Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots

Autoři: Emily E. Wear aff001;  Jawon Song aff002;  Gregory J. Zynda aff002;  Leigh Mickelson-Young aff001;  Chantal LeBlanc aff003;  Tae-Jin Lee aff001;  David O. Deppong aff001;  George C. Allen aff004;  Robert A. Martienssen aff003;  Matthew W. Vaughn aff002;  Linda Hanley-Bowdoin aff001;  William F. Thompson aff001
Působiště autorů: Department of Plant and Microbial Biology, North Carolina State University, Raleigh, North Carolina, United States of America aff001;  Texas Advanced Computing Center, University of Texas, Austin, Texas, United States of America aff002;  Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, United States of America aff003;  Department of Horticultural Science, North Carolina State University, Raleigh, North Carolina, United States of America aff004
Vyšlo v časopise: Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots. PLoS Genet 16(10): e32767. doi:10.1371/journal.pgen.1008623
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008623


Plant cells undergo two types of cell cycles–the mitotic cycle in which DNA replication is coupled to mitosis, and the endocycle in which DNA replication occurs in the absence of cell division. To investigate DNA replication programs in these two types of cell cycles, we pulse labeled intact root tips of maize (Zea mays) with 5-ethynyl-2’-deoxyuridine (EdU) and used flow sorting of nuclei to examine DNA replication timing (RT) during the transition from a mitotic cycle to an endocycle. Comparison of the sequence-based RT profiles showed that most regions of the maize genome replicate at the same time during S phase in mitotic and endocycling cells, despite the need to replicate twice as much DNA in the endocycle and the fact that endocycling is typically associated with cell differentiation. However, regions collectively corresponding to 2% of the genome displayed significant changes in timing between the two types of cell cycles. The majority of these regions are small with a median size of 135 kb, shift to a later RT in the endocycle, and are enriched for genes expressed in the root tip. We found larger regions that shifted RT in centromeres of seven of the ten maize chromosomes. These regions covered the majority of the previously defined functional centromere, which ranged between 1 and 2 Mb in size in the reference genome. They replicate mainly during mid S phase in mitotic cells but primarily in late S phase of the endocycle. In contrast, the immediately adjacent pericentromere sequences are primarily late replicating in both cell cycles. Analysis of CENH3 enrichment levels in 8C vs 2C nuclei suggested that there is only a partial replacement of CENH3 nucleosomes after endocycle replication is complete. The shift to later replication of centromeres and possible reduction in CENH3 enrichment after endocycle replication is consistent with a hypothesis that centromeres are inactivated when their function is no longer needed.

Klíčová slova:

Cell cycle and cell division – Centromeres – DNA replication – Gene expression – Genomic signal processing – Maize – Plant genomics – Synthesis phase


1. Edgar BA, Zielke N, Gutierrez C. Endocycles: A recurrent evolutionary innovation for post-mitotic cell growth. Nat Rev Mol Cell Biol. 2014;15: 197–210. doi: 10.1038/nrm3756 24556841

2. Lee HO, Davidson JM, Duronio RJ. Endoreplication: Polyploidy with purpose. Genes Dev. 2009;23: 2461–2477. doi: 10.1101/gad.1829209 19884253

3. Fox DT, Duronio RJ. Endoreplication and polyploidy: Insights into development and disease. Development. 2013;140: 3–12. doi: 10.1242/dev.080531 23222436

4. Galbraith DW, Harkins KR, Knapp S. Systemic endopolyploidy in Arabidopsis thaliana. Plant Physiol. 1991;96: 985–989. doi: 10.1104/pp.96.3.985 16668285

5. Joubes J, Chevalier C. Endoreduplication in higher plants. Plant Mol Biol. 2000;43: 735–745. doi: 10.1023/a:1006446417196 11089873

6. Breuer C, Ishida T, Sugimoto K. Developmental control of endocycles and cell growth in plants. Curr Opin Plant Biol. 2010;13: 654–660. doi: 10.1016/j.pbi.2010.10.006 21094078

7. Hayashi K, Hasegawa J, Matsunaga S. The boundary of the meristematic and elongation zones in roots: Endoreduplication precedes rapid cell expansion. Sci Rep. 2013;3: 2723. doi: 10.1038/srep02723 24121463

8. Bass HW, Wear EE, Lee TJ, Hoffman GG, Gumber HK, Allen GC, et al. A maize root tip system to study DNA replication programmes in somatic and endocycling nuclei during plant development. J Exp Bot. 2014;65: 2747–2756. doi: 10.1093/jxb/ert470 24449386

9. Baluska F. Nuclear size, DNA content, and chromatin condensation are different in individual tissues of the maize root apex. Protoplasma. 1990;158: 45–52.

