CenH3 distribution reveals extended centromeres in the model beetle Tribolium castaneum
Autoři:
Tena Gržan aff001; Evelin Despot-Slade aff001; Nevenka Meštrović aff001; Miroslav Plohl aff001; Brankica Mravinac aff001
Působiště autorů:
Division of Molecular Biology, Ruđer Bošković Institute, Zagreb, Croatia
aff001
Vyšlo v časopise:
CenH3 distribution reveals extended centromeres in the model beetle Tribolium castaneum. PLoS Genet 16(10): e32767. doi:10.1371/journal.pgen.1009115
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009115
Souhrn
Centromeres are chromosomal domains essential for kinetochore assembly and correct chromosome segregation. Inconsistent in their underlying DNA sequences, centromeres are defined epigenetically by the presence of the centromere-specific histone H3 variant CenH3. Most of the analyzed eukaryotes have monocentric chromosomes in which CenH3 proteins deposit into a single, primary constriction visible at metaphase chromosomes. Contrary to monocentrics, evolutionary sporadic holocentric chromosomes lack a primary constriction and have kinetochore activity distributed along the entire chromosome length. In this work, we identified cCENH3 protein, the centromeric H3 histone of the coleopteran model beetle Tribolium castaneum. By ChIP-seq analysis we disclosed that cCENH3 chromatin assembles upon a repertoire of repetitive DNAs. cCENH3 in situ mapping revealed unusually elongated T. castaneum centromeres that comprise approximately 40% of the chromosome length. Being the longest insect regional centromeres evidenced so far, T. castaneum centromeres are characterized by metapolycentric structure composed of several individual cCENH3-containing domains. We suggest that the model beetle T. castaneum with its metapolycentromeres could represent an excellent model for further studies of non-canonical centromeres in insects.
Zdroje
1. 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
2. Muller H, Gil J, Drinnenberg IA. The Impact of Centromeres on Spatial Genome Architecture. Trends Genet. 2019;35: 565–578. doi: 10.1016/j.tig.2019.05.003 31200946
3. Plohl M, Meštrović N, Mravinac B. Centromere identity from the DNA point of view. Chromosoma. 2014;123: 313–325. doi: 10.1007/s00412-014-0462-0 24763964
4. Melters DP, Paliulis L V., Korf IF, Chan SWL. Holocentric chromosomes: Convergent evolution, meiotic adaptations, and genomic analysis. Chromosom Res. 2012;20: 579–593. doi: 10.1007/s10577-012-9292-1 22766638
5. Schvarzstein M, Wignall SM, Villeneuve AM. Coordinating cohesion, co-orientation, and congression during meiosis: Lessons from holocentric chromosomes. Genes Dev. 2010;24: 219–228. doi: 10.1101/gad.1863610 20123904
6. Drinnenberg IA, DeYoung D, Henikoff S, Malik HS. Recurrent loss of CenH3 is associated with independent transitions to holocentricity in insects. Elife. 2014;3: e03676. doi: 10.7554/eLife.03676 25247700
7. Neumann P, Navrátilová A, Schroeder-Reiter E, Koblížková A, Steinbauerová V, Chocholová E, et al. Stretching the rules: Monocentric chromosomes with multiple centromere domains. PLoS Genet. 2012;8: e1002777. doi: 10.1371/journal.pgen.1002777 22737088
8. Neumann P, Pavlíková Z, Koblížková A, Fuková I, Jedličková V, Novák P, et al. Centromeres off the hook: Massive changes in centromere size and structure following duplication of cenh3 gene in Fabeae species. Mol Biol Evol. 2015;32: 1862–1879. doi: 10.1093/molbev/msv070 25771197
9. Naughton C, Gilbert N. Centromere chromatin structure—Lessons from neocentromeres. Exp Cell Res. 2020;389: 111899. doi: 10.1016/j.yexcr.2020.111899 32044308
10. Logsdon GA, Gambogi CW, Liskovykh MA, Barrey EJ, Larionov V, Miga KH, et al. Human Artificial Chromosomes that Bypass Centromeric DNA. Cell. 2019;178: 624–639.e19. doi: 10.1016/j.cell.2019.06.006 31348889
