Centromeres and kinetochores of Brassicaceae

Chromosome Research

Volumn 22, Issue 2, 2014, Pages 135-152

  Lermontova, Inna ^a   Sandmann, Michael ^a   Demidov, Dmitri ^a  

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

Author keywords

cenH3; Centromere; Kinetochore; Spindle assembly checkpoint

Indexed keywords

ARABIDOPSIS PROTEIN; HISTONE; PLANT DNA;

ARABIDOPSIS; CENTROMERE; CHROMOSOME SEGREGATION; CLASSIFICATION; DNA SEQUENCE; GENETIC ENGINEERING; GENETICS; GENOMIC INSTABILITY; MEIOSIS; METABOLISM; MICROTUBULE; MITOSIS; PLANT CHROMOSOME; PLANT GENE; TRANSCRIPTION INITIATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CENTROMERE; CHROMOSOME SEGREGATION; CHROMOSOMES, PLANT; DNA, PLANT; GENES, PLANT; GENETIC ENGINEERING; GENOMIC INSTABILITY; HISTONES; KINETOCHORES; MEIOSIS; MICROTUBULES; MITOSIS; SEQUENCE ANALYSIS, DNA; TRANSCRIPTIONAL ACTIVATION;

EID: 84905091101     PISSN: 09673849     EISSN: 15736849     Source Type: Journal    
DOI: 10.1007/s10577-014-9422-z     Document Type: Review

References (105)

