphisms and genomic organization of repetitive DNA from centromeric regions of Arabidopsis chromosomes. Plant Cell 11: 31-42.
18. Ishii T, Karimi-Ashtiyani R, Banaei-Moghaddam AM, Schubert V, Fuchs J, Houben A. 2015a. The differential loading of two barley CENH3 variants into distinct centromeric substructures is cell type-and development-specific. Chromosome Res 23: 277-284.
19. Ishii T, Sunamura N, Matsumoto A, Eltayeb AE, Tsujimoto H. 2015b. Preferential recruitment of the maternal centromere-specific histone H3 (CENH3) in oat (Avena sativa L.) ? pearl millet (Pennisetum glaucum L.) hybrid embryos. Chromosome Res 23: 709-718.
20. Jin W, Melo JR, Nagaki K, Talbert PB, Henikoff S, Dawe RK, Jiang J. 2004. Maize centromeres: organization and functional adaptation in the genetic background of oat. Plant Cell 16: 571-581.
21. Kim KE, Peluso P, Baybayan P, Yeadon PJ, Yu C, Fisher W, Chin CS, Rapicavoli NA, Rank DR, Li J, et al. 2014. Long-read, whole genome shotgun sequence data for five model organisms. Sci Data 1: 140045.
22. Lee HR, Hayden KE, Willard HF. 2011. Organization and molecular evolution of CENP-A-associated satellite DNA families in a basal primate genome. Genome Biol Evol 3: 1136-1149.
23. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
24. Lin X, Kaul S, Rounsley S, Shea TP, Benito MI, Town CD, Fujii CY, Mason T, Bowman CL, Barnstead M, et al. 1999. Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature 402: 761-768.
25. Maheshwari S, Tan EH, West A, Franklin FC, Comai L, Chan SW. 2015. Naturally occurring differences in CENH3 affect chromosome segregation in zygotic mitosis of hybrids. PLoS Genet 11: e1004970.
26. Malik HS, Henikoff S. 2001. Adaptive evolution of Cid, a centromere-specific histone in Drosophila. Genetics 157: 1293-1298.
27. Malik HS, Henikoff S. 2009. Major evolutionary transitions in centromere complexity. Cell 138: 1067-1082.
28. Malik HS, Vermaak D, Henikoff S. 2002. Recurrent evolution of DNA-binding motifs in the Drosophila centromeric histone. Proc Natl Acad Sci 99: 1449-1454.
29. Maluszynska J, Heslop-Harrison JS. 1991. Localization of tandemly repeated DNA sequences in Arabidopsis thaliana. Plant J 1: 159-166.
30. McKinley KL, Cheeseman IM. 2016. The molecular basis for centromere identity and function. Nat Rev Mol Cell Biol 17: 16-29.
31. Miga KH, Newton Y, Jain M, Altemose N, Willard HF, Kent WJ. 2014. Centromere reference models for human chromosomes X and Y satellite arrays. Genome Res 24: 697-707.
32. Nagaki K, Talbert PB, Zhong CX, Dawe RK, Henikoff S, Jiang J. 2003. Chromatin immunoprecipitation reveals that the 180-bp satellite repeat is the key functional DNA element of Arabidopsis thaliana centromeres. Genetics 163: 1221-1225.
33. Nagaki K, Cheng Z, Ouyang S, Talbert PB, Kim M, Jones KM, Henikoff S, Buell CR, Jiang J. 2004. Sequencing of a rice centromere uncovers active genes. Nat Genet 36: 138-145.
34. Nakano M, Cardinale S, Noskov VN, Gassmann R, Vagnarelli P, Kandels-Lewis S, Larionov V, Earnshaw WC, Masumoto H. 2008. Inactivation of a human kinetochore by specific targeting of chromatin modifiers. Dev Cell 14: 507-522.
35. Neumann P, Schubert V, Fukova I, Manning JE, Houben A, Macas J. 2016. Epigenetic histone marks of extended meta-polycentric centromeres of Lathyrus and Pisum chromosomes. Front Plant Sci 7: 234.
36. Paradis E, Claude J, Strimmer K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289-290.
37. Pluta AF, Mackay AM, Ainsztein AM, Goldberg IG, Earnshaw WC. 1995. The centromere: hub of chromosomal activities. Science 270: 1591-1594.
38. R Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.Rproject. org/.
39. Rosin L, Mellone BG. 2016. Co-evolving CENP-A and CAL1 domains mediate centromeric CENP-A deposition across Drosophila species. Dev Cell 37: 136-147.
40. Ross-Innes CS, Stark R, Teschendorff AE, Holmes KA, Ali HR, Dunning MJ, Brown GD, Gojis O, Ellis IO, Green AR, et al. 2012. Differential oestrogen receptor binding is associated with clinical outcome in breast cancer. Nature 481: 389-393.
41. Round EK, Flowers SK, Richards EJ. 1997. Arabidopsis thaliana centromere regions: genetic map positions and repetitive DNA structure. Genome Res 7: 1045-1053.
42. Sanei M, Pickering R, Kumke K, Nasuda S, Houben A. 2011. Loss of centromeric histone H3 (CENH3) from centromeres precedes uniparental chromosome elimination in interspecific barley hybrids. Proc Natl Acad Sci 108: 498-505.
43. Schneider KL, Xie Z, Wolfgruber TK, Presting GG. 2016. Inbreeding drives maize centromere evolution. Proc Natl Acad Sci 113: E987-E996.
44. Schubert V, Berr A, Meister A. 2012. Interphase chromatin organisation in Arabidopsis nuclei: constraints versus randomness. Chromosoma 121: 369-387.
45. Schueler MG, Higgins AW, Rudd MK, Gustashaw K, Willard HF. 2001. Genomic and genetic definition of a functional human centromere. Science 294: 109-115.
46. Schueler MG, Swanson W, Thomas PJ, Green ED. 2010. Adaptive evolution of foundation kinetochore proteins in primates. Mol Biol Evol 27: 1585-1597.
47. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, et al. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7: 539.
48. Smith GP. 1976. Evolution of repeated DNA sequences by unequal crossover. Science 191: 528-535.
49. Talbert PB, Masuelli R, Tyagi AP, Comai L, Henikoff S. 2002. Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell 14: 1053-1066.
50. Talbert PB, Bryson TD, Henikoff S. 2004. Adaptive evolution of centromere proteins in plants and animals. J Biol 3: 18.
51. Tek AL, Kashihara K, Murata M, Nagaki K. 2010. Functional centromeres in soybean include two distinct tandem repeats and a retrotransposon. Chromosome Res 18: 337-347.
52. Wieland G, Orthaus S, Ohndorf S, Diekmann S, Hemmerich P. 2004. Functional complementation of human centromere protein A (CENPA) by Cse4p from Saccharomyces cerevisiae. Mol Cell Biol 24: 6620-6630.
53. Wolfgruber TK, Sharma A, Schneider KL, Albert PS, Koo DH, Shi J, Gao Z, Han F, Lee H, Xu R, et al. 2009. Maize centromere structure and evolution: Sequence analysis of centromeres 2 and 5 reveals dynamic loci shaped primarily by retrotransposons. PLoS Genet 5: e1000743.
54. Zhang W, Lee HR, Koo DH, Jiang J. 2008a. Epigenetic modification of centromeric chromatin: hypomethylation of DNA sequences in the CENH3-associated chromatin in Arabidopsis thaliana and maize. Plant Cell 20: 25-34.
55. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, et al. 2008b. Model-based analysis of ChIP-Seq (MACS). Genome Biol 9: R137.
56. Zhong CX, Marshall JB, Topp C, Mroczek R, Kato A, Nagaki K, Birchler JA, Jiang J, Dawe RK. 2002. Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell 14: 2825-2836.
57. Zhou C, Zhang L, Duan J, Miki B,WuK. 2005. HISTONE DEACETYLASE19 is involved in jasmonic acid and ethylene signaling of pathogen response in Arabidopsis. Plant Cell 17: 1196-1204.