Evolutionary movement of centromeres in horse, donkey, and zebra.
Abstract: Centromere repositioning (CR) is a recently discovered biological phenomenon consisting of the emergence of a new centromere along a chromosome and the inactivation of the old one. After a CR, the primary constriction and the centromeric function are localized in a new position while the order of physical markers on the chromosome remains unchanged. These events profoundly affect chromosomal architecture. Since horses, asses, and zebras, whose evolutionary divergence is relatively recent, show remarkable morphological similarity and capacity to interbreed despite their chromosomes differing considerably, we investigated the role of CR in the karyotype evolution of the genus Equus. Using appropriate panels of BAC clones in FISH experiments, we compared the centromere position and marker order arrangement among orthologous chromosomes of Burchelli's zebra (Equus burchelli), donkey (Equus asinus), and horse (Equus caballus). Surprisingly, at least eight CRs took place during the evolution of this genus. Even more surprisingly, five cases of CR have occurred in the donkey after its divergence from zebra, that is, in a very short evolutionary time (approximately 1 million years). These findings suggest that in some species the CR phenomenon could have played an important role in karyotype shaping, with potential consequences on population dynamics and speciation.
Publication Date: 2006-01-18 PubMed ID: 16413164DOI: 10.1016/j.ygeno.2005.11.012Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Comparative Study
- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research article investigates the phenomenon known as centromere repositioning (CR) in horses, donkeys, and zebras. It found that during the evolution of these species, significant CR events have occurred, potentially influencing their karyotype development.
Understanding Centromere Repositioning (CR)
- Centromere Repositioning (CR) is a biological phenomenon that involves the shifting of the centromere to a new position on a chromosome, inactivating the existing one. The order of physical markers on the chromosome remains the same, yet its architecture changes drastically due to the new centromere location.
- The article reveals that key incidents of CR have been observed throughout the evolutionary journey of horses, donkeys, and zebras.
Investigation of CR in Genus Equus
- The study took aim at understanding the role of CR in the evolution of the karyotype – the number and visual appearance of the chromosomes – in the genus Equus, which includes horses, donkeys, and zebras. This group of animals shows notable similarities in physical structure and can interbreed, despite having considerable differences in their chromosomes.
- To explore this, the researchers utilized BAC (Bacterial Artificial Chromosomes) clones in Fluorescence In Situ Hybridization (FISH) experiments, which helped them compare the centromere positions and arrangements of physical markers on the chromosomes of the zebra, donkey, and horse.
Notable Findings
- The findings revealed that at least eight significant centromere repositioning events took place during the evolution of this genus.
- An unexpected revelation was that five of these CR events occurred in donkeys post their evolutionary divergence from zebras, and within a very short evolutionary timeframe- approximated at around 1 million years.
Implications of the Study
- The results suggest that centromere repositioning could have played a key role in shaping the karyotypes of some species, potentially influencing their population dynamics and even leading to new species.
- This understanding adds to the evolving narrative of genetic diversity and the varying evolutionary paths of related species.
Cite This Article
APA
Carbone L, Nergadze SG, Magnani E, Misceo D, Francesca Cardone M, Roberto R, Bertoni L, Attolini C, Francesca Piras M, de Jong P, Raudsepp T, Chowdhary BP, Guérin G, Archidiacono N, Rocchi M, Giulotto E.
(2006).
Evolutionary movement of centromeres in horse, donkey, and zebra.
Genomics, 87(6), 777-782.
https://doi.org/10.1016/j.ygeno.2005.11.012 Publication
Researcher Affiliations
- Department of Genetics and Microbiology, University of Bari, Via Amendola 165/A, 70126 Bari, Italy.
MeSH Terms
- Animals
- Biological Evolution
- Centromere / genetics
- Centromere / ultrastructure
- Chromosomes, Artificial, Bacterial / genetics
- Equidae / genetics
- Genetic Markers
- Horses / genetics
- In Situ Hybridization, Fluorescence
- Species Specificity
- Time Factors
Citations
This article has been cited 55 times.- Liu Y, Yi C, Fan C, Liu Q, Liu S, Shen L, Zhang K, Huang Y, Liu C, Wang Y, Tian Z, Han F. Pan-centromere reveals widespread centromere repositioning of soybean genomes.. Proc Natl Acad Sci U S A 2023 Oct 17;120(42):e2310177120.