1. Al-Shehbaz IA (2012) A generic and tribal synopsis of the Brassicaceae (Cruciferae). Taxon 61:931-954
2. Arabidopsis Genome I (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796-815
3. Aufsatz W, Mette MF, van der Winden J, Matzke AJ, Matzke M (2002) RNA-directed DNAmethylation in Arabidopsis. Proc Natl Acad Sci U S A 99(Suppl 4):16499-16506
4. Barnhart MC, Kuich PH, Stellfox ME, Ward JA, Bassett EA, Black BE, Foltz DR (2011) HJURP is a CENP-A chromatin assembly factor sufficient to form a functional de novo kinetochore. J Cell Biol 194:229-243
5. Bauwens S, Van Oostveldt P, Engler G, Van Montagu M (1991) Distribution of the rDNA and three classes of highly repetitive DNA in the chromatin of interphase nuclei of Arabidopsis thaliana. Chromosoma 101:41-48
6. Berr A, Pecinka A, Meister A, Kreth G, Fuchs J, Blattner FR, Lysak MA, Schubert I (2006) Chromosome arrangement and nuclear architecture but not centromeric sequences are conserved between Arabidopsis thaliana and Arabidopsis lyrata. Plant J Cell Mol Biol 48:771-783 (Pubitemid 44748255)
7. Black BE, Jansen LE, Maddox PS, Foltz DR, Desai AB, Shah JV, Cleveland DW (2007) Centromere identity maintained by nucleosomes assembled with histone H3 containing the CENP-A targeting domain. Mol Cell 25:309-322 (Pubitemid 46109610)
8. Blower MD, Daigle T, Kaufman T, Karpen GH (2006) Drosophila CENP-A mutations cause a BubR1-dependent early mitotic delay without normal localization of kinetochore components. PLoS Genet 2:e110
9. Brandes A, Thompson H, Dean C, Heslop-Harrison JS (1997) Multiple repetitive DNA sequences in the paracentromeric regions of Arabidopsis thaliana L. Chromosom Res 5:238-246 (Pubitemid 27355051)
10. Burgos-Rivera B, Dawe RK (2012) An Arabidopsis tissue-specific RNAi method for studying genes essential to mitosis. PLoS One 7:e51388
11. Caillaud MC, Paganelli L, Lecomte P, Deslandes L, Quentin M, Pecrix Y, Le Bris M, Marfaing N, Abad P, Favery B (2009) Spindle assembly checkpoint protein dynamics reveal conserved and unsuspected roles in plant cell division. PLoS One 4:e6757
12. Capesius I (1983) Sequence of the cryptic satellite DNA from the plant Sinapis alba. Biochim Biophys Acta 739:276-280
13. Chen Y, Baker RE, Keith KC, Harris K, Stoler S, Fitzgerald-Hayes M (2000) The N terminus of the centromere H3-like protein Cse4p performs an essential function distinct from that of the histone fold domain. Mol Cell Biol 20:7037-7048
14. Cooper JL, Henikoff S (2004) Adaptive evolution of the histone fold domain in centromeric histones. Mol Biol Evol 21:1712-1718 (Pubitemid 39096887)
15. Dawe RK, Reed LM, Yu HG, Muszynski MG, Hiatt EN (1999) A maize homolog of mammalian CENPC is a constitutive component of the inner kinetochore. Plant Cell 11:1227-1238
16. Demidov D, Schubert V, Kumke K, Weiß O, Karimi-Ashtiyani R, Buttlar R, Heckmann S, Waneer G, Dong Q, Han F, Houben A (2014) Anti-phosphorylated histone H2AThr120 - a universal microscopic marker for centromeric chromatin of mono- and holocentric plant species. Cytogenet. Genome Res. doi:10.1159/ 000360018
17. de Oliveira EA, Romeiro NC, Ribeiro Eda S, Santa-Catarina C, Oliveira AE, Silveira V, de Souza Filho GA, Venancio TM, Cruz MA (2012) Structural and functional characterization of the protein kinase Mps1 in Arabidopsis thaliana. PLoS One 7:e45707
18. De Rop V, Padeganeh A, Maddox PS (2012) CENP-A: the key player behind centromere identity, propagation, and kinetochore assembly. Chromosoma 121:527-538
19. Ding D, Muthuswamy S, Meier I (2012) Functional interaction between the Arabidopsis orthologs of spindle assembly checkpoint proteins MAD1 and MAD2 and the nucleoporin NUA. Plant Mol Biol 79:203-216
20. Dong QH, Han FP (2012) Phosphorylation of histone H2A is associated with centromere function and maintenance in meiosis. Plant J 71:800-809
