1932
0

Annual Review of Animal Biosciences

Volume 13, 2025

Evolution of 3D Chromatin Folding

  • Lucía Álvarez-González1 and Aurora Ruiz-Herrera1
  • Genome Integrity and Instability Group, Institut de Biotecnologia i Biomedicina and Departament de Biologia Cel.lular, Fisiologia i Immunologia, Universitat Autònoma de Barcelona, Cerdanyola del Vallès, Spain; email: [email protected], [email protected]
  • Vol. 13:49-71 (Volume publication date February 2025)
  • First published as a Review in Advance on November 12, 2024
  • Copyright © 2025 by the author(s).
    This work is licensed under a Creative Commons Attribution 4.0 International License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. See credit lines of images or other third-party material in this article for license information.

Abstract

Studies examining the evolution of genomes have focused mainly on sequence conservation. However, the inner working of a cell implies tightly regulated crosstalk between complex gene networks controlled by small dispersed regulatory elements of physically contacting DNA regions. How these different levels of chromatin organization crosstalk in different species underpins the potential for genome evolutionary plasticity. We review the evolution of chromatin organization across the Animal Tree of Life. We introduce general aspects of the mode and tempo of genome evolution to later explore the multiple layers of genome organization. We argue that both genome and chromosome size modulate patterns of chromatin folding and that chromatin interactions facilitate the formation of lineage-specific chromosomal reorganizations, especially in germ cells. Overall, analyzing the mechanistic forces involved in the maintenance of chromatin structure and function of the germ line is critical for understanding genome evolution, maintenance, and inheritance.

Keyword(s): 3D genome, ancestral genome, chromosomal reorganizations, germ cells, Hi-C, topologically associated domains
Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-111523-102233
2025-02-18
2025-06-18
Loading full text...

Full text loading...

/deliver/fulltext/animal/13/1/annurev-animal-111523-102233.html?itemId=/content/journals/10.1146/annurev-animal-111523-102233&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    von Naegeli C. 1884.. Mechanisch-Physiologische Theorie der Abstammungslehre. Munich, Ger.:: R. Oldenbourg
     [Google Scholar]
  2. 2.
    Ruiz-Herrera A, Robinson TJ. 2008.. Evolutionary plasticity and cancer breakpoints in human chromosome 3. . BioEssays 30::1126–37. https://doi.org/10.1002/bies.20829
    [Crossref] [Google Scholar]
  3. 3.
    Robinson TJ, Ruiz-Herrera A, Avise JC. 2008.. Hemiplasy and homoplasy in the karyotypic phylogenies of mammals. . PNAS 105::14477–81. https://doi.org/10.1073/pnas.0807433105
    [Crossref] [Google Scholar]
  4. 4.
    Farré M, Kim J, Proskuryakova AA, Zhang Y, Kulemzina AI, et al. 2019.. Evolution of gene regulation in ruminants differs between evolutionary breakpoint regions and homologous synteny blocks. . Genome Res. 29::576–89. https://doi.org/10.1101/gr.239863.118
    [Crossref] [Google Scholar]
  5. 5.
    Damas J, Corbo M, Kim J, Turner-Maier J, Farré M, et al. 2022.. Evolution of the ancestral mammalian karyotype and syntenic regions. . PNAS 119::e2209139119. https://doi.org/10.1073/pnas.2209139119
    [Crossref] [Google Scholar]
  6. 6.
    Farré M, Robinson TJ, Ruiz-Herrera A. 2015.. An Integrative Breakage Model of genome architecture, reshuffling and evolution: the Integrative Breakage Model of genome evolution, a novel multidisciplinary hypothesis for the study of genome plasticity. . BioEssays 37::479–88. https://doi.org/10.1002/bies.201400174
    [Crossref] [Google Scholar]
  7. 7.
    Farré M, Bosch M, López-Giráldez F, Ponsà M, Ruiz-Herrera A. 2011.. Assessing the role of tandem repeats in shaping the genomic architecture of great apes. . PLOS ONE 6::e27239. https://doi.org/10.1371/journal.pone.0027239
    [Crossref] [Google Scholar]
  8. 8.
    Álvarez-González L, Burden F, Doddamani D, Malinverni R, Leach E, et al. 2022.. 3D chromatin remodelling in the germ line modulates genome evolutionary plasticity. . Nat. Commun. 13::2608. https://doi.org/10.1038/s41467-022-30296-6
    [Crossref] [Google Scholar]
  9. 9.
    Álvarez-González L, Arias-Sardá C, Montes-Espuña L, Marín-Gual L, Vara C, et al. 2022.. Principles of 3D chromosome folding and evolutionary genome reshuffling in mammals. . Cell Rep. 41::111839. https://doi.org/10.1016/j.celrep.2022.111839
    [Crossref] [Google Scholar]
  10. 10.
    Vara C, Paytuví-Gallart A, Cuartero Y, Le Dily F, Garcia F, et al. 2019.. Three-dimensional genomic structure and cohesin occupancy correlate with transcriptional activity during spermatogenesis. . Cell Rep. 28::352–67.e9. https://doi.org/10.1016/j.celrep.2019.06.037
    [Crossref] [Google Scholar]
  11. 11.
    Rao SSP, Huntley MH, Durand NC, Stamenova EK, Bochkov ID, et al. 2014.. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. . Cell 159::1665–80. https://doi.org/10.1016/j.cell.2014.11.021
    [Crossref] [Google Scholar]
  12. 12.
    Vietri Rudan M, Barrington C, Henderson S, Ernst C, Odom DT, et al. 2015.. Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture. . Cell Rep. 10::1297–309. https://doi.org/10.1016/j.celrep.2015.02.004
    [Crossref] [Google Scholar]
  13. 13.