- Cappelletti E, Piras FM, Sola L, Santagostino M, Petersen JL, Bellone RR, Finno CJ, Peng S, Kalbfleisch TS, Bailey E, Nergadze SG, Giulotto E. The localization of centromere protein A is conserved among tissues.. Commun Biol 2023 Sep 21;6(1):963.
- Piras FM, Cappelletti E, Abdelgadir WA, Salamon G, Vignati S, Santagostino M, Sola L, Nergadze SG, Giulotto E. A Satellite-Free Centromere in Equus przewalskii Chromosome 10.. Int J Mol Sci 2023 Feb 18;24(4).
- Zhao J, Xie Y, Kong C, Lu Z, Jia H, Ma Z, Zhang Y, Cui D, Ru Z, Wang Y, Appels R, Jia J, Zhang X. Centromere repositioning and shifts in wheat evolution.. Plant Commun 2023 Jul 10;4(4):100556.
- Jeffery D, Lochhead M, Almouzni G. CENP-A: A Histone H3 Variant with Key Roles in Centromere Architecture in Healthy and Diseased States.. Results Probl Cell Differ 2022;70:221-261.
- Cappelletti E, Piras FM, Sola L, Santagostino M, Abdelgadir WA, Raimondi E, Lescai F, Nergadze SG, Giulotto E. Robertsonian Fusion and Centromere Repositioning Contributed to the Formation of Satellite-free Centromeres During the Evolution of Zebras.. Mol Biol Evol 2022 Aug 3;39(8).
- Piras FM, Cappelletti E, Santagostino M, Nergadze SG, Giulotto E, Raimondi E. Molecular Dynamics and Evolution of Centromeres in the Genus Equus.. Int J Mol Sci 2022 Apr 10;23(8).
- Peng S, Petersen JL, Bellone RR, Kalbfleisch T, Kingsley NB, Barber AM, Cappelletti E, Giulotto E, Finno CJ. Decoding the Equine Genome: Lessons from ENCODE.. Genes (Basel) 2021 Oct 27;12(11).
- Balzano E, Giunta S. Centromeres under Pressure: Evolutionary Innovation in Conflict with Conserved Function.. Genes (Basel) 2020 Aug 10;11(8).
- Mandáková T, Hloušková P, Koch MA, Lysak MA. Genome Evolution in Arabideae Was Marked by Frequent Centromere Repositioning.. Plant Cell 2020 Mar;32(3):650-665.
- Ling YH, Lin Z, Yuen KWY. Genetic and epigenetic effects on centromere establishment.. Chromosoma 2020 Mar;129(1):1-24.
- Cappelletti E, Piras FM, Badiale C, Bambi M, Santagostino M, Vara C, Masterson TA, Sullivan KF, Nergadze SG, Ruiz-Herrera A, Giulotto E. CENP-A binding domains and recombination patterns in horse spermatocytes.. Sci Rep 2019 Nov 1;9(1):15800.
- Lawrimore J, Bloom K. The regulation of chromosome segregation via centromere loops.. Crit Rev Biochem Mol Biol 2019 Aug;54(4):352-370.
- Bracewell R, Chatla K, Nalley MJ, Bachtrog D. Dynamic turnover of centromeres drives karyotype evolution in Drosophila.. Elife 2019 Sep 16;8.
- Roberti A, Bensi M, Mazzagatti A, Piras FM, Nergadze SG, Giulotto E, Raimondi E. Satellite DNA at the Centromere is Dispensable for Segregation Fidelity.. Genes (Basel) 2019 Jun 20;10(6).
- Hartley G, O'Neill RJ. Centromere Repeats: Hidden Gems of the Genome.. Genes (Basel) 2019 Mar 16;10(3).
- Nergadze SG, Piras FM, Gamba R, Corbo M, Cerutti F, McCarter JGW, Cappelletti E, Gozzo F, Harman RM, Antczak DF, Miller D, Scharfe M, Pavesi G, Raimondi E, Sullivan KF, Giulotto E. Birth, evolution, and transmission of satellite-free mammalian centromeric domains.. Genome Res 2018 Jun;28(6):789-799.