10. Alarcón MV, Salguero J. Transition zone cells reach G2 phase before initiating elongation in maize root apex. Biology Open. 2017;6: 909–913. doi: 10.1242/bio.025015 28495964

11. Hiratani I, Ryba T, Itoh M, Yokochi T, Schwaiger M, Chang CW, et al. Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol. 2008;6: e245. doi: 10.1371/journal.pbio.0060245 18842067

12. Hansen RS, Thomas S, Sandstrom R, Canfield TK, Thurman RE, Weaver M, et al. Sequencing newly replicated DNA reveals widespread plasticity in human replication timing. P Natl Acad Sci USA. 2010;107: 139–144.

13. Hiratani I, Ryba T, Itoh M, Rathjen J, Kulik M, Papp B, et al. Genome-wide dynamics of replication timing revealed by in vitro models of mouse embryogenesis. Genome Res. 2010;20: 155–169. doi: 10.1101/gr.099796.109 19952138

14. Rivera-Mulia JC, Buckley Q, Sasaki T, Zimmerman J, Didier RA, Nazor K, et al. Dynamic changes in replication timing and gene expression during lineage specification of human pluripotent stem cells. Genome Res. 2015;25: 1091–1103. doi: 10.1101/gr.187989.114 26055160

15. Birnbaum K, Jung JW, Wang JY, Lambert GM, Hirst JA, Galbraith DW, et al. Cell type–specific expression profiling in plants via cell sorting of protoplasts from fluorescent reporter lines. Nat Methods. 2005;2: 615–619. doi: 10.1038/nmeth0805-615 16170893

16. Iyer-Pascuzzi AS, Benfey PN. Fluorescence-activated cell sorting in plant developmental biology. In: Hennig L, Köhler C, editors. Plant Developmental Biology, Methods in Mol Biol. New York: Humana Press; 2010. pp. 313–319.

17. Tanurdzic M, Vaughn MW, Jiang H, Lee TJ, Slotkin RK, Sosinski B, et al. Epigenomic consequences of immortalized plant cell suspension culture. PLoS Biol. 2008;6: 2880–2895. doi: 10.1371/journal.pbio.0060302 19071958

18. Sugiyama M. Historical review of research on plant cell dedifferentiation. J Plant Res. 2015;128: 349–359. doi: 10.1007/s10265-015-0706-y 25725626

19. Wear EE, Song J, Zynda GJ, LeBlanc C, Lee TJ, Mickelson-Young L, et al. Genomic analysis of the DNA replication timing program during mitotic S phase in maize (Zea mays) root tips. Plant Cell. 2017;29: 2126–2149. doi: 10.1105/tpc.17.00037 28842533

20. Wear EE, Concia L, Brooks AM, Markham EA, Lee T-J, Allen GC, et al. Isolation of plant nuclei at defined cell cycle stages using EdU labeling and flow cytometry. In: Caillaud M-C, editor. Plant Cell Division: Methods and Protocols, Methods in Mol Biol. New York: Humana Press; 2016. pp. 69–86.

21. Concia L, Brooks AM, Wheeler E, Zynda GJ, Wear EE, LeBlanc C, et al. Genome-wide analysis of the Arabidopsis replication timing program. Plant Physiol. 2018;176: 2166–2185. doi: 10.1104/pp.17.01537 29301956

22. Bass HW, Hoffman GG, Lee TJ, Wear EE, Joseph SR, Allen GC, et al. Defining multiple, distinct, and shared spatiotemporal patterns of DNA replication and endoreduplication from 3D image analysis of developing maize Zea mays L.) root tip nuclei. Plant Mol Biol. 2015;89: 339–351. doi: 10.1007/s11103-015-0364-4 26394866

23. Savadel SD, Bass HW. Take a look at plant DNA replication: Recent insights and new questions. Plant Signal Behav. 2017;12: e1311437. doi: 10.1080/15592324.2017.1311437 28375043

24. Zynda GJ, Song J, Concia L, Wear EE, Hanley-Bowdoin L, Thompson WF, et al. Repliscan: A tool for classifying replication timing regions. BMC Bioinformatics. 2017;18: 362. doi: 10.1186/s12859-017-1774-x 28784090

25. Pryor A, Faulkner K, Rhoades MM, Peacock WJ. Asynchronous replication of heterochromatin in maize. P Natl Acad Sci USA. 1980;77: 6705–6709.