11. Gambogi CW, Black BE. The nucleosomes that mark centromere location on chromosomes old and new. Essays Biochem. 2019;63: 15–27. doi: 10.1042/EBC20180060 31015381
12. Earnshaw WC, Rothfield N. Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma. 1985;91: 313–321. doi: 10.1007/BF00328227 2579778
13. Henikoff S, Thakur J, Kasinathan S, Talbert PB. Remarkable Evolutionary Plasticity of Centromeric Chromatin. Cold Spring Harb Symp Quant Biol. 2017;82: 71–82. doi: 10.1101/sqb.2017.82.033605 29196559
14. Malik HS, Henikoff S. Phylogenomics of the nucleosome. Nat Struct Biol. 2003;10: 882–891. doi: 10.1038/nsb996 14583738
15. Akiyoshi B, Gull K. Discovery of unconventional kinetochores in kinetoplastids. Cell. 2014;156: 1247–1258. doi: 10.1016/j.cell.2014.01.049 24582333
16. Navarro-Mendoza MI, Pérez-Arques C, Panchal S, Nicolás FE, Mondo SJ, Ganguly P, et al. Early Diverging Fungus Mucor circinelloides Lacks Centromeric Histone CENP-A and Displays a Mosaic of Point and Regional Centromeres. Curr Biol. 2019;29: 3791–3802.e6. doi: 10.1016/j.cub.2019.09.024 31679929
17. Henikoff S, Ahmad K, Malik HS. The centromere paradox: Stable inheritance with rapidly evolving DNA. Science. 2001;293: 1098–1102. doi: 10.1126/science.1062939 11498581
18. Malik HS. The centromere-drive hypothesis: a simple basis for centromere complexity. Prog Mol Subcell Biol. 2009;48: 33–52. doi: 10.1007/978-3-642-00182-6_2 19521811
19. Sokoloff A. The Biology of Tribolium, With Special Emphasis on Genetic Aspects, Vol. 1. Clarendon Press, Oxford; 1972.
20. Grove SJ, Stork NE. An inordinate fondness for beetles. Invertebr Syst. 2000;14: 733–739.
21. Brown SJ, Shippy TD, Miller S, Bolognesi R, Beeman RW, Lorenzen MD, et al. The red flour beetle, Tribolium castaneum (Coleoptera): A model for studies of development and pest biology. Cold Spring Harb Protoc. 2009;4. doi: 10.1101/pdb.emo126 20147228
22. Adamski Z, Bufo SA, Chowański S, Falabella P, Lubawy J, Marciniak P, et al. Beetles as model organisms in physiological, biomedical and environmental studies—A review. Front Physiol. 2019;10: 1–22. doi: 10.3389/fphys.2019.00001 30723415
23. Richards S, Gibbs RA, Weinstock GM, Brown S, Denell R, Beeman RW, et al. The genome of the model beetle and pest Tribolium castaneum. Nature. 2008;452: 949–955. doi: 10.1038/nature06784 18362917
24. Herndon N, Shelton J, Gerischer L, Ioannidis P, Ninova M, Dönitz J, et al. Enhanced genome assembly and a new official gene set for Tribolium castaneum. BMC Genomics. 2020;21: 47. doi: 10.1186/s12864-019-6394-6 31937263
25. Ugarković D, Podnar M, Plohl M. Satellite DNA of the red flour beetle Tribolium castaneum—Comparative study of satellites from the genus Tribolium. Mol Biol Evol. 1996;13: 1059–1066. doi: 10.1093/oxfordjournals.molbev.a025668 8865660
26. Wang S, Lorenzen MD, Beeman RW, Brown SJ. Analysis of repetitive DNA distribution patterns in the Tribolium castaneum genome. Genome Biol. 2008;9: 1–14. doi: 10.1186/gb-2008-9-3-r61 18366801
27. Brown SJ, Henry JK, Black IV WC, Denell RE. Molecular genetic manipulation of the red flour beetle: Genome organization and cloning of a ribosomal protein gene. Insect Biochem. 1990;20: 185–193. doi: 10.1016/0020-1790(90)90011-I
28. Pavlek M, Gelfand Y, Plohl M, Meštrović N. Genome-wide analysis of tandem repeats in Tribolium castaneum genome reveals abundant and highly dynamic tandem repeat families with satellite DNA features in euchromatic chromosomal arms. DNA Res. 2015;22: 387–401. doi: 10.1093/dnares/dsv021 26428853
29. Khan SA, Eggleston H, Myles KM, Adelman ZN. Differentially and Co-expressed Genes in Embryo, Germ-Line and Somatic Tissues of Tribolium castaneum. G3 Genes|Genomes|Genetics. 2019;9: 2363–2373. doi: 10.1534/g3.119.400340 31113821