    Land M, Hauser L, Jun S-R, Nookaew I, Leuze MR, et al. 2015.. Insights from 20 years of bacterial genome sequencing. . Funct. Integr. Genom. 15::141–61. https://doi.org/10.1007/s10142-015-0433-4
    [Crossref] [Google Scholar]
  14. 14.
    Redi CA, Capanna E. 2012.. Genome size evolution: sizing mammalian genomes. . Cytogenet. Genome Res. 137::97–112. https://doi.org/10.1159/000338820
    [Crossref] [Google Scholar]
  15. 15.
    Kapusta A, Suh A, Feschotte C. 2017.. Dynamics of genome size evolution in birds and mammals. . PNAS 114::E1460–69. https://doi.org/10.1073/pnas.1616702114
    [Crossref] [Google Scholar]
  16. 16.
    Larkin DM, Pape G, Donthu R, Auvil L, Welge M, Lewin HA. 2009.. Breakpoint regions and homologous synteny blocks in chromosomes have different evolutionary histories. . Genome Res. 19::770–77. https://doi.org/10.1101/gr.086546.108
    [Crossref] [Google Scholar]
  17. 17.
    Murphy WJ, Larkin DM, der Wind AE, Bourque G, Tesler G, et al. 2005.. Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. . Science 309::613–17. https://doi.org/10.1126/science.1111387
    [Crossref] [Google Scholar]
  18. 18.
    Ruiz-Herrera A, Castresana J, Robinson TJ. 2006.. Is mammalian chromosomal evolution driven by regions of genome fragility?. Genome Biol. 7::R115. https://doi.org/10.1186/gb-2006-7-12-r115
    [Crossref] [Google Scholar]
  19. 19.
    Rens W, O'Brien PCM, Yang F, Solanky N, Perelman P, et al. 2001.. Karyotype relationships between distantly related marsupials from South America and Australia. . Chromosome Res. 9::301–8. https://doi.org/10.1023/A:1016646629889
    [Crossref] [Google Scholar]
  20. 20.
    Graphodatsky AS, Perelman PL, Sokolovskaya NV, Beklemisheva VR, Serdukova NA, et al. 2008.. Phylogenomics of the dog and fox family (Canidae, Carnivora) revealed by chromosome painting. . Chromosome Res. 16::129–43. https://doi.org/10.1007/s10577-007-1203-5
    [Crossref] [Google Scholar]
  21. 21.
    Trifonov VA, Stanyon R, Nesterenko AI, Fu B, Perelman PL, et al. 2008.. Multidirectional cross-species painting illuminates the history of karyotypic evolution in Perissodactyla. . Chromosome Res. 16::89–107. https://doi.org/10.1007/s10577-007-1201-7
    [Crossref] [Google Scholar]
  22. 22.
    Rubes J, Musilova P, Kopecna O, Kubickova S, Cernohorska H, Kulemsina AI. 2012.. Comparative molecular cytogenetics in Cetartiodactyla. . Cytogenet. Genome Res. 137::194–207. https://doi.org/10.1159/000338932
    [Crossref] [Google Scholar]
  23. 23.
    Ruiz-Herrera A, García F, Aguilera M, Garcia M, Ponsà Fontanals M. 2005.. Comparative chromosome painting in Aotus reveals a highly derived evolution. . Am. J. Primatol. 65::73–85. https://doi.org/10.1002/ajp.20098
    [Crossref] [Google Scholar]
  24. 24.
    Stanyon R, Rocchi M, Capozzi O, Roberto R, Misceo D, et al. 2008.. Primate chromosome evolution: ancestral karyotypes, marker order and neocentromeres. . Chromosome Res. 16::17–39. https://doi.org/10.1007/s10577-007-1209-z
    [Crossref] [Google Scholar]
  25. 25.
    Ferguson-Smith MA, Trifonov V. 2007.. Mammalian karyotype evolution. . Nat. Rev. Genet. 8::950–62. https://doi.org/10.1038/nrg2199
    [Crossref] [Google Scholar]
  26. 26.
    Ruiz-Herrera A, Farré M, Robinson TJ. 2012.. Molecular cytogenetic and genomic insights into chromosomal evolution. . Heredity 108::28–36. https://doi.org/10.1038/hdy.2011.102
    [Crossref] [Google Scholar]
  27. 27.
    Robinson TJ, Ruiz-Herrera A. 2008.. Defining the ancestral eutherian karyotype: a cladistic interpretation of chromosome painting and genome sequence assembly data. . Chromosome Res. 16::1133–41. https://doi.org/10.1007/s10577-008-1264-0
    [Crossref] [Google Scholar]
  28. 28.
    Dudchenko O, Shamim MS, Batra SS, Durand NC, Musial NT, et al. 2018.. The Juicebox Assembly Tools module facilitates de novo assembly of mammalian genomes with chromosome-length scaffolds for under $1000. . bioRxiv 254797. https://doi.org/10.1101/254797
  29. 29.
    Christmas MJ, Kaplow IM, Genereux DP, Dong MX, Hughes GM, et al. 2023.. Evolutionary constraint and innovation across hundreds of placental mammals. . Science 380:(6643):eabn3943. https://doi.org/10.1126/science.abn3943
    [Crossref] [Google Scholar]
  30. 30.
    Mazzoni CJ, Ciofi C, Waterhouse RM. 2023.. Biodiversity: an atlas of European reference genomes. . Nature 619::252. https://doi.org/10.1038/d41586-023-02229-w
    [Crossref] [Google Scholar]
  31. 31.
