Centromere Size and Its Relationship to Haploid Formation in Plants

Molecular Plant

Volumn 11, Issue 3, 2018, Pages 398-406

  Wang, Na ^a   Dawe, R Kelly ^a,b  

^a UNIVERSITY OF GEORGIA   (United States)

^b NONE   (United States)

Author keywords

aneuploidy; CENH3; CENP A; chromosome loss; genome elimination; kinetochore

Indexed keywords

PLANT PROTEIN;

CENTROMERE; GENETICS; HAPLOIDY; KINETOCHORE; METABOLISM; PLANT GENOME;

CENTROMERE; GENOME, PLANT; HAPLOIDY; KINETOCHORES; PLANT PROTEINS;

EID: 85042003087     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1016/j.molp.2017.12.009     Document Type: Review

References (106)

1. Akera, T., Chmatal, L., Trimm, E., Yang, K., Aonbangkhen, C., Chenoweth, D.M., Janke, C., Schultz, R.M., Lampson, M.A., Spindle asymmetry drives non-Mendelian chromosome segregation. Science 358 (2017), 668–672.
2. Allshire, R.C., Karpen, G.H., Epigenetic regulation of centromeric chromatin: old dogs, new tricks?. Nat. Rev. Genet. 9 (2008), 923–937.
3. Batzenschlager, M., Masoud, K., Janski, N., Houlne, G., Herzog, E., Evrard, J.L., Baumberger, N., Erhardt, M., Nomine, Y., Kieffer, B., et al. The GIP gamma-tubulin complex-associated proteins are involved in nuclear architecture in Arabidopsis thaliana. Front. Plant Sci., 4, 2013, 480.
4. Batzenschlager, M., Lermontova, I., Schubert, V., Fuchs, J., Berr, A., Koini, M.A., Houlne, G., Herzog, E., Rutten, T., Alioua, A., et al. Arabidopsis MZT1 homologs GIP1 and GIP2 are essential for centromere architecture. Proc. Natl. Acad. Sci. USA 112 (2015), 8656–8660.
5. Bennett, M.D., Smith, J.B., Ward, J., Jenkins, G., The relationship between nuclear DNA content and centromere volume in higher plants. J. Cell Sci. 47 (1981), 91–115.
6. Birchler, J., Gao, Z., Sharma, A., Presting, G., Han, F., Epigenetic aspects of centromere function in plants. Curr. Opin. Plant Biol. 14 (2011), 217–222.
7. Black, B.E., Foltz, D.R., Chakravarthy, S., Luger, K., Woods, V.L., Cleveland, D.W., Structural determinants for generating centromeric chromatin. Nature 430 (2004), 578–582.
8. Bodor, D.L., Mata, J.F., Sergeev, M., David, A.F., Salimian, K.J., Panchenko, T., Cleveland, D.W., Black, B.E., Shah, J.V., Jansen, L.E., The quantitative architecture of centromeric chromatin. Elife, 3, 2014, e02137.
9. Britt, A.B., Kuppu, S., Cenh3: an emerging player in haploid induction technology. Front. Plant Sci., 7, 2016, 357.
10. Buchwitz, B., Ahmad, K., Moore, L., Roth, M., Henikoff, S., Cell division - a histone-H3-like protein in C. elegans. Nature 401 (1999), 547–548.
11. Callimassia, M.A., Murray, B.G., Hammett, K.R., Bennett, M.D., Parental genome separation and asynchronous centromere division in interspecific F1 hybrids in Lathyrus. Chromosome Res. 2 (1994), 383–397.
12. Cheeseman, I.M., Chappie, J.S., Wilson-Kubalek, E.M., Desai, A., The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127 (2006), 983–997.
13. Collins, K., Furuyama, S., Biggins, S., Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A histone H3 variant. Curr. Biol. 14 (2004), 1968–1972.
14. Dawe, R.K., Reed, L.M., Yu, H.-G., Muszynski, M.G., Hiatt, E.N., A maize homolog of mammalian CENPC is a constitutive component of the inner kinetochore. Plant Cell 11 (1999), 1227–1238.
15. De Rop, V., Padeganeh, A., Maddox, P.S., CENP-A: the key player behind centromere identity, propagation, and kinetochore assembly. Chromosoma 121 (2012), 527–538.
16. De Storme, N., Keceli, B.N., Zamariola, L., Angenon, G., Geelen, D., CENH3-GFP: a visual marker for gametophytic and somatic ploidy determination in Arabidopsis thaliana. BMC Plant Biol., 16, 2016, 1.
17. Deyter, G., Biggins, S., The FACT complex interacts with the E3 ubiquitin ligase Psh1 to prevent ectopic localization of CENP-A. Genes Dev. 28 (2014), 1815–1826.
18. Deyter, G., Hildebrand, E., Barber, A., Biggins, S., Histone H4 facilitates the proteolysis of the budding yeast CENP-A(Cse4) centromeric histone variant. Genetics, 205, 2017, 113.
19. Drinnenberg, I.A., deYoung, D., Henikoff, S., Malik, H.S., Recurrent loss of CenH3 is associated with independent transitions to holocentricity in insects. Elife, 3, 2014, 03676.
20. Du, Y., Dawe, R.K., Maize NDC80 is a constitutive feature of the central kinetochore. Chromosome Res. 15 (2007), 767–775.
21. Du, Y.Q., Topp, C.N., Dawe, R.K., DNA binding of centromere protein C (CENPC) is stabilized by single-stranded RNA. PLoS Genet., 6, 2010, e1000835.
22. Dunleavy, E.M., Roche, D., Tagami, H., Lacoste, N., Ray-Gallet, D., Nakamura, Y., Daigo, Y., Nakatani, Y., Almouzni-Pettinotti, G., HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137 (2009), 485–497.
23. Fletcher, H.L., The radial positions of metaphase chromosomes may be a consequence of the relative strength of their interaction with the spindle and their size. Chromosome Res. 2 (1994), 21–24.
24. Foltz, D.R., Jansen, L.E., Bailey, A.O., Yates, J.R. 3rd, Bassett, E.A., Wood, S., Black, B.E., Cleveland, D.W., Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell 137 (2009), 472–484.
25. French, B.T., Westhorpe, F.G., Limouse, C., Straight, A.F., Xenopus laevis M18BP1 directly binds existing CENP-A nucleosomes to promote centromeric chromatin assembly. Dev. Cell, 42, 2017, 190.
26. Fu, S., Lv, Z., Gao, Z., Wu, H., Pang, J., Zhang, B., Dong, Q., Guo, X., Wang, X., Birchler, J., et al. De novo centromere formation on a chromosome fragment in maize. Proc. Natl. Acad. Sci. USA 110 (2013), 6033–6036.
27. Galli, M., Morgan, D., Cell size determines the strength of the spindle assembly checkpoint during embryonic development. Dev. Cell 36 (2016), 344–352.
28. Gao, D.Y., Gill, N., Kim, H.R., Walling, J.G., Zhang, W.L., Fan, C.Z., Yu, Y.S., Ma, J.X., SanMiguel, P., Jiang, N., et al. A lineage-specific centromere retrotransposon in Oryza brachyantha. Plant J. 60 (2009), 820–831.
29. Gascoigne, K.E., Takeuchi, K., Suzuki, A., Hori, T., Fukagawa, T., Cheeseman, I.M., Induced ectopic kinetochore assembly bypasses the requirement for CENP-aA nucleosomes. Cell 145 (2011), 410–422.
30. Gent, J.I., Wang, K., Jiang, J.M., Dawe, R.K., Stable patterns of CENH3 occupancy through maize lineages containing genetically similar centromeres. Genetics 200 (2015), 1105–1116.
31. Gent, J.I., Wang, N., Dawe, R.K., Stable centromere positioning in diverse sequence contexts of complex and satellite centromeres of maize and wild relatives. Genome Biol., 18, 2017, 121.
32. Gilles, L.M., Khaled, A., Laffaire, J.B., Chaignon, S., Gendrot, G., Laplaige, J., Berges, H., Beydon, G., Bayle, V., Barret, P., et al. Loss of pollen-specific phospholipase NOT LIKE DAD triggers gynogenesis in maize. EMBO J. 36 (2017), 707–717.
33. Gong, Z.Y., Wu, Y.F., Koblizkova, A., Torres, G.A., Wang, K., Iovene, M., Neumann, P., Zhang, W.L., Novak, P., Buell, C.R., et al. Repeatless and repeat-based centromeres in potato: implications for centromere evolution. Plant Cell 24 (2012), 3559–3574.
34. Gopalakrishnan, S., Sullivan, B., Trazzi, S., Della Valle, G., Robertson, K., DNMT3B interacts with constitutive centromere protein CENP-C to modulate DNA methylation and the histone code at centromeric regions. Hum. Mol. Genet. 18 (2009), 3178–3193.