30. Stuart JJ, Mocelin G. Cytogenetics of chromosome rearrangements in Tribolium castaneum. Genome. 1995;38: 673–680. doi: 10.1139/g95-085 18470196
31. Novák P, Neumann P, Pech J, Steinhaisl J, MacAs J. RepeatExplorer: A Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics. 2013;29: 792–793. doi: 10.1093/bioinformatics/btt054 23376349
32. Osanai-Futahashi M, Fujiwara H. Coevolution of telomeric repeats and telomeric repeat-specific non-LTR retrotransposons in insects. Mol Biol Evol. 2011;28: 2983–2986. doi: 10.1093/molbev/msr135 21642634
33. Malik HS, Henikoff S. Adaptive evolution of Cid, a centromere-specific histone in Drosophila. Genetics. 2001;157: 1293–1298. 11238413
34. Buchwitz BJ, Ahmad K, Moore LL, Roth MB, Henikoff S. A histone-H3-like protein in C. elegans. Nature. 1999;401: 547–548. doi: 10.1038/44062 10524621
35. Stoler S, Keith KC, Curnick KE, 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. 1995;9: 573–586. doi: 10.1101/gad.9.5.573 7698647
36. Nagaki K, Talbert PB, Zhong CX, Dawe RK, Henikoff S, Jiang J. Chromatin immunoprecipitation reveals that the 180-bp satellite repeat is the key functional DNA element of Arabidopsis thaliana centromeres. Genetics. 2003;163: 1221–1225. 12663558
37. Lam AL, Boivin CD, Bonney CF, Rudd MK, Sullivan BA. Human centromeric chromatin is a dynamic chromosomal domain that can spread over noncentromeric DNA. Proc Natl Acad Sci U S A. 2006;103: 4186–4191. doi: 10.1073/pnas.0507947103 16537506
38. Talbert PB, Sivakanthan K, Henikoff S. Simple and Complex Centromeric Satellites in Drosophila Sibling Species. Genetics. 2018;208: 977–990. doi: 10.1534/genetics.117.300620 29305387
39. Maheshwari S, Ishii T, Brown CT, Houben A, Comai L. Centromere location in Arabidopsis is unaltered by extreme divergence in CENH3 protein sequence. Genome Res. 2017;27: 471–478. doi: 10.1101/gr.214619.116 28223399
40. Henikoff JG, Thakur J, Kasinathan S, Henikoff S. A unique chromatin complex occupies young a-satellite arrays of human centromeres. Sci Adv. 2015;1: 1–12. doi: 10.1126/sciadv.1400234 25927077
41. Vlahović I, Gluncić M, Rosandić M, Ugarković Đ, Paar V. Regular higher order repeat structures in beetle Tribolium castaneum genome. Genome Biol Evol. 2017;9: 2668–2680. doi: 10.1093/gbe/evw174 27492235
42. Hartley G, O’Neill RJ. Centromere repeats: Hidden gems of the genome. Genes (Basel). 2019;10: 223. doi: 10.3390/genes10030223 30884847
43. Chang CH, Chavan A, Palladino J, Wei X, Martins NMC, Santinello B, et al. Islands of retroelements are major components of Drosophila centromeres. PLoS Biol. 2019;17: 1–40. doi: 10.1371/journal.pbio.3000241 31086362
44. de Sotero-Caio CG, Cabral-de-Mello DC, Calixto M da S, Valente GT, Martins C, Loreto V, et al. Centromeric enrichment of LINE-1 retrotransposons and its significance for the chromosome evolution of Phyllostomid bats. Chromosom Res. 2017;25: 313–325. doi: 10.1007/s10577-017-9565-9 28916913
45. Presting GG. Centromeric retrotransposons and centromere function. Curr Opin Genet Dev. 2018;49: 79–84. doi: 10.1016/j.gde.2018.03.004 29597064
46. Yadav V, Sun S, Billmyre RB, Thimmappa BC, Shea T, Lintner R, et al. RNAi is a critical determinant of centromere evolution in closely related fungi. Proc Natl Acad Sci U S A. 2018;115: 3108–3113. doi: 10.1073/pnas.1713725115 29507212
47. Vondrak T, Avila Robledillo L, Novak P, Koblizkova A, Neumann P, Macas J. Characterization of repeat arrays in ultra-long nanopore reads reveals frequent origin of satellite DNA from retrotransposon-derived tandem repeats. Plant J. 2020;101: 484–500. doi: 10.1111/tpj.14546 31559657
48. Bolzán AD. Interstitial telomeric sequences in vertebrate chromosomes: Origin, function, instability and evolution. Mutat Res. 2017;773: 51–65. doi: 10.1016/j.mrrev.2017.04.002 28927537