- Capozzi O, Stanyon R, Archidiacono N, Ishida T, Romanenko SA, Rocchi M. Rapid emergence of independent "chromosomal lineages" in silvered-leaf monkey triggered by Y/autosome translocation.. Sci Rep 2018 Feb 19;8(1):3250.
- Matveevsky S, Kolomiets O, Bogdanov A, Hakhverdyan M, Bakloushinskaya I. Chromosomal Evolution in Mole Voles Ellobius (Cricetidae, Rodentia): Bizarre Sex Chromosomes, Variable Autosomes and Meiosis.. Genes (Basel) 2017 Nov 3;8(11).
- Romanenko SA, Serdyukova NA, Perelman PL, Pavlova SV, Bulatova NS, Golenishchev FN, Stanyon R, Graphodatsky AS. Intrachromosomal Rearrangements in Rodents from the Perspective of Comparative Region-Specific Painting.. Genes (Basel) 2017 Aug 30;8(9).
- Johnston SE, Huisman J, Ellis PA, Pemberton JM. A High-Density Linkage Map Reveals Sexual Dimorphism in Recombination Landscapes in Red Deer (Cervus elaphus).. G3 (Bethesda) 2017 Aug 7;7(8):2859-2870.
- Palomar G, Ahmad F, Vasemägi A, Matsuba C, Nicieza AG, Cano JM. Comparative High-Density Linkage Mapping Reveals Conserved Genome Structure but Variation in Levels of Heterochiasmy and Location of Recombination Cold Spots in the Common Frog.. G3 (Bethesda) 2017 Feb 9;7(2):637-645.
- Chiatante G, Capozzi O, Svartman M, Perelman P, Centrone L, Romanenko SS, Ishida T, Valeri M, Roelke-Parker ME, Stanyon R. Centromere repositioning explains fundamental number variability in the New World monkey genus Saimiri.. Chromosoma 2017 Aug;126(4):519-529.
- Chatterjee G, Sankaranarayanan SR, Guin K, Thattikota Y, Padmanabhan S, Siddharthan R, Sanyal K. Repeat-Associated Fission Yeast-Like Regional Centromeres in the Ascomycetous Budding Yeast Candida tropicalis.. PLoS Genet 2016 Feb;12(2):e1005839.
- Santagostino M, Khoriauli L, Gamba R, Bonuglia M, Klipstein O, Piras FM, Vella F, Russo A, Badiale C, Mazzagatti A, Raimondi E, Nergadze SG, Giulotto E. Genome-wide evolutionary and functional analysis of the Equine Repetitive Element 1: an insertion in the myostatin promoter affects gene expression.. BMC Genet 2015 Oct 26;16:126.
- Huang J, Zhao Y, Bai D, Shiraigol W, Li B, Yang L, Wu J, Bao W, Ren X, Jin B, Zhao Q, Li A, Bao S, Bao W, Xing Z, An A, Gao Y, Wei R, Bao Y, Bao T, Han H, Bai H, Bao Y, Zhang Y, Daidiikhuu D, Zhao W, Liu S, Ding J, Ye W, Ding F, Sun Z, Shi Y, Zhang Y, Meng H, Dugarjaviin M. Donkey genome and insight into the imprinting of fast karyotype evolution.. Sci Rep 2015 Sep 16;5:14106.
- Purgato S, Belloni E, Piras FM, Zoli M, Badiale C, Cerutti F, Mazzagatti A, Perini G, Della Valle G, Nergadze SG, Sullivan KF, Raimondi E, Rocchi M, Giulotto E. Centromere sliding on a mammalian chromosome.. Chromosoma 2015 Jun;124(2):277-87.
- Bloom KS. Centromeric heterochromatin: the primordial segregation machine.. Annu Rev Genet 2014;48:457-84.
- Plohl M, Meštrović N, Mravinac B. Centromere identity from the DNA point of view.. Chromosoma 2014 Aug;123(4):313-25.
- Musilova P, Kubickova S, Vahala J, Rubes J. Subchromosomal karyotype evolution in Equidae.. Chromosome Res 2013 Apr;21(2):175-87.