35. Heckmann, S., Macas, J., Kumke, K., Fuchs, J., Schubert, V., Ma, L., Novak, P., Neumann, P., Taudien, S., Platzer, M., et al. The holocentric species Luzula elegans shows interplay between centromere and large-scale genome organization. Plant J. 73 (2013), 555–565.
36. Henikoff, S., Ahmad, K., Malik, H.S., The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293 (2001), 1098–1102.
37. Heun, P., Erhardt, S., Blower, M.D., Weiss, S., Skora, A.D., Karpen, G.H., Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev. Cell 10 (2006), 303–315.
38. Hori, T., Shang, W., Hara, M., Ariyoshi, M., Arimura, Y., Fujita, R., Kurumizaka, H., Fukagawa, T., Association of M18BP1/KNL2 with CENP-A nucleosome is essential for centromere formation in non-mammalian vertebrates. Dev. Cell, 42, 2017, 181.
39. Howman, E.V., Fowler, K.J., Newson, A.J., Redward, S., MacDonald, A.C., Kalitsis, P., Choo, K.H.A., Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. Proc. Natl. Acad. Sci. USA 97 (2000), 1148–1153.
40. Ingouff, M., Rademacher, S., Holec, S., Soljic, L., Xin, N., Readshaw, A., Foo, S.H., Lahouze, B., Sprunck, S., Berger, F., Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr. Biol. 20 (2010), 2137–2143.
41. Ishii, T., Karimi-Ashtiyani, R., Houben, A., Haploidization via chromosome elimination: means and mechanisms. Annu. Rev. Plant Biol. 67 (2016), 421–438.
42. Izuta, H., Ikeno, M., Suzuki, N., Tomonaga, T., Nozaki, N., Obuse, C., Kisu, Y., Goshima, N., Nomura, F., Nomura, N., et al. Comprehensive analysis of the ICEN (Interphase Centromere Complex) components enriched in the CENP-A chromatin of human cells. Genes Cells 11 (2006), 673–684.
43. Jansen, L.E.T., Black, B.E., Foltz, D.R., Cleveland, D.W., Propagation of centromeric chromatin requires exit from mitosis. J. Cell Biol. 176 (2007), 795–805.
44. Jiang, J., Birchler, J.A., Parrott, W.A., Dawe, R.K., A molecular view of plant centromeres. Trends Plant Sci. 8 (2003), 570–575.
45. Karimi-Ashtiyani, R., Ishii, T., Niessen, M., Stein, N., Heckmann, S., Gurushidze, M., Banaei-Moghaddam, A.M., Fuchs, J., Schubert, V., Koch, K., et al. Point mutation impairs centromeric CENH3 loading and induces haploid plants. Proc. Natl. Acad. Sci. USA 112 (2015), 11211–11216.
46. Kasha, K.J., Kao, K.N., High frequency haploid production in barley (Hordeum vulgare L.). Nature 225 (1970), 874–876.
47. Kelliher, T., Starr, D., Richbourg, L., Chintamanani, S., Delzer, B., Nuccio, M.L., Green, J., Chen, Z., McCuiston, J., Wang, W., et al. MATRILINEAL, a sperm-specific phospholipase, triggers maize haploid induction. Nature 542 (2017), 105–109.
48. Klare, K., Weir, J., Basilico, F., Zimniak, T., Massimiliano, L., Ludwigs, N., Herzog, F., Musacchio, A., CENP-C is a blueprint for constitutive centromere-associated network assembly within human kinetochores. J. Cell Biol. 210 (2015), 11–22.
49. Komaki, S., Schnittger, A., The spindle checkpoint in plants - a green variation over a conserved theme?. Curr. Opin. Plant Biol. 34 (2016), 84–91.
50. Kuppu, S., Tan, E., Nguyen, H., Rodgers, A., Comai, L., Chan, S., Britt, A., Point mutations in centromeric histone induce post-zygotic incompatibility and uniparental inheritance. PLoS Genet., 11, 2015, e1005494.
51. Kynast, R.G., Riera-Lizarazu, O., Vales, M.I., Okagaki, R.J., Maquieira, S.B., Chen, G., Ananiev, E.V., Odland, W.E., Russell, C.D., Stec, A.O., et al. A complete set of maize individual chromosome additions to the oat genome. Plant Physiol. 125 (2001), 1216–1227.
52. Lacoste, N., Woolfe, A., Tachiwana, H., Garea, A.V., Barth, T., Cantaloube, S., Kurumizaka, H., Imhof, A., Almouzni, G., Mislocalization of the centromeric histone variant CenH3/CENP-A in human cells depends on the chaperone DAXX. Mol. Cell 53 (2014), 631–644.