26. Marchal C, Sima J, Gilbert DM. Control of DNA replication timing in the 3D genome. Nat Rev Mol Cell Biol. 2019;20: 721–737. doi: 10.1038/s41580-019-0162-y 31477886

27. Hua BL, Orr-Weaver TL. DNA replication control during Drosophila development: Insights into the onset of S phase, replication initiation, and fork progression. Genetics. 2017;207: 29–47. doi: 10.1534/genetics.115.186627 28874453

28. Hammond MP, Laird CD. Chromosome structure and DNA replication in nurse and follicle cells of Drosophila melanogaster. Chromosoma. 1985;91: 267–278. doi: 10.1007/BF00328222 3920017

29. Hammond MP, Laird CD. Control of DNA replication and spatial distribution of defined DNA sequences in salivary gland cells of Drosophila melanogaster. Chromosoma. 1985;91: 279–286. doi: 10.1007/BF00328223 3920018

30. Nordman J, Li S, Eng T, Macalpine D, Orr-Weaver TL. Developmental control of the DNA replication and transcription programs. Genome Res. 2011;21: 175–181. doi: 10.1101/gr.114611.110 21177957

31. Hribova E, Holusova K, Travnicek P, Petrovska B, Ponert J, Simkova H, et al. The enigma of progressively partial endoreplication: New insights provided by flow cytometry and next-generation sequencing. Genome Biol Evol. 2016;8: 1996–2005. doi: 10.1093/gbe/evw141 27324917

32. Travnicek P, Certner M, Ponert J, Chumova Z, Jersakova J, Suda J. Diversity in genome size and GC content shows adaptive potential in orchids and is closely linked to partial endoreplication, plant life-history traits and climatic conditions. New Phytol. 2019;224: 1642–1656. doi: 10.1111/nph.15996 31215648

33. Bauer MJ, Birchler JA. Organization of endoreduplicated chromosomes in the endosperm of Zea mays L. Chromosoma. 2006;115: 383–394. doi: 10.1007/s00412-006-0068-2 16741707

34. Jacob Y, Stroud H, Leblanc C, Feng S, Zhuo L, Caro E, et al. Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases. Nature. 2010;466: 987–991. doi: 10.1038/nature09290 20631708

35. Salic A, Mitchison TJ. A chemical method for fast and sensitive detection of DNA synthesis in vivo. P Natl Acad Sci USA. 2008;105: 2415–2420.

36. Mickelson-Young L, Wear E, Mulvaney P, Lee TJ, Szymanski ES, Allen G, et al. A flow cytometric method for estimating S-phase duration in plants. J Exp Bot. 2016;67: 6077–6087. doi: 10.1093/jxb/erw367 27697785

37. Yarosh W, Spradling AC. Incomplete replication generates somatic DNA alterations within Drosophila polytene salivary gland cells. Genes Dev. 2014;28: 1840–1855. doi: 10.1101/gad.245811.114 25128500

38. Peacock WJ, Dennis ES, Rhoades MM, Pryor AJ. Highly repeated DNA sequence limited to knob heterochromatin in maize. P Natl Acad Sci USA. 1981;78: 4490–4494.

39. Ananiev EV, Phillips RL, Rines HW. A knob-associated tandem repeat in maize capable of forming fold-back DNA segments: Are chromosome knobs megatransposons? P Natl Acad Sci USA. 1998;95: 10785–10790.

40. Rivin CJ, Cullis CA, Walbot V. Evaluating quantitative variation in the genome of Zea mays. Genetics. 1986;113: 1009–1019. 3744025

41. Ananiev EV, Phillips RL, Rines HW. Chromosome-specific molecular organization of maize (Zea mays L.) centromeric regions. P Natl Acad Sci USA. 1998;95: 13073–13078.