- Kalitsis P, Choo KH. The evolutionary life cycle of the resilient centromere.. Chromosoma 2012 Aug;121(4):327-40.
- Rocchi M, Archidiacono N, Schempp W, Capozzi O, Stanyon R. Centromere repositioning in mammals.. Heredity (Edinb) 2012 Jan;108(1):59-67.
- Graphodatsky AS, Trifonov VA, Stanyon R. The genome diversity and karyotype evolution of mammals.. Mol Cytogenet 2011 Oct 12;4:22.
- Black BE, Jansen LE, Foltz DR, Cleveland DW. Centromere identity, function, and epigenetic propagation across cell divisions.. Cold Spring Harb Symp Quant Biol 2010;75:403-18.
- Alkan C, Cardone MF, Catacchio CR, Antonacci F, O'Brien SJ, Ryder OA, Purgato S, Zoli M, Della Valle G, Eichler EE, Ventura M. Genome-wide characterization of centromeric satellites from multiple mammalian genomes.. Genome Res 2011 Jan;21(1):137-45.
- Shang WH, Hori T, Toyoda A, Kato J, Popendorf K, Sakakibara Y, Fujiyama A, Fukagawa T. Chickens possess centromeres with both extended tandem repeats and short non-tandem-repetitive sequences.. Genome Res 2010 Sep;20(9):1219-28.
- Gosálvez J, Crespo F, Vega-Pla JL, López-Fernández C, Cortés-Gutiérrez EI, Devila-Rodriguez MI, Mezzanotte R. Shared Y chromosome repetitive DNA sequences in stallion and donkey as visualized using whole-genomic comparative hybridization.. Eur J Histochem 2010 Jan 28;54(1):e2.
- Piras FM, Nergadze SG, Magnani E, Bertoni L, Attolini C, Khoriauli L, Raimondi E, Giulotto E. Uncoupling of satellite DNA and centromeric function in the genus Equus.. PLoS Genet 2010 Feb 12;6(2):e1000845.
- Trifonov VA, Kosyakova N, Romanenko SA, Stanyon R, Graphodatsky AS, Liehr T. New insights into the karyotypic evolution in muroid rodents revealed by multicolor banding applying murine probes.. Chromosome Res 2010 Feb;18(2):265-75.
- Srikulnath K, Nishida C, Matsubara K, Uno Y, Thongpan A, Suputtitada S, Apisitwanich S, Matsuda Y. Karyotypic evolution in squamate reptiles: comparative gene mapping revealed highly conserved linkage homology between the butterfly lizard (Leiolepis reevesii rubritaeniata, Agamidae, Lacertilia) and the Japanese four-striped rat snake (Elaphe quadrivirgata, Colubridae, Serpentes).. Chromosome Res 2009;17(8):975-86.
- Wade CM, Giulotto E, Sigurdsson S, Zoli M, Gnerre S, Imsland F, Lear TL, Adelson DL, Bailey E, Bellone RR, Blöcker H, Distl O, Edgar RC, Garber M, Leeb T, Mauceli E, MacLeod JN, Penedo MC, Raison JM, Sharpe T, Vogel J, Andersson L, Antczak DF, Biagi T, Binns MM, Chowdhary BP, Coleman SJ, Della Valle G, Fryc S, Guérin G, Hasegawa T, Hill EW, Jurka J, Kiialainen A, Lindgren G, Liu J, Magnani E, Mickelson JR, Murray J, Nergadze SG, Onofrio R, Pedroni S, Piras MF, Raudsepp T, Rocchi M, Røed KH, Ryder OA, Searle S, Skow L, Swinburne JE, Syvänen AC, Tozaki T, Valberg SJ, Vaudin M, White JR, Zody MC, Lander ES, Lindblad-Toh K. Genome sequence, comparative analysis, and population genetics of the domestic horse.. Science 2009 Nov 6;326(5954):865-7.
- Musilova P, Kubickova S, Horin P, Vodicka R, Rubes J. Karyotypic relationships in Asiatic asses (kulan and kiang) as defined using horse chromosome arm-specific and region-specific probes.. Chromosome Res 2009;17(6):783-90.
