Stretching the Rules: Monocentric Chromosomes with Multiple Centromere Domains
The centromere is a functional chromosome domain that is essential for faithful chromosome segregation during cell division and that can be reliably identified by the presence of the centromere-specific histone H3 variant CenH3. In monocentric chromosomes, the centromere is characterized by a single CenH3-containing region within a morphologically distinct primary constriction. This region usually spans up to a few Mbp composed mainly of centromere-specific satellite DNA common to all chromosomes of a given species. In holocentric chromosomes, there is no primary constriction; the centromere is composed of many CenH3 loci distributed along the entire length of a chromosome. Using correlative fluorescence light microscopy and high-resolution electron microscopy, we show that pea (Pisum sativum) chromosomes exhibit remarkably long primary constrictions that contain 3–5 explicit CenH3-containing regions, a novelty in centromere organization. In addition, we estimate that the size of the chromosome segment delimited by two outermost domains varies between 69 Mbp and 107 Mbp, several factors larger than any known centromere length. These domains are almost entirely composed of repetitive DNA sequences belonging to 13 distinct families of satellite DNA and one family of centromeric retrotransposons, all of which are unevenly distributed among pea chromosomes. We present the centromeres of Pisum as novel “meta-polycentric” functional domains. Our results demonstrate that the organization and DNA composition of functional centromere domains can be far more complex than previously thought, do not require single repetitive elements, and do not require single centromere domains in order to segregate properly. Based on these findings, we propose Pisum as a useful model for investigation of centromere architecture and the still poorly understood role of repetitive DNA in centromere evolution, determination, and function.
Vyšlo v časopise:
Stretching the Rules: Monocentric Chromosomes with Multiple Centromere Domains. PLoS Genet 8(6): e32767. doi:10.1371/journal.pgen.1002777
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002777
Souhrn
The centromere is a functional chromosome domain that is essential for faithful chromosome segregation during cell division and that can be reliably identified by the presence of the centromere-specific histone H3 variant CenH3. In monocentric chromosomes, the centromere is characterized by a single CenH3-containing region within a morphologically distinct primary constriction. This region usually spans up to a few Mbp composed mainly of centromere-specific satellite DNA common to all chromosomes of a given species. In holocentric chromosomes, there is no primary constriction; the centromere is composed of many CenH3 loci distributed along the entire length of a chromosome. Using correlative fluorescence light microscopy and high-resolution electron microscopy, we show that pea (Pisum sativum) chromosomes exhibit remarkably long primary constrictions that contain 3–5 explicit CenH3-containing regions, a novelty in centromere organization. In addition, we estimate that the size of the chromosome segment delimited by two outermost domains varies between 69 Mbp and 107 Mbp, several factors larger than any known centromere length. These domains are almost entirely composed of repetitive DNA sequences belonging to 13 distinct families of satellite DNA and one family of centromeric retrotransposons, all of which are unevenly distributed among pea chromosomes. We present the centromeres of Pisum as novel “meta-polycentric” functional domains. Our results demonstrate that the organization and DNA composition of functional centromere domains can be far more complex than previously thought, do not require single repetitive elements, and do not require single centromere domains in order to segregate properly. Based on these findings, we propose Pisum as a useful model for investigation of centromere architecture and the still poorly understood role of repetitive DNA in centromere evolution, determination, and function.
Zdroje
1. JiangJMBirchlerJAParrottWADaweRK 2003 A molecular view of plant centromeres. Trends Plant Sci 8 570 575
2. MalikHSHenikoffS 2009 Major evolutionary transitions in centromere complexity. Cell 138 1067 1082
3. BlackBEBassettEA 2008 The histone variant CENP-A and centromere specification. Curr Opin Cell Biol 20 91 100
4. SullivanBAKarpenGH 2004 Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin. Nat Struct Mol Biol 11 1076 1083
5. RibeiroSAVagnarelliPDongYHoriTMcEwenBF 2010 A super-resolution map of the vertebrate kinetochore. Proc Natl Acad Sci U S A 107 10484 10489
6. MarshallOJMarshallATChooKH 2008 Three-dimensional localization of CENP-A suggests a complex higher order structure of centromeric chromatin. J Cell Biol 183 1193 1202
7. HeckmannSSchroeder-ReiterEKumkeKMaLNagakiK 2011 Holocentric chromosomes of Luzula elegans are characterized by a longitudinal centromere groove, chromosome bending, and a terminal nucleolus organizer region. Cytogenet Genome Res 134 220 228
8. NagakiKMurataM 2005 Characterization of CENH3 and centromere-associated DNA sequences in sugarcane. Chromosome Res 13 195 203
9. DernburgAF 2001 Here, there, and everywhere: kinetochore function on holocentric chromosomes. J Cell Biol 153 F33 38
10. MacasJNeumannPNavrátilováA 2007 Repetitive DNA in the pea (Pisum sativum L.) genome: comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula. BMC Genomics 8 427 427
11. PlohlMLuchettiAMestrovicNMantovaniB 2008 Satellite DNAs between selfishness and functionality: Structure, genomics and evolution of tandem repeats in centromeric (hetero)chromatin. Gene 409 72 82
12. KawabeANasudaSCharlesworthD 2006 Duplication of centromeric histone H3 (HTR12) gene in Arabidopsis halleri and A. lyrata, plant species with multiple centromeric satellite sequences. Genetics 174 2021 2032
13. MonenJMaddoxPSHyndmanFOegemaKDesaiA 2005 Differential role of CENP-A in the segregation of holocentric C-elegans chromosomes during meiosis and mitosis. Nature Cell Biol 7 1248 1255
14. SaneiMPickeringRKumkeKNasudaSHoubenA 2011 Loss of centromeric histone H3 (CENH3) from centromeres precedes uniparental chromosome elimination in interspecific barley hybrids. Proc Natl Acad Sci U S A 108 E498 505
15. MoraesICLermontovaISchubertI 2011 Recognition of A. thaliana centromeres by heterologous CENH3 requires high similarity to the endogenous protein. Plant Mol Biol 75 253 261
16. MalikHS 2009 The centromere-drive hypothesis: a simple basis for centromere complexity. Prog Mol Subcell Biol 48 33 52
17. BinarovaPHauseBDolezelJDraberP 1998 Association of gamma-tubulin with kinetochore/centromeric region of plant chromosomes. Plant J 14 751 757
18. ten HoopenRManteuffelRDolezelJMalyshevaLSchubertI 2000 Evolutionary conservation of kinetochore protein sequences in plants. Chromosoma 109 482 489
19. PepperDABrinkleyBR 1977 Localization of tubulin in the mitotic apparatus of mammalian cells by immunofluorescence and immunoelectron microscopy. Chromosoma 60 223 235
20. NovákPNeumannPMacasJ 2010 Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinformatics 11 378 378
21. NeumannPNavrátilováAKoblížkováAKejnovskýEHřibováE 2011 Plant centromeric retrotransposons: a structural and cytogenetic perspective. Mob DNA 2 4
22. HallAEKeithKCHallSECopenhaverGPPreussD 2004 The rapidly evolving field of plant centromeres. Current Opin Plant Biol 7 108 114
23. ZhangWFriebeBGillBSJiangJ 2010 Centromere inactivation and epigenetic modifications of a plant chromosome with three functional centromeres. Chromosoma 119 553 563
24. HigginsAWGustashawKMWillardHF 2005 Engineered human dicentric chromosomes show centromere plasticity. Chromosome Res 13 745 762
25. DaweRKHenikoffS 2006 Centromeres put epigenetics in the driver's seat. Trends Biochem Sci 31 662 669
26. McFarlaneRJHumphreyTC 2010 A role for recombination in centromere function. Trends Genet 26 209 213
27. NagakiKKashiharaKMurataM 2005 Visualization of diffuse centromeres with centromere-specific histone H3 in the holocentric plant Luzula nivea. Plant Cell 17 1886 1893
28. BarlowPWNevinD 1976 Quantitative karyology of some species of Luzula. Plant Syst Evol 125 77 86
29. C. elegans Sequencing Consortium 1998 Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282 2012 2018
30. HaizelTLimYKLeitchARMooreG 2005 Molecular analysis of holocentric centromeres of Luzula species. Cytogenet Genome Res 109 134 143
31. LeeHRZhangWLangdonTJinWYanH 2005 Chromatin immunoprecipitation cloning reveals rapid evolutionary patterns of centromeric DNA in Oryza species. Proc Natl Acad Sci U S A 102 11793 11798
32. TalbertPBBayesJJHenikoffS 2009 Evolution of centromeres and kinetochores: A two-part fugue De WulfPEarnshawWC The kinetochore: from molecular discoveries to cancer therapy New York Springer 193 229 editors
33. NeumannPPožárkováDVránaJDoleželJMacasJ 2002 Chromosome sorting and PCR-based physical mapping in pea (Pisum sativum L.). Chromosome Res 10 63 71
34. BennettMDLeitchIJ 1997 Nuclear DNA amounts in angiosperms - 583 new estimates. Ann Botany 80 169 196
35. NeumannPLysákMDoleželJMacasJ 1998 Isolation of chromosomes from Pisum sativum L. hairy root cultures and their analysis by flow cytometry. Plant Sci 137 205 215
36. PruferKStenzelUDannemannMGreenRELachmannM 2008 PatMaN: rapid alignment of short sequences to large databases. Bioinformatics 24 1530 1531
37. Schroeder-ReiterESaneiMHoubenAWannerG 2012 Current SEM techniques for de- and re-construction of centromeres to determine 3D CENH3 distribution in barley mitotic chromosomes. J Microsc 246 96 106
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 6
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