53. Laurie, D.A., The frequency of fertilization in wheat X pearl-millet crosses. Genome 32 (1989), 1063–1067.
54. Lee, H.R., Zhang, W.L., Langdon, T., Jin, W.W., Yan, H.H., Cheng, Z.K., Jiang, J.M., Chromatin immunoprecipitation cloning reveals rapid evolutionary patterns of centromeric DNA in Oryza species. Proc. Natl. Acad. Sci. USA 102 (2005), 11793–11798.
55. Lermontova, I., Schubert, V., Fuchs, J., Klatte, S., Macas, J., Schubert, I., Loading of Arabidopsis centromeric histone CENH3 occurs mainly during G2 and requires the presence of the histone fold domain. Plant Cell 18 (2006), 2443–2451.
56. Lermontova, I., Fuchs, J., Schubert, V., Schubert, I., Loading time of the centromeric histone H3 variant differs between plants and animals. Chromosoma 116 (2007), 507–510.
57. Lermontova, I., Koroleva, O., Rutten, T., Fuchs, J., Schubert, V., Moraes, I., Koszegi, D., Schubert, I., Knockdown of CENH3 in Arabidopsis reduces mitotic divisions and causes sterility by disturbed meiotic chromosome segregation. Plant J. 68 (2011), 40–50.
58. Lermontova, I., Rutten, T., Schubert, I., Deposition, turnover, and release of CENH3 at Arabidopsis centromeres. Chromosoma 120 (2011), 633–640.
59. Lermontova, I., Kuhlmann, M., Friedel, S., Rutten, T., Heckmann, S., Sandmann, M., Demidov, D., Schubert, V., Schubert, I., Arabidopsis kinetochore null2 is an upstream component for centromeric histone H3 variant cenH3 deposition at centromeres. Plant Cell 25 (2013), 3389–3404.
60. Li, X., Dawe, R.K., Fused sister kinetochores initiate the reductional division in meiosis I. Nat. Cell Biol. 11 (2009), 1103–1108.
61. Liu, S.T., Rattner, J.B., Jablonski, S.A., Yen, T.J., Mapping the assembly pathways that specify formation of the trilaminar kinetochore plates in human cells. J. Cell Biol. 175 (2006), 41–53.
62. Liu, Y., Su, H., Pang, J., Goo, Z., Wang, X., Birchler, J., Han, F., Sequential de novo centromere formation and inactivation on a chromosomal fragment in maize. Proc. Natl. Acad. Sci. USA 112 (2015), E1263–E1271.
63. Liu, Y.L., Su, H.D., Zhang, J., Liu, Y., Han, F.P., Birchler, J.A., Dynamic epigenetic states of maize centromeres. Front. Plant Sci., 6, 2015, 904.
64. Liu, C., Li, X., Meng, D., Zhong, Y., Chen, C., Dong, X., Xu, X., Chen, B., Li, W., Li, L., et al. A 4-bp insertion at ZmPLA1 encoding a putative phospholipase a generates haploid induction in maize. Mol. Plant 10 (2017), 520–522.
65. Maddox, P., Hyndman, F., Monen, J., Oegema, K., Desai, A., Functional genomics identifies a Myb domain-containing protein family required for assembly of CENP-A chromatin. J. Cell Biol. 176 (2007), 757–763.
66. Maehara, K., Takahashi, K., Saitoh, S., CENP-A reduction induces a p53-dependent cellular senescence response to protect cells from executing defective mitoses. Mol. Cell. Biol. 30 (2010), 2090–2104.
67. Maheshwari, S., Tan, E.H., West, A., Franklin, F.C.H., Comai, L., Chan, S.W.L., Naturally occurring differences in CENH3 affect chromosome segregation in zygotic mitosis of hybrids. PLoS Genet., 11, 2015, e1004970.
68. Mellone, B.G., Grive, K.J., Shteyn, V., Bowers, S.R., Oderberg, I., Karpen, G.H., Assembly of Drosophila centromeric chromatin proteins during mitosis. PLoS Genet., 7, 2011, e1002068.
69. Mizuguchi, G., Xiao, H., Wisniewski, J., Smith, M.M., Wu, C., Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-specific nucleosomes. Cell 129 (2007), 1153–1164.
70. Morey, L., Barnes, K., Chen, Y., Fitzgerald-Hayes, M., Baker, R., The histone fold domain of Cse4 is sufficient for CEN targeting and propagation of active centromeres in budding yeast. Eukaryot. Cell 3 (2004), 1533–1543.
71. Murata, M., Ogura, Y., Motoyoshi, F., Centromeric repetitive sequences in Arabidopsis thaliana. Jpn. J. Genet. 69 (1994), 361–370.
72. Nagaki, K., Murata, M., Characterization of CENH3 and centromere-associated DNA sequences in sugarcane. Chromosome Res. 13 (2005), 195–203.
73. Nagaki, K., Kashihara, K., Murata, M., Visualization of diffuse centromeres with centromere-specific histone H3 in the holocentric plant Luzula nivea. Plant Cell 17 (2005), 1886–1893.
74. Nasuda, S., Hudakova, S., Schubert, I., Houben, A., Endo, T., Stable barley chromosomes without centromeric repeats. Proc. Natl. Acad. Sci. USA 102 (2005), 9842–9847.
75. Neumann, P., Pavlikova, Z., Koblizkova, A., Fukova, I., Jedlickova, V., Novak, P., Macas, J., Centromeres off the hook: massive changes in centromere size and structure following duplication of CenH3 gene in Fabeae species. Mol. Biol. Evol. 32 (2015), 1862–1879.
76. Obuse, C., Yang, H., Nozaki, N., Goto, S.H., Okazaki, T., Yoda, K., Proteomics analysis of the centromere complex from HeLa interphase cells: UV-damaged DNA binding 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 9 (2004), 105–120.
77. Pazy, B., Plitmann, U., Chromosome divergence in the genus Cuscuta and its systematic implications. Caryologia 48 (1995), 173–180.
78. Pearson, C.G., Yeh, E., Gardner, M., Odde, D., Salmon, E.D., Bloom, K., Stable kinetochore-microtubule attachment constrains centromere positioning in metaphase. Curr. Biol. 14 (2004), 1962–1967.
79. Phansalkar, R., Lapierre, P., Mellone, B.G., Evolutionary insights into the role of the essential centromere protein CAL1 in Drosophila. Chromosome Res. 20 (2012), 493–504.
80. Rago, F., Cheeseman, I.M., Review series: the functions and consequences of force at kinetochores. J. Cell Biol. 200 (2013), 557–565.
81. Ranjitkar, P., Press, M., Yi, X., Baker, R., MacCoss, M., Biggins, S., An E3 ubiquitin ligase prevents ectopic localization of the centromeric histone H3 variant via the centromere targeting domain. Mol. Cell 40 (2010), 455–464.
82. Ravi, M., Chan, S.W., Haploid plants produced by centromere-mediated genome elimination. Nature 464 (2010), 615–618.
83. Ravi, M., Shibata, F., Ramahi, J.S., Nagaki, K., Chen, C.B., Murata, M., Chan, S.W.L., Meiosis-specific loading of the centromere-specific histone CENH3 in Arabidopsis thaliana. PLoS Genet., 7, 2011, e1002121.
84. Regnier, V., Vagnarelli, P., Fukagawa, T., Zerjal, T., Burns, E., Trouche, D., Earnshaw, W., Brown, W., CENP-A is required for accurate chromosome segregation and sustained kinetochore association of BubR1. Mol. Cell. Biol. 25 (2005), 3967–3981.
85. RieraLizarazu, O., Rines, H., Phillips, R., Cytological and molecular characterization of oat x maize partial hybrids. Theor. Appl. Genet. 93 (1996), 123–135.
86. Sandmann, M., Talbert, P., Demidov, D., Kuhlmann, M., Rutten, T., Conrad, U., Lermontova, I., Targeting of Arabidopsis KNL2 to centromeres depends on the conserved CENPC-k motif in its C terminus. Plant Cell 29 (2017), 144–155.
87. Sanei, M., Pickering, R., Kumke, K., Nasuda, S., Houben, A., Loss of centromeric histone H3 (CENH3) from centromeres precedes uniparental chromosome elimination in interspecific barley hybrids. Proc. Natl. Acad. Sci. USA 108 (2011), E498–E505.
88. Sato, H., Shibata, F., Murata, M., Characterization of a Mis12 homologue in Arabidopsis thaliana. Chromosome Res. 13 (2005), 827–834.
89. Schuh, M., Lehner, C.F., Heidmann, S., Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr. Biol. 17 (2007), 237–243.