- Han Y, Zhang Z, Liu C, Liu J, Huang S, Jiang J, Jin W. Centromere repositioning in cucurbit species: implication of the genomic impact from centromere activation and inactivation.. Proc Natl Acad Sci U S A 2009 Sep 1;106(35):14937-41.
- Cellamare A, Catacchio CR, Alkan C, Giannuzzi G, Antonacci F, Cardone MF, Della Valle G, Malig M, Rocchi M, Eichler EE, Ventura M. New insights into centromere organization and evolution from the white-cheeked gibbon and marmoset.. Mol Biol Evol 2009 Aug;26(8):1889-900.
- Lomiento M, Jiang Z, D'Addabbo P, Eichler EE, Rocchi M. Evolutionary-new centromeres preferentially emerge within gene deserts.. Genome Biol 2008;9(12):R173.
- Schaeffer SW, Bhutkar A, McAllister BF, Matsuda M, Matzkin LM, O'Grady PM, Rohde C, Valente VL, Aguadé M, Anderson WW, Edwards K, Garcia AC, Goodman J, Hartigan J, Kataoka E, Lapoint RT, Lozovsky ER, Machado CA, Noor MA, Papaceit M, Reed LK, Richards S, Rieger TT, Russo SM, Sato H, Segarra C, Smith DR, Smith TF, Strelets V, Tobari YN, Tomimura Y, Wasserman M, Watts T, Wilson R, Yoshida K, Markow TA, Gelbart WM, Kaufman TC. Polytene chromosomal maps of 11 Drosophila species: the order of genomic scaffolds inferred from genetic and physical maps.. Genetics 2008 Jul;179(3):1601-55.
- Kobayashi T, Yamada F, Hashimoto T, Abe S, Matsuda Y, Kuroiwa A. Centromere repositioning in the X chromosome of XO/XO mammals, Ryukyu spiny rat.. Chromosome Res 2008;16(4):587-93.
- Trifonov VA, Stanyon R, Nesterenko AI, Fu B, Perelman PL, O'Brien PC, Stone G, Rubtsova NV, Houck ML, Robinson TJ, Ferguson-Smith MA, Dobigny G, Graphodatsky AS, Yang F. Multidirectional cross-species painting illuminates the history of karyotypic evolution in Perissodactyla.. Chromosome Res 2008;16(1):89-107.
- Chowdhary BP, Raudsepp T. The horse genome derby: racing from map to whole genome sequence.. Chromosome Res 2008;16(1):109-27.
- Capozzi O, Purgato S, Verdun di Cantogno L, Grosso E, Ciccone R, Zuffardi O, Della Valle G, Rocchi M. Evolutionary and clinical neocentromeres: two faces of the same coin?. Chromosoma 2008 Aug;117(4):339-44.
- Nakamura T, Matsubara K, Yasuda SP, Tsuchiya K, Matsuda Y. Chromosome homology between mouse and three Muridae species, Millardia meltada, Acomys dimidiatus and Micromys minutus, and conserved chromosome segments in murid karyotypes.. Chromosome Res 2007;15(8):1023-32.
- Musilova P, Kubickova S, Zrnova E, Horin P, Vahala J, Rubes J. Karyotypic relationships among Equus grevyi, Equus burchelli and domestic horse defined using horse chromosome arm-specific probes.. Chromosome Res 2007;15(6):807-13.
- Nakamura T, Kuroiwa A, Nishida-Umehara C, Matsubara K, Yamada F, Matsuda Y. Comparative chromosome painting map between two Ryukyu spiny rat species, Tokudaia osimensis and Tokudaia tokunoshimensis (Muridae, Rodentia).. Chromosome Res 2007;15(6):799-806.
- Yan H, Jiang J. Rice as a model for centromere and heterochromatin research.. Chromosome Res 2007;15(1):77-84.
- Cardone MF, Alonso A, Pazienza M, Ventura M, Montemurro G, Carbone L, de Jong PJ, Stanyon R, D'Addabbo P, Archidiacono N, She X, Eichler EE, Warburton PE, Rocchi M. Independent centromere formation in a capricious, gene-free domain of chromosome 13q21 in Old World monkeys and pigs.. Genome Biol 2006;7(10):R91.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists