CENH3-GFP: A visual marker for gametophytic and somatic ploidy determination in Arabidopsis thaliana

BMC Plant Biology

Volumn 16, Issue 1, 2016, Pages

  De Storme, Nico ^a   Keçeli, Burcu Nur ^a   Zamariola, Linda ^a   Angenon, Geert ^b   Geelen, Danny ^a  

^a GHENT UNIVERSITY   (Belgium)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

Arabidopsis; CENH3; Centromere; Endomitosis; Meiosis; Ploidy analysis

Indexed keywords

ARABIDOPSIS PROTEIN; GENETIC MARKER; GREEN FLUORESCENT PROTEIN; HISTONE;

ARABIDOPSIS; CENTROMERE; FLOWER; GENETIC MARKER; GENETICS; GROWTH, DEVELOPMENT AND AGING; MEIOSIS; PLANT CHROMOSOME; PLANT GAMETOGENESIS; PLOIDY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CENTROMERE; CHROMOSOMES, PLANT; GAMETOGENESIS, PLANT; GENETIC MARKERS; GERM CELLS, PLANT; GREEN FLUORESCENT PROTEINS; HISTONES; MEIOSIS; PLOIDIES;

EID: 84952759942     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-015-0700-5     Document Type: Article

References (67)

1. Pinto DLP, Barros BD, Viccini LF, de Campos JMS, da Silva ML, Otoni WC. Ploidy stability of somatic embryogenesis-derived Passiflora cincinnata Mast. plants as assessed by flow cytometry. Plant Cell Tissue Organ Cult. 2010;103(1):71-9.
2. Mestiri I, Chague V, Tanguy AM, Huneau C, Huteau V, Belcram H, et al. Newly synthesized wheat allohexaploids display progenitor-dependent meiotic stability and aneuploidy but structural genomic additivity. New Phytol. 2010;186(1):86-101.
3. Torres EM, Williams BR, Amon A. Aneuploidy: Cells losing their balance. Genetics. 2008;179(2):737-46.
4. Dawe RK. Meiotic chromosome organization and segregation in plants. Annu Rev Plant Physiol Plant Mol Biol. 1998;49:371-95.
5. Sharma CBSR. Chemically Induced Aneuploidy in Higher-Plants. Mutagenesis. 1990;5(2):105-25.
6. Matzke MA, Mette MF, Kanno T, Matzke AJM. Does the intrinsic instability of aneuploid genomes have a causal role in cancer? Trends Genet. 2003;19(5):253-6.
7. Petronczki M, Siomos MF, Nasmyth K. Un menage a quatre: The molecular biology of chromosome segregation in meiosis. Cell. 2003;112(4):423-40.
8. Henry IM, Dilkes BP, Young K, Watson B, Wu H, Comai L. Aneuploidy and genetic variation in the Arabidopsis thaliana triploid response. Genetics. 2005;170(4):1979-88.
9. De Storme N, Geelen D. The Arabidopsis Mutant jason Produces Unreduced First Division Restitution Male Gametes through a Parallel/Fused Spindle Mechanism in Meiosis II. Plant Physiol. 2011;155(3):1403-15.
10. Cousin A, Heel K, Cowling WA, Nelson AN. An Efficient High-throughput Flow Cytometric Method for Estimating DNA Ploidy Level in Plants. Cytometry Part A. 2009;75A(12):1015-9.
11. Ochatt SJ. Flow cytometry in plant breeding. Cytometry Part A. 2008;73A(7):581-98.
12. Dolezel J, Greilhuber J, Suda J. Estimation of nuclear DNA content in plants using flow cytometry. Nat Protoc. 2007;2(9):2233-44.
13. Mirzaghaderi G. A simple metaphase chromosome preparation from meristematic root tip cells of wheat for karyotyping or in situ hybridization. Afr J Biotechnol. 2010;9(3):314-8.
14. Anamthawat-Jónsson K. Preparation of chromosomes from plant leaf meristems for karyotype analysis and in situ hybridization. Methods Cell Sci. 2003;25:91-5.
15. Busch W, Herrmann RG, Houben A, Martin R. Efficient preparation of plant metaphase spreads. Plant Mol Biol Report. 1996;14(2):149-55.
16. Delaat AMM, Gohde W, Vogelzang MJDC. Determination of Ploidy of Single Plants and Plant Populations by Flow Cytometry. Plant Breed. 1987;99(4):303-7.
17. Dolezel J, Bartos J. Plant DNA flow cytometry and estimation of nuclear genome size. Ann Bot. 2005;95(1):99-110.
18. Ahloowal BS. A Root Tip Squash Technique for Screening Chromosome Number in Lolium. Euphytica. 1965;14(2):170-3.
19. Preeda N, Yanagi T, Sone K, Taketa S, Okuda N. Chromosome observation method at metaphase and pro-metaphase stages in diploid and octoploid strawberries. Sci Hortic. 2007;114(2):133-7.
20. Jiang JM, Gill BS. Current status and the future of fluorescence in situ hybridization (FISH) in plant genome research. Genome. 2006;49(9):1057-68.