90. Screpanti, E., De Antoni, A., Alushin, G., Petrovic, A., Melis, T., Nogales, E., Musacchio, A., Direct binding of Cenp-C to the Mis12 complex joins the inner and outer kinetochore. Curr. Biol. 21 (2011), 391–398.
91. Sekulic, N., Black, B., Molecular underpinnings of centromere identity and maintenance. Trends Biochem. Sci. 37 (2012), 220–229.
92. Shono, N., Ohzeki, J., Otake, K., Martins, N., Nagase, T., Kimura, H., Larionov, V., Earnshaw, W., Masumoto, H., CENP-C and CENP-I are key connecting factors for kinetochore and CENP-A assembly. J. Cell Sci. 128 (2015), 4572–4587.
93. Stoler, S., Keith, K.C., Curnick, K.E., Fitzgerald-Hayes, M., A mutation in Cse4, an essential gene encoding a novel chromatin-associated protein in yeast, causes chromosome nondisjunction and cell-cycle arrest at mitosis. Genes Dev. 9 (1995), 573–586.
94. Sullivan, K.F., Hechenberger, M., Masri, K., Human Cenp-a contains a histone H3 related histone fold domain that is required for targeting to the centromere. J. Cell Biol. 127 (1994), 581–592.
95. Talbert, P.B., Bryson, T.D., Henikoff, S., Adaptive evolution of centromere proteins in plants and animals. J. Biol., 3, 2004, 18.
96. Topp, C., Okagaki, R., Melo, J., Kynast, R., Phillips, R., Dawe, R., Identification of a maize neocentromere in an oat-maize addition line. Cytogenet. Genome Res. 124 (2009), 228–238.
97. Van Hooser, A.A., Ouspenski, I.I., Gregson, H.C., Starr, D.A., Yen, T.J., Goldberg, M.L., Yokomori, K., Earnshaw, W.C., Sullivan, K.F., Brinkley, B.R., Specification of kinetochore-forming chromatin by the histone H3 variant CENP-A. J. Cell Sci. 114 (2001), 3529–3542.
98. Vermaak, D., Hayden, H.S., Henikoff, S., Centromere targeting element within the histone fold domain of Cid. Mol. Cell. Biol. 22 (2002), 7553–7561.
99. Wang, K., Wu, Y.F., Zhang, W.L., Dawe, R.K., Jiang, J.M., Maize centromeres expand and adopt a uniform size in the genetic background of oat. Genome Res. 24 (2014), 107–116.
100. Warburton, P.E., Cooke, C.A., Bourassa, S., Vafa, O., Sullivan, B.A., Stetten, G., Gimelli, G., Warburton, D., TylerSmith, C., Sullivan, K.F., et al. Immunolocalization of CENP-A suggests a distinct nucleosome structure at the inner kinetochore plate of active centromeres. Curr. Biol. 7 (1997), 901–904.
101. Yan, H.H., Talbert, P.B., Lee, H.R., Jett, J., Henikoff, S., Chen, F., Jiang, J.M., Intergenic locations of rice centromeric chromatin. PLoS Biol. 6 (2008), 2563–2575.
102. Zhang, H., Dawe, R.K., Total centromere size and genome size are strongly correlated in ten grass species. Chromosome Res. 20 (2012), 403–412.
103. Zhang, X., Li, X., Marshall, J., Zhong, C., Dawe, R., Phosphoserines on maize CENTROMERIC HISTONE H3 and histone H3 demarcate the centromere and pericentromere during chromosome segregation. Plant Cell 17 (2005), 572–583.
104. Zhang, B., Lv, Z., Pang, J., Liu, Y., Guo, X., Fu, S., Li, J., Dong, Q., Wu, H., Gao, Z., et al. Formation of a functional maize centromere after loss of centromeric sequences and gain of ectopic sequences. Plant Cell 25 (2013), 1979–1989.
105. Zhang, H.Q., Koblizkova, A., Wang, K., Gong, Z.Y., Oliveira, L., Torres, G.A., Wu, Y.F., Zhang, W.L., Novak, P., Buell, C.R., et al. Boom-bust turnovers of megabase-sized centromeric DNA in Solanum species: rapid evolution of DNA sequences associated with centromeres. Plant Cell 26 (2014), 1436–1447.
106. Zhong, C.X., Marshall, J.B., Topp, C., Mroczek, R., Kato, A., Nagaki, K., Birchler, J.A., Jiang, J.M., Dawe, R.K., Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell 14 (2002), 2825–2836.