49. He L, Liu J, Torres GA, Zhang H, Jiang J, Xie C. Interstitial telomeric repeats are enriched in the centromeres of chromosomes in Solanum species. Chromosom Res. 2013;21: 5–13. doi: 10.1007/s10577-012-9332-x 23250588
50. Macas J, Navrátilová A, Mészáros T. Sequence subfamilies of satellite repeats related to rDNA intergenic spacer are differentially amplified on Vicia sativa chromosomes. Chromosoma. 2003;112: 152–158. doi: 10.1007/s00412-003-0255-3 14579131
51. Kumke K, Macas J, Fuchs J, Altschmied L, Kour J, Dhar MK, et al. Plantago lagopus B Chromosome is enriched in 5S rDNA-derived satellite DNA. Cytogenet Genome Res. 2016;148: 68–73. doi: 10.1159/000444873 27173804
52. Vittorazzi SE, Lourenço LB, Del-Grande ML, Recco-Pimentel SM. Satellite DNA derived from 5S rDNA in Physalaemus cuvieri (Anura, Leiuperidae). Cytogenet Genome Res. 2011;134: 101–107. doi: 10.1159/000325540 21464559
53. Yang X, Zhao H, Zhang T, Zeng Z, Zhang P, Zhu B, et al. Amplification and adaptation of centromeric repeats in polyploid switchgrass species. New Phytol. 2018;218: 1645–1657. doi: 10.1111/nph.15098 29577299
54. Huang YC, Lee CC, Kao CY, Chang NC, Lin CC, Shoemaker D, et al. Evolution of long centromeres in fire ants. BMC Evol Biol. 2016;16: 1–14. doi: 10.1186/s12862-015-0575-y 26727998
55. Brinkley BR, Valdivia MM, Tousson A, Brenner SL. Compound kinetochores of the Indian muntjac. Chromosoma. 1984;91: 1–11. doi: 10.1007/BF00286479 6525895
56. Chi JX, Huang L, Nie W, Wang J, Su B, Yang F. Defining the orientation of the tandem fusions that occurred during the evolution of Indian muntjac chromosomes by BAC mapping. Chromosoma. 2005;114: 167–172. doi: 10.1007/s00412-005-0004-x 16010580
57. Kursel LE, Malik HS. The cellular mechanisms and consequences of centromere drive. Curr Opin Cell Biol. 2018;52: 58–65. doi: 10.1016/j.ceb.2018.01.011 29454259
58. Iwata-Otsubo A, Dawicki-McKenna JM, Akera T, Falk SJ, Chmátal L, Yang K, et al. Expanded Satellite Repeats Amplify a Discrete CENP-A Nucleosome Assembly Site on Chromosomes that Drive in Female Meiosis. Curr Biol. 2017;27: 2365–2373.e8. doi: 10.1016/j.cub.2017.06.069 28756949
59. Talbert PB, Henikoff S. What makes a centromere? Exp Cell Res. 2020;389: 111895. doi: 10.1016/j.yexcr.2020.111895 32035948
60. Cortes-Silva N, Ulmer J, Kiuchi T, Hsieh E, Cornilleau G, Ladid I, et al. CenH3-Independent Kinetochore Assembly in Lepidoptera Requires CCAN, Including CENP-T. Curr Biol. 2020;30: 561–572. doi: 10.1016/j.cub.2019.12.014 32032508
61. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9: 671–675. doi: 10.1038/nmeth.2089 22930834
62. Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. GenBank. Nucleic Acids Res. 2016;44: D67–D72. doi: 10.1093/nar/gkv1276 26590407
63. Bao W, Kojima KK, Kohany O. Repbase Update, a database of repetitive elements in eukaryotic genomes. Mob DNA. 2015;6: 4–9. doi: 10.1186/s13100-015-0035-7 25750667
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 10
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Proč při poslechu některé muziky prostě musíme tančit?
- Chůze do schodů pomáhá prodloužit život a vyhnout se srdečním chorobám
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- „Jednohubky“ z klinického výzkumu – 2024/44
Nejčtenější v tomto čísle
- Evaluation of both exonic and intronic variants for effects on RNA splicing allows for accurate assessment of the effectiveness of precision therapies
- RNA-directed DNA Methylation
- The DNA methylome of human sperm is distinct from blood with little evidence for tissue-consistent obesity associations
- Correction: Molecular predictors of brain metastasis-related microRNAs in lung adenocarcinoma