42. Presting GG, Malysheva L, Fuchs J, Schubert I. A TY3/GYPSY retrotransposon-like sequence localizes to the centromeric regions of cereal chromosomes. Plant J. 1998;16: 721–728. doi: 10.1046/j.1365-313x.1998.00341.x 10069078

43. Miller JT, Dong FG, Jackson SA, Song J, Jiang JM. Retrotransposon-related DNA sequences in the centromeres of grass chromosomes. Genetics. 1998;150: 1615–1623. 9832537

44. Baucom RS, Estill JC, Chaparro C, Upshaw N, Jogi A, Deragon JM, et al. Exceptional diversity, non-random distribution, and rapid evolution of retroelements in the B73 maize genome. PLoS Genet. 2009;5: e1000732. doi: 10.1371/journal.pgen.1000732 19936065

45. Gent JI, Schneider KL, Topp CN, Rodriguez C, Presting GG, Dawe RK. Distinct influences of tandem repeats and retrotransposons on CENH3 nucleosome positioning. Epigenet Chromatin. 2011;4: 3.

46. Jiao Y, Peluso P, Shi J, Liang T, Stitzer MC, Wang B, et al. Improved maize reference genome with single-molecule technologies. Nature. 2017;546: 524–527. doi: 10.1038/nature22971 28605751

47. Anderson SN, Stitzer MC, Brohammer AB, Zhou P, Noshay JM, O'Connor CH, et al. Transposable elements contribute to dynamic genome content in maize. Plant J. 2019;100: 1052–1065. doi: 10.1111/tpj.14489 31381222

48. Zhao PA, Sasaki T, Gilbert DM. High-resolution Repli-seq defines the temporal choreography of initiation, elongation and termination of replication in mammalian cells. Genome Biol. 2020;21: 1–20.

49. Van't Hof J. DNA replication in plants. In: DePamphilis M, editor. DNA replication in eukaryotic cells. New York: Cold Spring Harbor Laboratory Press; 1996. pp. 1005–1014.

50. SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, et al. Nested retrotransposons in the intergenic regions of the maize genome. Science. 1996;274: 765–768. doi: 10.1126/science.274.5288.765 8864112

51. Liu R, Vitte C, Ma J, Mahama AA, Dhliwayo T, Lee M, et al. A GeneTrek analysis of the maize genome. P Natl Acad Sci USA. 2007;104: 11844–11849.

52. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, et al. The B73 maize genome: Complexity, diversity, and dynamics. Science. 2009;326: 1112–1115. doi: 10.1126/science.1178534 19965430

53. Comai L, Maheshwari S, Marimuthu MPA. ​Plant centromeres​. Curr Opin Plant Biol. 2017;36: 158–167. doi: 10.1016/j.pbi.2017.03.003 28411416

54. Fukagawa T, Earnshaw WC. The centromere: Chromatin foundation for the kinetochore machinery. Dev Cell. 2014;30: 497–509.

55. McKinley KL, Cheeseman IM. The molecular basis for centromere identity and function. Nat Rev Mol Cell Biol. 2016;17: 16–29. doi: 10.1038/nrm.2015.5 26601620

56. Gent JI, Nannas NJ, Liu Y, Su H, Zhao H, Gao Z, et al. Genomics of maize centromeres. In: Bennetzen J, Flint-Garcia S, Hirsch C, Tuberosa R, editors. The Maize Genome. Compendium of Plant Genomes. Cham: Springer; 2018. p. 59–80.

57. Gent JI, Wang N, Dawe RK. Stable centromere positioning in diverse sequence contexts of complex and satellite centromeres of maize and wild relatives. Genome Biol. 2017;18. doi: 10.1186/s13059-017-1156-8 28126036

58. Zhong CX, Marshall JB, Topp C, Mroczek R, Kato A, Nagaki K, et al. Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell. 2002;14: 2825–2836. doi: 10.1105/tpc.006106 12417704

59. Presting GG. Centromeric retrotransposons and centromere function. Curr Opin Genet Dev. 2018;49: 79–84. doi: 10.1016/j.gde.2018.03.004 29597064

60. Zhao H, Zhu X, Wang K, Gent JI, Zhang W, Dawe RK, et al. Gene expression and chromatin modifications associated with maize centromeres. G3-Genes Genom Genet. 2015;6: 183–192.

61. Zhang W, Lee HR, Koo DH, Jiang J. Epigenetic modification of centromeric chromatin: Hypomethylation of DNA sequences in the CENH3-associated chromatin in Arabidopsis thaliana and maize. Plant Cell. 2008;20: 25–34. doi: 10.1105/tpc.107.057083 18239133

62. Gent JI, Madzima TF, Bader R, Kent MR, Zhang X, Stam M, et al. Accessible DNA and relative depletion of H3K9me2 at maize loci undergoing RNA-directed DNA methylation. Plant Cell. 2014;26: 4903–4917. doi: 10.1105/tpc.114.130427 25465407

63. Maheshwari S, Tan EH, West A, Franklin FCH, Comai L, Chan SW. Naturally occurring differences in CENH3 affect chromosome segregation in zygotic mitosis of hybrids. PLoS Genet. 2015;11: e1004970. doi: 10.1371/journal.pgen.1004970 25622028

64. Shelby RD, Monier K, Sullivan KF. Chromatin assembly at kinetochores is uncoupled from DNA replication. J Cell Biol. 2000;151: 1113–1118. doi: 10.1083/jcb.151.5.1113 11086012

65. Jansen LE, Black BE, Foltz DR, Cleveland DW. Propagation of centromeric chromatin requires exit from mitosis. J Cell Biol. 2007;176: 795–805. doi: 10.1083/jcb.200701066 17339380

66. Boyarchuk E, Montes de Oca R, Almouzni G. Cell cycle dynamics of histone variants at the centromere, a model for chromosomal landmarks. Curr Opin Cell Biol. 2011;23: 266–276. doi: 10.1016/ 21470840

67. Nagaki K, Kashihara K, Murata M. Visualization of diffuse centromeres with centromere-specific histone H3 in the holocentric plant Luzula nivea. Plant Cell. 2005;17: 1886–1893. doi: 10.1105/tpc.105.032961 15937225

68. 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. 2006;18: 2443–2451. doi: 10.1105/tpc.106.043174 17028205

69. Lermontova I, Fuchs J, Schubert V, Schubert I. Loading time of the centromeric histone H3 variant differs between plants and animals. Chromosoma. 2007;116: 507–510. doi: 10.1007/s00412-007-0122-8 17786463

70. Schubert V, Lermontova I, Schubert I. Loading of the centromeric histone H3 variant during meiosis–how does it differ from mitosis? Chromosoma. 2014;123: 491–497. doi: 10.1007/s00412-014-0466-9 24806806

71. Nechemia-Arbely Y, Miga KH, Shoshani O, Aslanian A, McMahon MA, Lee AY, et al. DNA replication acts as an error correction mechanism to maintain centromere identity by restricting CENP-A to centromeres. Nat Cell Biol. 2019;21: 743–754. doi: 10.1038/s41556-019-0331-4 31160708

72. Sugimoto-Shirasu K, Roberts K. “Big it up”: Endoreduplication and cell-size control in plants. Curr Opin Plant Biol. 2003;6: 544–553. doi: 10.1016/j.pbi.2003.09.009 14611952

73. Bhosale R, Boudolf V, Cuevas F, Lu R, Eekhout T, Hu Z, et al. A spatiotemporal DNA endoploidy map of the Arabidopsis root reveals roles for the endocycle in root development and stress adaptation. The Plant Cell. 2018;30: 2330–2351. doi: 10.1105/tpc.17.00983 30115738

74. Cooper S. Rethinking synchronization of mammalian cells for cell cycle analysis. Cell Mol Life Sci. 2003;60: 1099–1106. doi: 10.1007/s00018-003-2253-2 12861378

75. Phillips RL, Kaeppler SM, Olhoft P. Genetic instability of plant tissue cultures: Breakdown of normal controls. P Natl Acad Sci USA. 1994;91: 5222–5226.

76. Mayshar Y, Ben-David U, Lavon N, Biancotti JC, Yakir B, Clark AT, et al. Identification and classification of chromosomal aberrations in human induced pluripotent stem cells. Cell Stem Cell. 2010;7: 521–531. doi: 10.1016/j.stem.2010.07.017 20887957

77. Laurent LC, Ulitsky I, Slavin I, Tran H, Schork A, Morey R, et al. Dynamic changes in the copy number of pluripotency and cell proliferation genes in human ESCs and iPSCs during reprogramming and time in culture. Cell Stem Cell. 2011;8: 106–118. doi: 10.1016/j.stem.2010.12.003 21211785

78. Armstrong RL, Das S, Hill CA, Duronio RJ, Nordman JT. Rif1 functions in a tissue-specific manner to control replication timing through its PP1-binding motif. Genetics. 2020;215: 75–87. doi: 10.1534/genetics.120.303155 32144132

79. Dimitrova DS, Gilbert DM. The spatial position and replication timing of chromosomal domains are both established in early G1 phase. Molecular Cell. 1999;4: 983–993. doi: 10.1016/s1097-2765(00)80227-0 10635323

80. Frawley LE, Orr-Weaver TL. Polyploidy. Curr Biol. 2015;25: R353–R358. doi: 10.1016/j.cub.2015.03.037 25942544

81. Schwaiger M, Stadler MB, Bell O, Kohler H, Oakeley EJ, Schubeler D. Chromatin state marks cell-type- and gender-specific replication of the Drosophila genome. Genes Dev. 2009;23: 589–601. doi: 10.1101/gad.511809 19270159

82. Ryba T, Hiratani I, Lu J, Itoh M, Kulik M, Zhang J, et al. Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res. 2010;20: 761–770. doi: 10.1101/gr.099655.109 20430782

83. Lubelsky Y, Prinz JA, DeNapoli L, Li YL, Belsky JA, MacAlpine DM. DNA replication and transcription programs respond to the same chromatin cues. Genome Res. 2014;24: 1102–1114. doi: 10.1101/gr.160010.113 24985913

84. Armstrong RL, Penke TJR, Strahl BD, Matera AG, McKay DJ, MacAlpine DM, et al. Chromatin conformation and transcriptional activity are permissive regulators of DNA replication initiation in Drosophila. Genome Res. 2018;28: 1688–1700. doi: 10.1101/gr.239913.118 30279224

85. Massey DJ, Kim D, Brooks KE, Smolka MB, Koren A. Next-generation sequencing enables spatiotemporal resolution of human centromere replication timing. Genes. 2019;10: 269.

86. McCarroll RM, Fangman WL. Time of replication of yeast centromeres and telomeres. Cell. 1988;54: 505–513. doi: 10.1016/0092-8674(88)90072-4 3042152

87. Raghuraman MK, Winzeler EA, Collingwood D, Hunt S, Wodicka L, Conway A, et al. Replication dynamics of the yeast genome. Science. 2001;294: 115–121. doi: 10.1126/science.294.5540.115 11588253

88. Kim SM, Dubey DD, Huberman JA. Early-replicating heterochromatin. Genes Dev. 2003;17: 330–335. doi: 10.1101/gad.1046203 12569122

89. Koren A, Tsai HJ, Tirosh I, Burrack LS, Barkai N, Berman J. Epigenetically-inherited centromere and neocentromere DNA replicates earliest in S-phase. PLoS Genet. 2010;6: e1001068. doi: 10.1371/journal.pgen.1001068 20808889

90. Tenhagen KG, Gilbert DM, Willard HF, Cohen SN. Replication timing of DNA-sequences associated with human centromeres and telomeres. Mol Cell Biol. 1990;10: 6348–6355. doi: 10.1128/mcb.10.12.6348 2247059

91. O'Keefe R, Henderson S, Spector DL. Dynamic organization of DNA replication in mammalian cell nuclei: Spatially and temporally defined replication of chromosome-specific satelite DNA sequences. J Cell Biol. 1992;116.

92. Hultdin M, Gronlund E, Norrback KF, Just T, Taneja K, Roos G. Replication timing of human telomeric DNA and other repetitive sequences analyzed by fluorescence in situ hybridization and flow cytometry. Exp Cell Res. 2001;271: 223–229. doi: 10.1006/excr.2001.5391 11716534

93. Sullivan B, Karpen G. Centromere identity in Drosophila is not determined in vivo by replication timing. J Cell Biol. 2001;154: 683–690. doi: 10.1083/jcb.200103001 11514585

94. Ouspenski II, Van Hooser AA, Brinkley BR. Relevance of histone acetylation and replication timing for deposition of centromeric histone CENP-A. Exp Cell Res. 2003;285: 175–188. doi: 10.1016/s0014-4827(03)00011-9 12706113

95. Shang WH, Hori T, Martins NM, Toyoda A, Misu S, Monma N, et al. Chromosome engineering allows the efficient isolation of vertebrate neocentromeres. Dev Cell. 2013;24: 635–648. doi: 10.1016/j.devcel.2013.02.009 23499358

96. Fuchs J, Strehl S, Brandes A, Schweizer D, Schubert I. Molecular—cytogenetic characterization of the Vicia faba genome—heterochromatin differentiation, replication patterns and sequence localization. Chromosome Res. 1998;6: 219–230. doi: 10.1023/a:1009215802737 9609666

97. Schubert I. Late-replicating satellites: Something for all centromeres? Trends Genet. 1998;14: 385–386. doi: 10.1016/s0168-9525(98)01570-4 9820025

98. Jasencakova Z, Meister A, Schubert I. Chromatin organization and its relation to replication and histone acetylation during the cell cycle in barley. Chromosoma. 2001;110: 83–92. doi: 10.1007/s004120100132 11453558

99. Samaniego R, de la Torre C, de la Espina SMD. Dynamics of replication foci and nuclear matrix during S phase in Allium cepa L. cells. Planta. 2002;215: 195–204. doi: 10.1007/s00425-002-0741-5 12029468

100. Müller CA, Nieduszynski CA. Conservation of replication timing reveals global and local regulation of replication origin activity. Genome Res. 2012;22: 1953–1962. doi: 10.1101/gr.139477.112 22767388

101. Pohl TJ, Brewer BJ, Raghuraman MK. Functional centromeres determine the activation time of pericentric origins of DNA replication in Saccharomyces cerevisiae. PLoS Genet. 2012;8: e1002677. doi: 10.1371/journal.pgen.1002677 22589733

102. Natsume T, Müller CA, Katou Y, Retkute R, Gierliński M, Araki H, et al. Kinetochores coordinate pericentromeric cohesion and early DNA replication by Cdc7-Dbf4 kinase recruitment. Mol Cell. 2013;50: 661–674. doi: 10.1016/j.molcel.2013.05.011 23746350

103. Macheret M, Halazonetis TD. Intragenic origins due to short G1 phases underlie oncogene-induced DNA replication stress. Nature. 2018;555: 112–116. doi: 10.1038/nature25507 29466339

104. Smith OK, Kim R, Fu HQ, Martin MM, Lin CM, Utani K, et al. Distinct epigenetic features of differentiation-regulated replication origins. Epigenet Chromatin. 2016;9: 18.

105. Wheeler E, Brooks AM, Concia L, Vera D, Wear EE, LeBlanc C, et al. Arabidopsis DNA replication initiates in intergenic, AT-rich open chromatin. Plant Physiol. 2020;183: 206–220. doi: 10.1104/pp.19.01520 32205451

106. Albert PS, Gao Z, Danilova TV, Birchler JA. Diversity of chromosomal karyotypes in maize and its relatives. Cytogenet Genome Res. 2010;129: 6–16. doi: 10.1159/000314342 20551613

107. Albert PS, Zhang T, Semrau K, Rouillard J-M, Kao Y-H, Wang C-JR, et al. Whole-chromosome paints in maize reveal rearrangements, nuclear domains, and chromosomal relationships. P Natl Acad Sci USA. 2019;116: 1679–1685.

108. Hemmerich P, Weidtkamp-Peters S, Hoischen C, Schmiedeberg L, Erliandri I, Diekmann S. Dynamics of inner kinetochore assembly and maintenance in living cells. J Cell Biol. 2008;180: 1101–1114. doi: 10.1083/jcb.200710052 18347072

109. Dembinsky D, Woll K, Saleem M, Liu Y, Fu Y, Borsuk LA, et al. Transcriptomic and proteomic analyses of pericycle cells of the maize primary root. Plant Physiol. 2007;145: 575–588. doi: 10.1104/pp.107.106203 17766395

110. Orr-Weaver TL. When bigger is better: The role of polyploidy in organogenesis. Trends Genet. 2015;31: 307–315. doi: 10.1016/j.tig.2015.03.011 25921783

111. del Arco AG, Edgar BA, Erhardt S. In vivo analysis of centromeric proteins reveals a stem cell-specific asymmetry and an essential role in differentiated, non-proliferating cells. Cell Rep. 2018;22: 1982–1993. doi: 10.1016/j.celrep.2018.01.079 29466727

112. Wong CYY, Lee BCH, Yuen KWY. Epigenetic regulation of centromere function. Cell Mol Life Sci. 2020: 1–19.

113. Muller S, Almouzni G. Chromatin dynamics during the cell cycle at centromeres. Nat Rev Genet. 2017;18: 192–208. doi: 10.1038/nrg.2016.157 28138144

114. Zhang XL, Li XX, Marshall JB, Zhong CX, Dawe RK. Phosphoserines on maize centromeric histone H3 and histone H3 demarcate the centromere and pericentromere during chromosome segregation. Plant Cell. 2005;17: 572–583. doi: 10.1105/tpc.104.028522 15659628

115. Demidov D, Heckmann S, Weiss O, Rutten T, Tomastikova ED, Kuhlmann M, et al. Deregulated phosphorylation of CENH3 at Ser65 affects the development of floral meristems in Arabidopsis thaliana. Frontiers in Plant Science. 2019;10. doi: 10.3389/fpls.2019.00010 30766542

116. Niikura Y, Kitagawa R, Ogi H, Abdulle R, Pagala V, Kitagawa K. CENP-A K124 ubiquitylation is required for CENP-A deposition at the centromere. Dev Cell. 2015;32: 589–603. doi: 10.1016/j.devcel.2015.01.024 25727006

117. Bui M, Pitman M, Nuccio A, Roque S, Donlin-Asp PG, Nita-Lazar A, et al. Internal modifications in the CENP-A nucleosome modulate centromeric dynamics. Epigenet Chromatin. 2017;10: 17.

118. Takebayashi S, Dileep V, Ryba T, Dennis JH, Gilbert DM. Chromatin-interaction compartment switch at developmentally regulated chromosomal domains reveals an unusual principle of chromatin folding. P Natl Acad Sci USA. 2012;109: 12574–12579.

119. Heinz KS, Casas-Delucchi CS, Torok T, Cmarko D, Rapp A, Raska I, et al. Peripheral re-localization of constitutive heterochromatin advances its replication timing and impairs maintenance of silencing marks. Nucleic Acids Res. 2018;46: 6112–6128. doi: 10.1093/nar/gky368 29750270

120. McNulty SM, Sullivan LL, Sullivan BA. Human centromeres produce chromosome-specific and array-specific alpha satellite transcripts that are complexed with CENP-A and CENP-C. Dev Cell. 2017;42: 226–240. e226. doi: 10.1016/j.devcel.2017.07.001 28787590

121. Topp CN, Zhong CX, Dawe RK. Centromere-encoded RNAs are integral components of the maize kinetochore. P Natl Acad Sci USA. 2004;101: 15986–15991.

122. Du Y, Topp CN, Dawe RK. DNA binding of centromere protein C (CENPC) is stabilized by single-stranded RNA. PLoS Genet. 2010;6: e1000835. doi: 10.1371/journal.pgen.1000835 20140237

123. Liu Y, Su H, Zhang J, Liu Y, Feng C, Han F. Back-spliced RNA from retrotransposon binds to centromere and regulates centromeric chromatin loops in maize. PLoS biology. 2020;18: e3000582. doi: 10.1371/journal.pbio.3000582 31995554

124. Krishnakumar V, Choi Y, Beck E, Wu Q, Luo A, Sylvester A, et al. A maize database resource that captures tissue-specific and subcellular-localized gene expression, via fluorescent tags and confocal imaging (Maize Cell Genomics Database). Plant Cell Physiol. 2015;56: e12. doi: 10.1093/pcp/pcu178 25432973

125. Dong P, Tu X, Chu PY, Lu P, Zhu N, Grierson D, et al. 3d chromatin architecture of large plant genomes determined by local a/b compartments. Mol Plant. 2017;10: 1497–1509. doi: 10.1016/j.molp.2017.11.005 29175436

126. Sotelo-Silveira M, Chavez Montes RA, Sotelo-Silveira JR, Marsch-Martinez N, de Folter S. Entering the next dimension: Plant genomes in 3d. Trends Plant Sci. 2018;23: 598–612. doi: 10.1016/j.tplants.2018.03.014 29703667

127. Gendrel AV, Lippman Z, Martienssen R, Colot V. Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods. 2005;2: 213–218. doi: 10.1038/nmeth0305-213 16163802

128. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv [Preprint]. arXiv:13033997. 2013 [cited 2020 July 1]. Available from:

129. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and samtools. Bioinformatics. 2009;25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

130. Quinlan AR, Hall IM. Bedtools: A flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26: 841–842. doi: 10.1093/bioinformatics/btq033 20110278

131. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotechnol. 2011;29: 24–26. doi: 10.1038/nbt.1754 21221095

132. Merchant N, Lyons E, Goff S, Vaughn M, Ware D, Micklos D, et al. The iPlant collaborative: Cyberinfrastructure for enabling data to discovery for the life sciences. PLoS Biol. 2016;14: e1002342. doi: 10.1371/journal.pbio.1002342 26752627

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