21. Elowe S (2011) Bub1 and BubR1: at the interface between chromosome attachment and the spindle checkpoint. Mol Cell Biol 31:3085-3093
22. Elowe S, Dulla K, Uldschmid A, Li X, Dou Z, Nigg EA (2010) Uncoupling of the spindle-checkpoint and chromosome-congression functions of BubR1. J Cell Sci 123:84-94
23. Fang G (2002) Checkpoint protein BubR1 acts synergistically with Mad2 to inhibit anaphase-promoting complex. Mol Biol Cell 13:755-766
24. Fang Y, Spector DL (2005) Centromere positioning and dynamics in living Arabidopsis plants. Mol Biol Cell 16:5710-5718 (Pubitemid 41752220)
25. Figueroa J, Saffrich R, Ansorge W, Valdivia MM (1998) Microinjection of antibodies to centromere protein CENP-A arrests cells in interphase but does not prevent mitosis. Chromosoma 107:397-405 (Pubitemid 29057532)
26. Fransz P, Armstrong S, Alonso-Blanco C, Fischer TC, Torres-Ruiz RA, Jones G (1998) Cytogenetics for the model system Arabidopsis thaliana. Plant J Cell Mol Biol 13:867-876 (Pubitemid 28178648)
27. 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 (Pubitemid 30353092)
28. Franzke A, Lysak MA, Al-Shehbaz IA, Koch MA, Mummenhoff K (2011) Cabbage family affairs: the evolutionary history of Brassicaceae. Trends Plant Sci 16:108-116
29. Gartenberg M (2009) Heterochromatin and the cohesion of sister chromatids. Chromosom Res Int J Mol Supramol Evol Asp Chromosom Biol 17:229-238
30. Grellet F, Delcasso D, Panabieres F, Delseny M (1986) Organization and evolution of a higher plant alphoid-like satellite DNA sequence. J Mol Biol 187:495-507
31. Hall SE, Kettler G, Preuss D (2003) Centromere satellites from Arabidopsis populations: maintenance of conserved and variable domains. Genome Res 13:195-205 (Pubitemid 36575768)
32. Hallden C, Bryngelsson T, Sall T, Gustafsson M (1987) Distribution and evolution of a tandemly repeated DNA-sequence in the family Brassicaceae. JMol Evol 25:318-323
33. Hallden C, Svensson M, Bryngelsson T, Lind C (1990) Tandemly repeated DNA-sequences in Brassicaceae - a characterization of the sequences in Cochlearia-Officinalis and Isatis-Tinctoria. Hereditas 113:291-295
34. Hauf S (2013) The spindle assembly checkpoint: progress and persistent puzzles. Biochem Soc Trans 41:1755-1760
35. Hayashi T, Fujita Y, Iwasaki O, Adachi Y, Takahashi K, Yanagida M (2004) Mis16 and Mis18 are required for CENP-A loading and histone deacetylation at centromeres. Cell 118:715-729 (Pubitemid 39221731)
36. Heckmann S, Lermontova I, Berckmans B, De Veylder L, Baumlein H, Schubert I (2011) The E2F transcription factor family regulates CENH3 expression in Arabidopsis thaliana. Plant J Cell Mol Biol 68:646-656
37. Hemmerich P, Weidtkamp-Peters S, Hoischen C, Schmiedeberg L, Erliandri I, Diekmann S (2008) Dynamics of inner kinetochore assembly and maintenance in living cells. J Cell Biol 180:1101-1114 (Pubitemid 351468468)
38. 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
39. Houben A, Mette MF, Teo CH, Lermontova I, Schubert I (2013) Engineered plant minichromosomes. Int J Dev Biol 57:651-657
40. Howman EV, Fowler KJ, Newson AJ, Redward S, MacDonald AC, Kalitsis P, Choo KH (2000) Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. Proc Natl Acad Sci U S A 97:1148-1153 (Pubitemid 30080827)
41. Hoyt MA, Totis L, Roberts BT (1991) S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 66:507-517 (Pubitemid 121001387)
42. Hu TT, Pattyn P, Bakker EG, Cao J, Cheng JF, Clark RM, Fahlgren N, Fawcett JA, Grimwood J, Gundlach H, Haberer G, Hollister JD, Ossowski S, Ottilar RP, Salamov AA, Schneeberger K, Spannagl M, Wang X, Yang L, Nasrallah ME, Bergelson J, Carrington JC, Gaut BS, Schmutz J, Mayer KF, Van de Peer Y, Grigoriev IV, Nordborg M, Weigel D, Guo YL (2011) The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet 43:476-481
43. Hylander N (1957) Cardaminopsis suecica (Fr.) Hiit., a northern amphidiploid species. Bull Jard Bot Brux 27:591-604
44. Izuta H, Ikeno M, Suzuki N, Tomonaga T, Nozaki N, Obuse C, Kisu Y, Goshima N, Nomura F, Nomura N, Yoda K (2006) Comprehensive analysis of the ICEN(Interphase Centromere Complex) components enriched in the CENP-A chromatin of human cells. Genes Cells 11:673-684
45. Jansen LE, Black BE, Foltz DR, Cleveland DW (2007) Propagation of centromeric chromatin requires exit from mitosis. J Cell Biol 176:795-805 (Pubitemid 46425540)
46. Kamm A, Galasso I, Schmidt T, Heslopharrison JS (1995) Analysis of a repetitive DNA family from Arabidopsis-Arenosa and relationships between Arabidopsis species. Plant Mol Biol 27:853-862
47. Kapusi E, Ma L, Teo CH, Hensel G, Himmelbach A, Schubert I, Mette MF, Kumlehn J, Houben A (2012) Telomere-mediated truncation of barley chromosomes. Chromosoma 121:181-190
48. Kawabe A, Nasuda S (2005) Structure and genomic organization of centromeric repeats in Arabidopsis species. Mol Genet Genomics 272:593-602 (Pubitemid 40379315)
49. Kawabe A, Hansson B, Hagenblad J, Forrest A, Charlesworth D (2006) Centromere locations and associated chromosome rearrangements in Arabidopsis lyrata and A. thaliana. Genetics 173:1613-1619 (Pubitemid 44127662)
50. Kumekawa N, Hosouchi T, Tsuruoka H, Kotani H (2000) The size and sequence organization of the centromeric region of Arabidopsis thaliana chromosome 5. DNA Res 7:315-321
51. Lara-Gonzalez P, Westhorpe FG, Taylor SS (2012) The spindle assembly checkpoint. Curr Biol 22:R966-R980
52. Larsen NA, Al-Bassam J, Wei RR, Harrison SC (2007) Structural analysis of Bub3 interactions in the mitotic spindle checkpoint. Proc Natl Acad Sci U S A 104:1201-1206 (Pubitemid 46183982)
53. Lee SH, Itkin-Ansari P, Levine F (2010) CENP-A, a protein required for chromosome segregation in mitosis, declines with age in islet but not exocrine cells. Aging (Albany NY) 2:785-790
54. Lermontova I, Schubert I (2013) CENH3 for establishing and maintenance of centromeres. In: Jiang J, Birchler JA (eds) Plant centromere biology. Wiley, Oxford, p 210
55. Lermontova I, Schubert V, Fuchs J, Klatte S, Macas J, Schubert I (2006) Loading of Arabidopsis centromeric histone CENH3 occurs mainly during G2 and requires the presence of the histone fold domain. Plant Cell 18:2443-2451 (Pubitemid 44749881)
56. Lermontova I, Fuchs J, Schubert V, Schubert I (2007) Loading time of the centromeric histone H3 variant differs between plants and animals. Chromosoma 116:507-510 (Pubitemid 350120986)
57. Lermontova I, Fuchs J, Schubert I (2008) The Arabidopsis checkpoint protein Bub3.1 is essential for gametophyte development. Front Biosci J Virtual Libr 13:5202-5211 (Pubitemid 351599670)
58. Lermontova I, Koroleva O, Rutten T, Fuchs J, Schubert V, Moraes I, Koszegi D, Schubert I (2011a) Knockdown of CENH3 in Arabidopsis reduces mitotic divisions and causes sterility by disturbed meiotic chromosome segregation. Plant J Cell Mol Biol 68:40-50
59. Lermontova I, Rutten T, Schubert I (2011b) Deposition, turnover, and release of CENH3 at Arabidopsis centromeres. Chromosoma 120:633-640
60. Lermontova I, Kuhlmann M, Friedel S, Rutten T, Heckmann S, Sandmann M, Demidov D, Schubert V, Schubert I (2013) Arabidopsis KINETOCHORE NULL2 is an upstream component for centromeric histone H3 variant cenH3 deposition at centromeres. Plant Cell 25:3389-3404
61. Li R, Murray AW (1991) Feedback control of mitosis in budding yeast. Cell 66:519-531 (Pubitemid 121001388)
62. Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, McCombie WR, Lavine K, Mittal V, May B, Kasschau KD, Carrington JC, Doerge RW, Colot V, Martienssen R (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430:471-476 (Pubitemid 38987911)
63. Lysak MA, Koch MA, Beaulieu JM, Meister A, Leitch IJ (2009) The dynamic ups and downs of genome size evolution in Brassicaceae. Mol Biol Evol 26:85-98
64. Maluszynska J, Heslop-Harrison JS (1991) Localization of tandemly repeated DNA-sequences in Arabidopsis thaliana. Plant J 1:159-166 (Pubitemid 121001057)
65. Martinez-Zapater JM, Estelle MA, Somerville CR (1986) A highly repeated DNA-sequence in Arabidopsis thaliana. Mol Gen Genet 204:417-423
66. May BP, Lippman ZB, Fang Y, Spector DL, Martienssen RA (2005) Differential regulation of strand-specific transcripts from Arabidopsis centromeric satellite repeats. PLoS Genet 1:e79
67. Mendiburo MJ, Padeken J, Fulop S, Schepers A, Heun P (2011) Drosophila CENH3 is sufficient for centromere formation. Science 334:686-690
68. Menges M, Murray JA (2002) Synchronous Arabidopsis suspension cultures for analysis of cell-cycle gene activity. Plant J Cell Mol Biol 30:203-212 (Pubitemid 34536240)
69. Monen J, Maddox PS, Hyndman F, Oegema K, Desai A (2005) Differential role of CENP-A in the segregation of holocentric C. elegans chromosomes during meiosis and mitosis. Nat Cell Biol 7:1248-1255
70. Moraes IC, Lermontova I, Schubert I (2011) Recognition of A. thaliana centromeres by heterologous CENH3 requires high similarity to the endogenous protein. Plant Mol Biol 75:253-261
71. Murata M (2013) Plant centromere biology. Wiley, Oxford
72. Musacchio A, Salmon ED (2007) The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 8:379-393 (Pubitemid 46643240)
73. 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
74. Obuse C, Yang H, Nozaki N, Goto S, Okazaki T, Yoda K (2004) Proteomics analysis of the centromere complex from HeLa interphase cells: UV-damaged DNAbinding protein 1 (DDB-1) is a component of the CEN-complex, while BMI-1 is transiently co-localized with the centromeric region in interphase. Genes Cells Devoted Mol Cell Mech 9:105-120 (Pubitemid 38312955)
75. Ogura Y, Shibata F, Sato H, Murata M (2004) Characterization of a CENP-C homolog in Arabidopsis thaliana. Gene Genet Syst 79:139-144 (Pubitemid 39243764)
76. Pelissier T, Tutois S, Deragon JM, Tourmente S, Genestier S, Picard G (1995) Athila, a new retroelement from Arabidopsis thaliana. Plant Mol Biol 29:441-452 (Pubitemid 3012221)
77. Pelissier T, Tutois S, Tourmente S, Deragon JM, Picard G (1996) DNA regions flanking the major Arabidopsis thaliana satellite are principally enriched in Athila retroelement sequences. Genetica 97:141-151 (Pubitemid 3041869)
78. Phansalkar R, Lapierre P, Mellone BG (2012) Evolutionary insights into the role of the essential centromere protein CAL1 in Drosophila. Chromosom Res Int J Mol Supramol Evol Asp Chromosom Biol 20:493-504
79. Ravi M, Chan SW (2010) Haploid plants produced by centromere-mediated genome elimination. Nature 464:615-618
80. Ravi M, Kwong PN, Menorca RM, Valencia JT, Ramahi JS, Stewart JL, Tran RK, Sundaresan V, Comai L, Chan SW (2010) The rapidly evolving centromere-specific histone has stringent functional requirements in Arabidopsis thaliana. Genetics 186:461-471
81. Ravi M, Shibata F, Ramahi JS, Nagaki K, Chen C, Murata M, Chan SW(2011)Meiosis-specific loading of the centromere-specific histone CENH3 in Arabidopsis thaliana. PLoS Genet 7:e1002121
82. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425
83. Sato H, Shibata F, Murata M (2005) Characterization of a Mis12 homologue in Arabidopsis thaliana. Chromosom Res Int J Mol Supramol Evol Asp Chromosom Biol 13:827-834 (Pubitemid 41768773)
84. Schubert V, Lermontova I, Shubert I (2014) Loading of the centromeric histone H3 variant during meiosis - how does it differ from mitosis? Chromosoma in press
85. Schuh M, Lehner CF, Heidmann S (2007) Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr Biol 17:237-243 (Pubitemid 46186017)
86. Schuyler SC, Wu YF, Kuan VJ (2012) The Mad1-Mad2 balancing act - a damaged spindle checkpoint in chromosome instability and cancer. J Cell Sci 125:4197-4206
87. She W, Grimanelli D, Rutowicz K, Whitehead MW, Puzio M, Kotlinski M, Jerzmanowski A, Baroux C (2013) Chromatin reprogramming during the somatic-to-reproductive cell fate transition in plants. Development 140:4008-4019
88. Shelby RD, Monier K, Sullivan KF (2000) Chromatin assembly at kinetochores is uncoupled from DNA replication. J Cell Biol 151:1113-1118
89. Simoens CR, Gielen J, Van Montagu M, Inze D (1988) Characterization of highly repetitive sequences of Arabidopsis thaliana. Nucleic Acids Res 16:6753-6766
90. Sudakin V, Chan GK, Yen TJ (2001) Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2. J Cell Biol 154:925-936 (Pubitemid 34286173)
91. Suijkerbuijk SJ, van Dam TJ, Karagoz GE, von Castelmur E, Hubner NC, Duarte AM, Vleugel M, Perrakis A, Rudiger SG, Snel B, Kops GJ (2012) The vertebrate mitotic checkpoint protein BUBR1 is an unusual pseudokinase. Dev Cell 22:1321-1329
92. Sullivan KF, Hechenberger M, Masri K (1994) Human CENP-A contains a histone H3 related histone fold domain that is required for targeting to the centromere. J Cell Biol 127:581-592 (Pubitemid 24332958)
93. 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 (Pubitemid 34609216)
94. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739
95. Teo CH, Ma L, Kapusi E, Hensel G, Kumlehn J, Schubert I, Houben A, Mette MF (2011) Induction of telomere-mediated chromosomal truncation and stability of truncated chromosomes in Arabidopsis thaliana. Plant J Cell Mol Biol 68:28-39
96. Teo CH, Lermontova I, Houben A, Mette MF, Schubert I (2013) De novo generation of plant centromeres at tandem repeats. Chromosoma 122:233-241
97. Thompson H, Schmidt R, Brandes A, Heslop-Harrison JS, Dean C (1996) A novel repetitive sequence associated with the centromeric regions of Arabidopsis thaliana chromosomes. Mol Gen Genet 253:247-252 (Pubitemid 26420011)
98. Wang M, Tang D, Luo Q, Jin Y, Shen Y, Wang K, Cheng Z (2012) BRK1, a Bub1-related kinase, is essential for generating proper tension between homologous kinetochores at metaphase I of rice meiosis. Plant Cell 24:4961-4973
99. Weiss E, Winey M (1996) The Saccharomyces cerevisiae spindle pole body duplication gene MPS1 is part of a mitotic checkpoint. J Cell Biol 132:111-123 (Pubitemid 26035079)
100. Wieland G, Orthaus S, Ohndorf S, Diekmann S, Hemmerich P (2004) Functional complementation of human centromere protein A (CENP-A) by Cse4p from Saccharomyces cerevisiae. Mol Cell Biol 24:6620-6630 (Pubitemid 38949852)
101. Williams JS, Hayashi T, Yanagida M, Russell P (2009) Fission yeast Scm3 mediates stable assembly of Cnp1/CENP-A into centromeric chromatin. Mol Cell 33:287-298
102. Yoda K, Ando S, Okuda A, Kikuchi A, Okazaki T (1998) In vitro assembly of the CENP-B/alpha-satellite DNA/core histone complex: CENP-B causes nucleosome positioning. Gene Cells Dev Mol Cell Mech 3:533-548 (Pubitemid 28475323)
103. Zhang W, Lee HR, Koo DH, Jiang J (2008) Epigenetic modification of centromeric chromatin: hypomethylation of DNA sequences in the CENH3-associated chromatin in Arabidopsis thaliana and maize. Plant Cell 20:25-34 (Pubitemid 352844031)
104. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621-2632 (Pubitemid 41071302)
105. Zwick ME, Salstrom JL, Langley CH (1999) Genetic variation in rates of nondisjunction: association of two naturally occurring polymorphisms in the chromokinesin nod with increased rates of nondisjunction in Drosophila melanogaster. Genetics 152:1605-1614 (Pubitemid 29370339)