21. Hizume M, Shibata F, Matsusaki Y, Garajova Z. Chromosome identification and comparative karyotypic analyses of four Pinus species. Theor Appl Genet. 2002;105(4):491-7.
22. Murata M, HeslopHarrison JS, Motoyoshi F. Physical mapping of the 5S ribosomal RNA genes in Arabidopsis thaliana by multi-color fluorescence in situ hybridization with cosmid clones. Plant J. 1997;12(1):31-7.
23. Weiss H, Maluszynska J. Molecular cytogenetic analysis of polyploidization in the anther tapetum of diploid and autotetraploid Arabidopsis thaliana plants. Ann Bot. 2001;87(6):729-35.
24. Kim JS, Childs KL, Islam-Faridi MN, Menz MA, Klein RR, Klein PE, et al. Integrated karyotyping of sorghum by in situ hybridization of landed BACs. Genome. 2002;45(2):402-12.
25. Sadder MT, Weber G. Karyotype of maize (Zea mays L.) mitotic metaphase chromosomes as revealed by fluorescence in situ hybridization (FISH) with cytogenetic DNA markers. Plant Mol Biol Report. 2001;19(2):117-23.
26. Armstrong SJ, Jones GH. Meiotic cytology and chromosome behaviour in wild-type Arabidopsis thaliana. J Exp Bot. 2003;54(380):1-10.
27. Maluszynska J, Heslop-Harrison JS. Localization of Tandemly Repeated DNA-Sequences in Arabidopsis thaliana. Plant J. 1991;1(2):159-66.
28. Schubert V, Klatte M, Pecinka A, Meister A, Jasencakova Z, Schubert I. Sister chromatids are often incompletely aligned in meristematic and endopolyploid interphase nuclei of Arabidopsis thaliana. Genetics. 2006;172(1):467-75.
29. Houben A, Schubert I. DNA and proteins of plant centromeres. Curr Opin Plant Biol. 2003;6(6):554-60.
30. Talbert PB, Masuelli R, Tyagi AP, Comai L, Henikoff S. Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell. 2002;14(5):1053-66.
31. ten Hoopen R, Schleker T, Manteuffel R, Schubert I. Transient CENP-E-like kinetochore proteins in plants. Chromosom Res. 2002;10(7):561-70.
32. Du YQ, Topp CN, Dawe RK. DNA Binding of Centromere Protein C (CENPC) Is Stabilized by Single-Stranded RNA. Plos Genetics. 2010;6(2):e1000835.
33. 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(10):2443-51.
34. Shibata F, Murata M. Differential localization of the centromere-specific proteins in the major centromeric satellite of Arabidopsis thaliana. J Cell Sci. 2004;117(14):2963-70.
35. Earnshaw WC, Ratrie H, Stetten G. Visualization of Centromere Proteins Cenp-B and Cenp-C on a Stable Dicentric Chromosome in Cytological Spreads. Chromosoma. 1989;98(1):1-12.
36. Henikoff S, Ahmad K, Malik HS. The centromere paradox: Stable inheritance with rapidly evolving DNA. Science. 2001;293(5532):1098-102.
37. Nagaki K, Song JQ, Stupar RM, Parokonny AS, Yuan QP, Ouyang S, et al. Molecular and cytological analyses of large tracks of centromeric DNA reveal the structure and evolutionary dynamics of maize centromeres. Genetics. 2003;163(2):759-70.
38. Cheng ZK, Dong FG, Langdon T, Shu OY, Buell CR, Gu MH, et al. Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell. 2002;14(8):1691-704.
39. Birchler JA, Gao Z, Sharma A, Presting GG, Han FP. Epigenetic aspects of centromere function in plants. Curr Opin Plant Biol. 2011;14(2):217-22.
40. Jiang JM, Nasuda S, Dong FG, Scherrer CW, Woo SS, Wing RA, et al. A conserved repetitive DNA element located in the centromeres of cereal chromosomes. Proc Natl Acad Sci U S A. 1996;93(24):14210-3.
41. Furuyama S, Biggins S. Centromere identity is specified by a single centromeric nucleosome in budding yeast. Proc Natl Acad Sci U S A. 2007;104(37):14706-11.
42. Okamoto Y, Nakano M, Ohzeki JI, Larionov V, Masumoto H. A minimal CENP-A core is required for nucleation and maintenance of a functional human centromere. Embo J. 2007;26(5):1279-91.
43. Howman EV, Fowler KJ, Newson AJ, Redward S, MacDonald AC, Kalitsis P, et al. Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. Proc Natl Acad Sci U S A. 2000;97(3):1148-53.
44. Samel A, Cuomo A, Bonaldi T, Ehrenhofer-Murray AE. Methylation of CenH3 arginine 37 regulates kinetochore integrity and chromosome segregation. Proc Natl Acad Sci. 2012;109(23):9029-34.
45. Goshima G, Kiyomitsu T, Yoda K, Yanagida M. Human centromere chromatin protein hMis12, essential for equal segregation, is independent of CENP-A loading pathway. J Cell Biol. 2003;160(1):25-39.
46. Ravi M, Kwong PN, Menorca RMG, Valencia JT, Ramahi JS, Stewart JL, et al. The Rapidly Evolving Centromere-Specific Histone Has Stringent Functional Requirements in Arabidopsis thaliana. Genetics. 2010;186(2):461-71.
47. Fang Y, Spector DL. Centromere Positioning and Dynamics in Living Arabidopsis Plants. Mol Biol Cell. 2005;16:5710-8.
48. Erilova A, Brownfield L, Exner V, Rosa M, Twell D, Scheid OM, et al. Imprinting of the Polycomb Group Gene MEDEA Serves as a Ploidy Sensor in Arabidopsis. Plos Genetics. 2009;5(9):e1000663.
49. Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, et al. Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development. 2004;131(3):657-68.
50. Breuninger H, Rikirsch E, Hermann M, Ueda M, Laux T. Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev Cell. 2008;14(6):867-76.
51. De Storme N, De Schrijver J, Van Criekinge W, Wewer V, Dörmann P, Geelen D. GLUCAN SYNTHASE-LIKE8 and STEROL METHYLTRANSFERASE2 Are Required for Ploidy Consistency of the Sexual Reproduction System in Arabidopsis. Plant Cell. 2013;25(2):387-403.
52. Ravi M, Shibata F, Ramahi JS, Nagaki K, Chen CB, Murata M, et al. Meiosis-Specific Loading of the Centromere-Specific Histone CENH3 in Arabidopsis thaliana. Plos Genetics. 2011;7(6):e1002121.
53. Ingouff M, Hamamura Y, GourgueS M, Higashiyama T, Berger F. Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr Biol. 2007;17(12):1032-7.
54. Lermontova I, Koroleva O, Rutten T, Fuchs J, Schubert V, Moraes I, et al. Knockdown of CENH3 in Arabidopsis reduces mitotic divisions and causes sterility by disturbed meiotic chromosome segregation. Plant J. 2011;68(1):40-50.
55. Li JH, Farmer AD, Lindquist IE, Dukowic-Schulze S, Mudge J, Li T, et al. Characterization of a set of novel meiotically-active promoters in Arabidopsis. BMC Plant Biol. 2012;12:104.
56. Wang YX, Magnard JL, McCormick S, Yang M. Progression through meiosis I and meiosis II in Arabidopsis anthers is regulated by an A-type cyclin predominately expressed in prophase I. Plant Physiol. 2004;136(4):4127-35.
57. de Mesa MC, Santiago-Domenech N, Pliego-Alfaro F, Quesada MA, Mercado JA. TheCaMV 35S promoter is highly active on floral organs and pollen of transgenic strawberry plants. Plant Cell Rep. 2004;23(1-2):32-8.
58. Twell D, Klein TM, Fromm ME, Mccormick S. Transient Expression of Chimeric Genes Delivered into Pollen by Microprojectile Bombardment. Plant Physiol. 1989;91(4):1270-4.
59. Wilkinson JE, Twell D, Lindsey K. Activities of CaMV 35S and nos promoters in pollen: Implications for field release of transgenic plants. J Exp Bot. 1997;48(307):265-75.
60. Dutt M, Dhekney SA, Soriano L, Kandel R, Grosser JW. Temporal and spatial control of gene expression in horticultural crops. Horticulture Res. 2014;1:14047.
61. Jin QW, Trelles-Sticken E, Scherthan H, Loidl J. Yeast nuclei display prominent centromere clustering that is reduced in nondividing cells and in meiotic prophase. J Cell Biol. 1998;141(1):21-9.
62. Jin QW, Fuchs J, Loidl J. Centromere clustering is a major determinant of yeast interphase nuclear organization. J Cell Sci. 2000;113(11):1903-12.
63. Fussell CP. The Rabl orientation: a prelude to synapsis. In: Moens PB, editor. Meiosis. Orlando: Academic; 1987. p. 275-99.
64. Nagl W. DNA Endoreduplication and Polyteny Understood as Evolutionary Strategies. Nature. 1976;261(5561):614-5.
65. Sugimoto-Shirasu K, Roberts K. "Big it up": endoreduplication and cell-size control in plants. Curr Opin Plant Biol. 2003;6(6):544-53.
66. Jones GH, Heslop-Harrison J. Classical and molecular cytogenetics of Arabidopsis thaliana. Oxford: Oxford University Press; 1996.
67. Galbraith DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E. Rapid Flow Cytometric Analysis of the Cell Cycle in Intact Plant Tissues. Science. 1983;220(4601):1049-51.