    Koepfli K-P, Paten B, O'Brien SJ. 2015.. The Genome 10K Project: a way forward. . Annu Rev. Anim. Biosci. 3::57–111. https://doi.org/10.1146/annurev-animal-090414-014900
    [Crossref] [Google Scholar]
  32. 32.
    Lewin HA, Robinson GE, Kress WJ, Baker WJ, Coddington J, et al. 2018.. Earth BioGenome Project: sequencing life for the future of life. . PNAS 115::4325–33. https://doi.org/10.1073/pnas.1720115115
    [Crossref] [Google Scholar]
  33. 33.
    Hogg CJ. 2023.. Translating genomic advances into biodiversity conservation. . Nat. Rev. Genet. 25::362–73. https://doi.org/10.1038/s41576-023-00671-0
    [Crossref] [Google Scholar]
  34. 34.
    Theissinger K, Fernandes C, Formenti G, Bista I, Berg PR, et al. 2023.. How genomics can help biodiversity conservation. . Trends Genet. 39::545–59. https://doi.org/10.1016/j.tig.2023.01.005
    [Crossref] [Google Scholar]
  35. 35.
    Simakov O, Bredeson J, Berkoff K, Marletaz F, Mitros T, et al. 2022.. Deeply conserved synteny and the evolution of metazoan chromosomes. . Sci. Adv. 8::eabi5884. https://doi.org/10.1126/sciadv.abi5884
    [Crossref] [Google Scholar]
  36. 36.
    Zimmermann B, Montenegro JD, Robb SMC, Fropf WJ, Weilguny L, et al. 2023.. Topological structures and syntenic conservation in sea anemone genomes. . Nat. Commun. 14::8270. https://doi.org/10.1038/s41467-023-44080-7
    [Crossref] [Google Scholar]
  37. 37.
    Simakov O, Marlétaz F, Yue J-X, O'Connell B, Jenkins J, et al. 2020.. Deeply conserved synteny resolves early events in vertebrate evolution. . Nat. Ecol. Evol. 4::820–30. https://doi.org/10.1038/s41559-020-1156-z
    [Crossref] [Google Scholar]
  38. 38.
    Ruiz-Trillo I, Kin K, Casacuberta E. 2023.. The origin of metazoan multicellularity: a potential microbial black swan event. . Annu. Rev. Microbiol. 77::499–516. https://doi.org/10.1146/annurev-micro-032421-120023
    [Crossref] [Google Scholar]
  39. 39.
    King N, Rokas A. 2017.. Embracing uncertainty in reconstructing early animal evolution. . Curr. Biol. 27::R1081–88. https://doi.org/10.1016/j.cub.2017.08.054
    [Crossref] [Google Scholar]
  40. 40.
    Kumar S, Suleski M, Craig JM, Kasprowicz AE, Sanderford M, et al. 2022.. TimeTree 5: an expanded resource for species divergence times. . Mol. Biol. Evol. 39::msac174. https://doi.org/10.1093/molbev/msac174
    [Crossref] [Google Scholar]
  41. 41.
    Sacerdot C, Louis A, Bon C, Berthelot C, Roest Crollius H. 2018.. Chromosome evolution at the origin of the ancestral vertebrate genome. . Genome Biol. 19::166. https://doi.org/10.1186/s13059-018-1559-1
    [Crossref] [Google Scholar]
  42. 42.
    Valenzuela N, Adams DC. 2011.. Chromosome number and sex determination coevolve in turtles. . Evolution 65::1808–13. https://doi.org/10.1111/j.1558-5646.2011.01258.x
    [Crossref] [Google Scholar]
  43. 43.
    Deakin JE, Potter S, O'Neill R, Ruiz-Herrera A, Cioffi MB, et al. 2019.. Chromosomics: bridging the gap between genomes and chromosomes. . Genes 10::627. https://doi.org/10.3390/genes10080627
    [Crossref] [Google Scholar]
  44. 44.
    Waters PD, Patel HR, Ruiz-Herrera A, Álvarez-González L, Lister NC, et al. 2021.. Microchromosomes are building blocks of bird, reptile, and mammal chromosomes. . PNAS 118::e2112494118. https://doi.org/10.1073/pnas.2112494118
    [Crossref] [Google Scholar]
  45. 45.
    Capilla L, Sánchez-Guillén RA, Farré M, Paytuví-Gallart A, Malinverni R, 2016.. Mammalian comparative genomics reveals genetic and epigenetic features associated with genome reshuffling in Rodentia. . Genome Biol. Evol. 8::3703–17. https://doi.org/10.1093/gbe/evw276
    [Google Scholar]
  46. 46.
    Ullastres A, Farré M, Capilla L, Ruiz-Herrera A. 2014.. Unraveling the effect of genomic structural changes in the rhesus macaque—implications for the adaptive role of inversions. . BMC Genom. 15::530. https://doi.org/10.1186/1471-2164-15-530
    [Crossref] [Google Scholar]
  47. 47.
    Carvalho CMB, Zhang F, Lupski JR. 2010.. Genomic disorders: a window into human gene and genome evolution. . PNAS 107::1765–71. https://doi.org/10.1073/pnas.0906222107
    [Crossref] [Google Scholar]
  48. 48.
    Vara C, Paytuví-Gallart A, Cuartero Y, Álvarez-González L, Marín-Gual L, et al. 2021.. The impact of chromosomal fusions on 3D genome folding and recombination in the germ line. . Nat. Commun. 12::2981. https://doi.org/10.1038/s41467-021-23270-1
    [Crossref] [Google Scholar]
  49. 49.
    Cain CE, Blekhman R, Marioni JC, Gilad Y. 2011.. Gene expression differences among primates are associated with changes in a histone epigenetic modification. . Genetics 187::1225–34. https://doi.org/10.1534/genetics.110.126177
    [Crossref] [Google Scholar]
  50. 50.
    Dong X, Weng Z. 2013.. The correlation between histone modifications and gene expression. . Epigenomics 5::113–16. https://doi.org/10.2217/epi.13.13
    [Crossref] [Google Scholar]
  51. 51.
    Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, et al. 2009.. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. . Science 326::289–93. https://doi.org/10.1126/science.1181369
    [Crossref] [Google Scholar]
  52. 52.
    Dixon JR, Gorkin DU, Ren B. 2016.. Chromatin domains: the unit of chromosome organization. . Mol. Cell 62::668–80. https://doi.org/10.1016/j.molcel.2016.05.018
    [Crossref] [Google Scholar]
  53. 53.
    Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, et al. 2012.. Topological domains in mammalian genomes identified by analysis of chromatin interactions. . Nature 485::376–80. https://doi.org/10.1038/nature11082
    [Crossref] [Google Scholar]
  54. 54.
    Pombo A, Dillon N. 2015.. Three-dimensional genome architecture: players and mechanisms. . Nat. Rev. Mol. Cell Biol. 16::245–57. https://doi.org/10.1038/nrm3965
    [Crossref] [Google Scholar]
  55. 55.
    Yu M, Ren B. 2017.. The three-dimensional organization of mammalian genomes. . Annu. Rev. Cell Dev. Biol. 33::265–89. https://doi.org/10.1146/annurev-cellbio-100616-060531
    [Crossref] [Google Scholar]
  56. 56.
    Lazar NH, Nevonen KA, O'Connell B, McCann C, O'Neill RJ, et al. 2018.. Epigenetic maintenance of topological domains in the highly rearranged gibbon genome. . Genome Res. 28::983–97. https://doi.org/10.1101/gr.233874.117
    [Crossref] [Google Scholar]
  57. 57.
    Van Bortle K, Ramos E, Takenaka N, Yang J, Wahi JE, Corces VG. 2012.. Drosophila CTCF tandemly aligns with other insulator proteins at the borders of H3K27me3 domains. . Genome Res. 22::2176–87. https://doi.org/10.1101/gr.136788.111
    [Crossref] [Google Scholar]
  58. 58.
    Martin D, Pantoja C, Miñán AF, Valdes-Quezada C, Moltó E, et al. 2011.. Genome-wide CTCF distribution in vertebrates defines equivalent sites that aid the identification of disease-associated genes. . Nat. Struct. Mol. Biol. 18::708–14. https://doi.org/10.1038/nsmb.2059
    [Crossref] [Google Scholar]
  59. 59.
    Bonev B, Cavalli G. 2016.. Organization and function of the 3D genome. . Nat. Rev. Genet. 17::661–78. https://doi.org/10.1038/nrg.2016.112
    [Crossref] [Google Scholar]
  60. 60.
    Ren G, Jin W, Cui K, Rodrigez J, Hu G, et al. 2017.. CTCF-mediated enhancer-promoter interaction is a critical regulator of cell-to-cell variation of gene expression. . Mol. Cell 67::1049–58.e6. https://doi.org/10.1016/j.molcel.2017.08.026
    [Crossref] [Google Scholar]
  61. 61.
    Nora EP, Goloborodko A, Valton A-L, Gibcus JH, Uebersohn A, et al. 2017.. Targeted degradation of CTCF decouples local insulation of chromosome domains from genomic compartmentalization. . Cell 169::930–44.e22. https://doi.org/10.1016/j.cell.2017.05.004
    [Crossref] [Google Scholar]
  62. 62.
    Schwarzer W, Abdennur N, Goloborodko A, Pekowska A, Fudenberg G, et al. 2017.. Two independent modes of chromatin organization revealed by cohesin removal. . Nature 551::51–56. https://doi.org/10.1038/nature24281
    [Crossref] [Google Scholar]
  63. 63.
    Heinz S, Texari L, Hayes MGB, Urbanowski M, Chang MW, et al. 2018.. Transcription elongation can affect genome 3D structure. . Cell 174::1522–36.e22. https://doi.org/10.1016/j.cell.2018.07.047
    [Crossref] [Google Scholar]
  64. 64.
    Du Z, Zheng H, Huang B, Ma R, Wu J, et al. 2017.. Allelic reprogramming of 3D chromatin architecture during early mammalian development. . Nature 547::232–35. https://doi.org/10.1038/nature23263
    [Crossref] [Google Scholar]
  65. 65.
    Bonev B, Mendelson Cohen N, Szabo Q, Fritsch L, Papadopoulos GL, et al. 2017.. Multiscale 3D genome rewiring during mouse neural development. . Cell 171::557–72.e24. https://doi.org/10.1016/j.cell.2017.09.043
    [Crossref] [Google Scholar]
  66. 66.
    Szabo Q, Bantignies F, Cavalli G. 2019.. Principles of genome folding into topologically associating domains. . Sci. Adv. 5::eaaw1668. https://doi.org/10.1126/sciadv.aaw1668
    [Crossref] [Google Scholar]
  67. 67.
    Raffo A, Paulsen J. 2023.. The shape of chromatin: insights from computational recognition of geometric patterns in Hi-C data. . Brief. Bioinform. 24::bbad302. https://doi.org/10.1093/bib/bbad302
    [Crossref] [Google Scholar]
  68. 68.
    Dekker J, Marti-Renom MA, Mirny LA. 2013.. Exploring the three-dimensional organization of genomes: interpreting chromatin interaction data. . Nat. Rev. Genet. 14::390–403. https://doi.org/10.1038/nrg3454
    [Crossref] [Google Scholar]
  69. 69.
    Sexton T, Yaffe E, Kenigsberg E, Bantignies F, Leblanc B, et al. 2012.. Three-dimensional folding and functional organization principles of the Drosophila genome. . Cell 148::458–72. https://doi.org/10.1016/j.cell.2012.01.010
    [Crossref] [Google Scholar]
  70. 70.
    Dillon N. 2004.. Heterochromatin structure and function. . Biol. Cell 96::631–37. https://doi.org/10.1016/j.biolcel.2004.06.003
    [Crossref] [Google Scholar]
  71. 71.
    Eagen KP. 2018.. Principles of chromosome architecture revealed by Hi-C. . Trends Biochem. Sci. 43::469–78. https://doi.org/10.1016/j.tibs.2018.03.006
    [Crossref] [Google Scholar]
  72. 72.
    Penagos-Puig A, Furlan-Magaril M. 2020.. Heterochromatin as an important driver of genome organization. . Front. Cell Dev. Biol. 8::579137. https://doi.org/10.3389/fcell.2020.579137
    [Crossref] [Google Scholar]
  73. 73.
    Hoencamp C, Dudchenko O, Elbatsh AMO, Brahmachari S, Raaijmakers JA, et al. 2021.. 3D genomics across the tree of life reveals condensin II as a determinant of architecture type. . Science 372:984–89. https://doi.org/10.1126/science.abe2218
    [Google Scholar]
  74. 74.
    Rabl C. 1885.. Über Zelltheilung. . Morphol. Jahrb. 10::214–330
     [Google Scholar]
  75. 75.
    Cremer T, Cremer C. 2001.. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. . Nat. Rev. Genet. 2::292–301. https://doi.org/10.1038/35066075
    [Crossref] [Google Scholar]
  76. 76.
    Shim S-H. 2021.. Super-resolution microscopy of genome organization. . Genes Genom. 43::281–87. https://doi.org/10.1007/s13258-021-01044-9
    [Crossref] [Google Scholar]
  77. 77.
    Fritz AJ, Sehgal N, Pliss A, Xu J, Berezney R. 2019.. Chromosome territories and the global regulation of the genome. . Genes Chromosom. Cancer 58::407–26. https://doi.org/10.1002/gcc.22732
    [Crossref] [Google Scholar]
  78. 78.
    van de Werken HJG, Haan JC, Feodorova Y, Bijos D, Weuts A, et al. 2017.. Small chromosomal regions position themselves autonomously according to their chromatin class. . Genome Res. 27::922–33. https://doi.org/10.1101/gr.213751.116
    [Crossref] [Google Scholar]
  79. 79.
    Solovei I, Thanisch K, Feodorova Y. 2016.. How to rule the nucleus: Divide et impera. . Curr. Opin. Cell Biol. 40::47–59. https://doi.org/10.1016/j.ceb.2016.02.014
    [Crossref] [Google Scholar]
  80. 80.
    Foley NM, Mason VC, Harris AJ, Bredemeyer KR, Damas J, et al. 2023.. A genomic timescale for placental mammal evolution. . Science 380:(6643):eabl8189. https://doi.org/10.1126/science.abl8189
    [Crossref] [Google Scholar]
  81. 81.
    Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, et al. 2011.. Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification. . Science 334::521–24. https://doi.org/10.1126/science.1211028
    [Crossref] [Google Scholar]
  82. 82.
    Deakin JE, O'Neill RJ. 2020.. Evolution of marsupial genomes. . Annu. Rev. Anim. Biosci. 8::25–45. https://doi.org/10.1146/annurev-animal-021419-083555
    [Crossref] [Google Scholar]
  83. 83.
    Schmidt D, Schwalie PC, Wilson MD, Ballester B, Gonalves Â, et al. 2012.. Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. . Cell 148::335–48. https://doi.org/10.1016/j.cell.2011.11.058
    [Crossref] [Google Scholar]
  84. 84.
    Mirny LA. 2011.. The fractal globule as a model of chromatin architecture in the cell. . Chromosome Res. 19::37–51. https://doi.org/10.1007/s10577-010-9177-0
    [Crossref] [Google Scholar]
  85. 85.
    Shedlock AM, Edwards SV. 2009.. Amniotes (amniota). . In The Timetree of Life, ed. SB Hedges, S Kumar , pp. 375–79. Oxford, UK:: Oxford Univ. Press
     [Google Scholar]
  86. 86.
    Damas J, Kim J, Farré M, Griffin DK, Larkin DM. 2018.. Reconstruction of avian ancestral karyotypes reveals differences in the evolutionary history of macro- and microchromosomes. . Genome Biol. 19::155. https://doi.org/10.1186/s13059-018-1544-8
    [Crossref] [Google Scholar]
  87. 87.
    Srikulnath K, Ahmad SF, Singchat W, Panthum T. 2021.. Why do some vertebrates have microchromosomes?. Cells 10::2182. https://doi.org/10.3390/cells10092182
    [Crossref] [Google Scholar]
  88. 88.
    Habermann FA, Cremer M, Walter J, Kreth G, von Hase J, et al. 2001.. Arrangements of macro- and microchromosomes in chicken cells. . Chromosome Res. 9::569–84. https://doi.org/10.1023/A:1012447318535
    [Crossref] [Google Scholar]
  89. 89.
    Mandrioli M, Bandinelli S, Manicardi GC. 2014.. Occurrence of Rabl-like telomere clustering in the holocentric chromosomes of the peach potato aphid Myzus persicae (Hemiptera; Aphididae). . Cytogenet. Genome Res. 144::68–75. https://doi.org/10.1159/000366049
    [Crossref] [Google Scholar]
  90. 90.
    Pouokam M, Cruz B, Burgess S, Segal MR, Vazquez M, Arsuaga J. 2019.. The Rabl configuration limits topological entanglement of chromosomes in budding yeast. . Sci. Rep. 9::6795. https://doi.org/10.1038/s41598-019-42967-4
    [Crossref] [Google Scholar]
  91. 91.
    Corbo M, Damas J, Bursell MG, Lewin HA. 2022.. Conservation of chromatin conformation in carnivores. . PNAS 119::e2120555119. https://doi.org/10.1073/pnas.2120555119
    [Crossref] [Google Scholar]
  92. 92.
    Sandoval-Velasco M, Dudchenko O, Rodríguez JA, Pérez Estrada C, Dehasque M, et al. 2024.. Three-dimensional genome architecture persists in a 52,000-year-old woolly mammoth skin sample. . Cell 187::3541–62.e51. https://doi.org/10.1016/j.cell.2024.06.002
    [Crossref] [Google Scholar]
  93. 93.
    Dekker J, Misteli T. 2015.. Long-range chromatin interactions. . Cold Spring Harb. Perspect. Biol. 7::a019356. https://doi.org/10.1101/cshperspect.a019356
    [Crossref] [Google Scholar]
  94. 94.
    Long HS, Greenaway S, Powell G, Mallon A-M, Lindgren CM, Simon MM. 2022.. Making sense of the linear genome, gene function and TADs. . Epigenetics Chromatin 15::4. https://doi.org/10.1186/s13072-022-00436-9
    [Crossref] [Google Scholar]
  95. 95.
    Kentepozidou E, Aitken SJ, Feig C, Stefflova K, Ibarra-Soria X, et al. 2020.. Clustered CTCF binding is an evolutionary mechanism to maintain topologically associating domains. . Genome Biol. 21::5. https://doi.org/10.1186/s13059-019-1894-x
    [Crossref] [Google Scholar]
  96. 96.
    Merkenschlager M, Nora EP. 2016.. CTCF and cohesin in genome folding and transcriptional gene regulation. . Annu. Rev. Genom. Hum. Genet. 17::17–43. https://doi.org/10.1146/annurev-genom-083115-022339
    [Crossref] [Google Scholar]
  97. 97.
    Phillips JE, Corces VG. 2009.. CTCF: master weaver of the genome. . Cell 137::1194–211. https://doi.org/10.1016/j.cell.2009.06.001
    [Crossref] [Google Scholar]
  98. 98.
    Patel L, Kang R, Rosenberg SC, Qiu Y, Raviram R, et al. 2019.. Dynamic reorganization of the genome shapes the recombination landscape in meiotic prophase. . Nat. Struct. Mol. Biol. 26::164–74. https://doi.org/10.1038/s41594-019-0187-0
    [Crossref] [Google Scholar]
  99. 99.
    Zhang H, Emerson DJ, Gilgenast TG, Titus KR, Lan Y, et al. 2019.. Chromatin structure dynamics during the mitosis-to-G1 phase transition. . Nature 576::158–62. https://doi.org/10.1038/s41586-019-1778-y
    [Crossref] [Google Scholar]
  100. 100.
    Liu Z, Belmonte JCI, Zhang W, Qu J, Liu G-H. 2022.. Deciphering aging at three-dimensional genomic resolution. . Cell Insight 1::100034. https://doi.org/10.1016/j.cellin.2022.100034
    [Crossref] [Google Scholar]
  101. 101.
    Fishman V, Battulin N, Nuriddinov M, Maslova A, Zlotina A, et al. 2019.. 3D organization of chicken genome demonstrates evolutionary conservation of topologically associated domains and highlights unique architecture of erythrocytes’ chromatin. . Nucleic Acids Res. 47::648–65. https://doi.org/10.1093/nar/gky1103
    [Crossref] [Google Scholar]
  102. 102.
    Wike CL, Guo Y, Tan M, Nakamura R, Shaw DK, et al. 2021.. Chromatin architecture transitions from zebrafish sperm through early embryogenesis. . Genome Res. 31::981–94. https://doi.org/10.1101/gr.269860.120
    [Crossref] [Google Scholar]
  103. 103.
    Zhou Y, Shearwin-Whyatt L, Li J, Song Z, Hayakawa T, et al. 2021.. Platypus and echidna genomes reveal mammalian biology and evolution. . Nature 592::756–62. https://doi.org/10.1038/s41586-020-03039-0
    [Crossref] [Google Scholar]
  104. 104.
    Acemel RD, Lupiáñez DG. 2023.. Evolution of 3D chromatin organization at different scales. . Curr. Opin. Genet. Dev. 78::102019. https://doi.org/10.1016/j.gde.2022.102019
    [Crossref] [Google Scholar]
  105. 105.
    Ea V, Baudement M-O, Lesne A, Forné T. 2015.. Contribution of topological domains and loop formation to 3D chromatin organization. . Genes 6::734–50. https://doi.org/10.3390/genes6030734
    [Crossref] [Google Scholar]
  106. 106.
    Fudenberg G, Imakaev M, Lu C, Goloborodko A, Abdennur N, Mirny LA. 2016.. Formation of chromosomal domains by loop extrusion. . Cell Rep. 15::2038–49. https://doi.org/10.1016/j.celrep.2016.04.085
    [Crossref] [Google Scholar]
  107. 107.
    Rogers TF, Simakov O. 2023.. Emerging questions on the mechanisms and dynamics of 3D genome evolution in spiralians. . Brief. Funct. Genom. 22::533–42. https://doi.org/10.1093/bfgp/elad043
    [Crossref] [Google Scholar]
  108. 108.
    Dudchenko O, Batra SS, Omer AD, Nyquist SK, Hoeger M, et al. 2017.. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. . Science 356::92–95. https://doi.org/10.1126/science.aal3327
    [Crossref] [Google Scholar]
  109. 109.
    Lukyanchikova V, Nuriddinov M, Belokopytova P, Taskina A, Liang J, et al. 2022.. Anopheles mosquitoes reveal new principles of 3D genome organization in insects. . Nat. Commun. 13::1960. https://doi.org/10.1038/s41467-022-29599-5
    [Crossref] [Google Scholar]
  110. 110.
    Cavalli G, Misteli T. 2013.. Functional implications of genome topology. . Nat. Struct. Mol. Biol. 20::290–99. https://doi.org/10.1038/nsmb.2474
    [Crossref] [Google Scholar]
  111. 111.
    Arnould C, Rocher V, Saur F, Bader AS, Muzzopappa F, et al. 2023.. Chromatin compartmentalization regulates the response to DNA damage. . Nature 623::183–92. https://doi.org/10.1038/s41586-023-06635-y
    [Crossref] [Google Scholar]
  112. 112.
    Mellone BG, Fachinetti D. 2021.. Diverse mechanisms of centromere specification. . Curr. Biol. 31::R1491–504. https://doi.org/10.1016/j.cub.2021.09.083
    [Crossref] [Google Scholar]
  113. 113.
    Muller H, Gil J, Drinnenberg IA. 2019.. The impact of centromeres on spatial genome architecture. . Trends Genet. 35::565–78. https://doi.org/10.1016/j.tig.2019.05.003
    [Crossref] [Google Scholar]
  114. 114.
    Ferreri GC, Marzelli M, Rens W, O'Neill RJ. 2004.. A centromere-specific retroviral element associated with breaks of synteny in macropodine marsupials. . Cytogenet. Genome Res. 107::115–18. https://doi.org/10.1159/000079580
    [Crossref] [Google Scholar]
  115. 115.
    Metcalfe CJ, Bulazel KV, Ferreri GC, Schroeder-Reiter E, Wanner G, et al. 2007.. Genomic instability within centromeres of interspecific marsupial hybrids. . Genetics 177::2507–17. https://doi.org/10.1534/genetics.107.082313
    [Crossref] [Google Scholar]
  116. 116.
    O'Neill RJ, Eldridge MDB, Metcalfe CJ. 2004.. Centromere dynamics and chromosome evolution in marsupials. . J. Hered. 95::375–81. https://doi.org/10.1093/jhered/esh063
    [Crossref] [Google Scholar]
  117. 117.
    Westerman M, Meredith RW, Springer MS. 2010.. Cytogenetics meets phylogenetics: a review of karyotype evolution in diprotodontian marsupials. . J. Hered. 101::690–702. https://doi.org/10.1093/jhered/esq076
    [Crossref] [Google Scholar]
  118. 118.
    Branco MR, Pombo A. 2006.. Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations. . PLOS Biol. 4::e138. https://doi.org/10.1371/journal.pbio.0040138
    [Crossref] [Google Scholar]
  119. 119.
    van Schaik T, Vos M, Peric-Hupkes D, Celie PHN, van Steensel B. 2020.. Cell cycle dynamics of lamina-associated DNA. . EMBO Rep. 21::e50636. https://doi.org/10.15252/embr.202050636
    [Crossref] [Google Scholar]
  120. 120.
    White M. 1978.. Modes of Speciation. San Francisco, CA:: W.H. Freeman
     [Google Scholar]
  121. 121.
    Fuller ZL, Leonard CJ, Young RE, Schaeffer SW, Phadnis N. 2018.. Ancestral polymorphisms explain the role of chromosomal inversions in speciation. . PLOS Genet. 14::e1007526. https://doi.org/10.1371/journal.pgen.1007526
    [Crossref] [Google Scholar]
  122. 122.
    Giner-Delgado C, Villatoro S, Lerga-Jaso J, Gayà-Vidal M, Oliva M, et al. 2019.. Evolutionary and functional impact of common polymorphic inversions in the human genome. . Nat. Commun. 10::4222. https://doi.org/10.1038/s41467-019-12173-x
    [Crossref] [Google Scholar]
  123. 123.
    Harr B. 2006.. Genomic islands of differentiation between house mouse subspecies. . Genome Res. 16::730–37. https://doi.org/10.1101/gr.5045006
    [Crossref] [Google Scholar]
  124. 124.
    Hejase HA, Salman-Minkov A, Campagna L, Hubisz MJ, Lovette IJ, et al. 2020.. Genomic islands of differentiation in a rapid avian radiation have been driven by recent selective sweeps. . PNAS 117::30554–65. https://doi.org/10.1073/pnas.2015987117
    [Crossref] [Google Scholar]
  125. 125.
    Malinsky M, Challis RJ, Tyers AM, Schiffels S, Terai Y, et al. 2015.. Genomic islands of speciation separate cichlid ecomorphs in an East African crater lake. . Science 350::P1493–98. https://doi.org/10.1126/science.aac9927
    [Crossref] [Google Scholar]
  126. 126.
    Nadeau NJ, Whibley A, Jones RT, Davey JW, Dasmahapatra KK, et al. 2012.. Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing. . Philos. Trans. R. Soc. B 367::343–53. https://doi.org/10.1098/rstb.2011.0198
    [Crossref] [Google Scholar]
  127. 127.
    Hahn MW, White BJ, Muir CD, Besansky NJ. 2012.. No evidence for biased co-transmission of speciation islands in Anopheles gambiae. . Philos. Trans. R. Soc. B 367::374–84. https://doi.org/10.1098/rstb.2011.0188
    [Crossref] [Google Scholar]
  128. 128.
    Nosil P, Feder JL. 2012.. Genomic divergence during speciation: causes and consequences. . Philos. Trans. R. Soc. B 367::332–42. https://doi.org/10.1098/rstb.2011.0263
    [Crossref] [Google Scholar]
  129. 129.
    Rieseberg LH. 2001.. Chromosomal rearrangements and speciation. . Trends Ecol. Evol. 16::351–58. https://doi.org/10.1016/S0169-5347(01)02187-5
    [Crossref] [Google Scholar]
  130. 130.
    Wang Y, Wang H, Zhang Y, Du Z, Si W, et al. 2019.. Reprogramming of meiotic chromatin architecture during spermatogenesis. . Mol. Cell 73::547–61.e6. https://doi.org/10.1016/j.molcel.2018.11.019
    [Crossref] [Google Scholar]
  131. 131.
    Vara C, Ruiz-Herrera A. 2021.. Unpacking chromatin remodelling in germ cells: implications for development and evolution. . Trends Genet. 38::422–25. https://doi.org/10.1016/j.tig.2021.10.007
    [Crossref] [Google Scholar]
  132. 132.
    Reig-Viader R, Capilla L, Vila-Cejudo M, Garcia F, Anguita B, et al. 2014.. Telomere homeostasis is compromised in spermatocytes from patients with idiopathic infertility. . Fertil. Steril. 102::728–738.e1. https://doi.org/10.1016/j.fertnstert.2014.06.005
    [Crossref] [Google Scholar]
  133. 133.
    Ruiz-Herrera A, Vozdova M, Fernández J, Sebestova H, Capilla L, et al. 2017.. Recombination correlates with synaptonemal complex length and chromatin loop size in bovids—insights into mammalian meiotic chromosomal organization. . Chromosoma 126::615–31. https://doi.org/10.1007/s00412-016-0624-3
    [Crossref] [Google Scholar]
  134. 134.
    Storlazzi A, Gargano S, Ruprich-Robert G, Falque M, David M, et al. 2010.. Recombination proteins mediate meiotic spatial chromosome organization and pairing. . Cell 141::94–106. https://doi.org/10.1016/j.cell.2010.02.041
    [Crossref] [Google Scholar]
  135. 135.
    Wang S, Zickler D, Kleckner N, Zhang L. 2015.. Meiotic crossover patterns: obligatory crossover, interference and homeostasis in a single process. . Cell Cycle 14::305–14. https://doi.org/10.4161/15384101.2014.991185
    [Crossref] [Google Scholar]
  136. 136.
    Zickler D, Kleckner N. 2015.. Recombination, pairing, and synapsis of homologs during meiosis. . Cold Spring Harb. Perspect. Biol. 7::a016626. https://doi.org/10.1101/cshperspect.a016626
    [Crossref] [Google Scholar]
  137. 137.
    Subramanian VV, Hochwagen A. 2014.. The meiotic checkpoint network: step-by-step through meiotic prophase. . Cold Spring Harb. Perspect. Biol. 6::a016675. https://doi.org/10.1101/cshperspect.a016675
    [Crossref] [Google Scholar]
  138. 138.
    Waters PD, Ruiz-Herrera A. 2020.. Meiotic executioner genes protect the Y from extinction. . Trends Genet. 36::728–38. https://doi.org/10.1016/j.tig.2020.06.008
    [Crossref] [Google Scholar]
  139. 139.
    Rathke C, Baarends WM, Awe S, Renkawitz-Pohl R. 2014.. Chromatin dynamics during spermiogenesis. . Biochim. Biophys. Acta Gene Regul. Mech. 1839::155–68. https://doi.org/10.1016/j.bbagrm.2013.08.004
    [Crossref] [Google Scholar]
  140. 140.
    Ward WS. 2010.. Function of sperm chromatin structural elements in fertilization and development. . Mol. Hum. Reprod. 16::30–36. https://doi.org/10.1093/molehr/gap080
    [Crossref] [Google Scholar]
  141. 141.
    Ahmed EA, Scherthan H, de Rooij DG. 2015.. DNA double strand break response and limited repair capacity in mouse elongated spermatids. . Int. J. Mol. Sci. 16::29923–35. https://doi.org/10.3390/ijms161226214
    [Crossref] [Google Scholar]
  142. 142.
    Cavé T, Desmarais R, Lacombe-Burgoyne C, Boissonneault G. 2019.. Genetic instability and chromatin remodeling in spermatids. . Genes 10::40. https://doi.org/10.3390/genes10010040
    [Crossref] [Google Scholar]
  143. 143.
    Garagna S, Page J, Fernandez-Donoso R, Zuccotti M, Searle JB. 2014.. The Robertsonian phenomenon in the house mouse: mutation, meiosis and speciation. . Chromosoma 123::529–44. https://doi.org/10.1007/s00412-014-0477-6
    [Crossref] [Google Scholar]
  144. 144.
    Jones K. 1998.. Robertsonian fusion and centric fission in karyotype evolution of higher plants. . Bot. Rev. 64::273–89. https://doi.org/10.1007/BF02856567
    [Crossref] [Google Scholar]
  145. 145.
    Capilla L, Medarde N, Alemany-Schmidt A, Oliver-Bonet M, Ventura J, Ruiz-Herrera A. 2014.. Genetic recombination variation in wild Robertsonian mice: on the role of chromosomal fusions and Prdm9 allelic background. . Proc. R. Soc. B 281::20140297. https://doi.org/10.1098/rspb.2014.0297
    [Crossref] [Google Scholar]
  146. 146.
    Berríos S, Manieu C, López Fenner J, Ayarza E, Page J, et al. 2013.. Robertsonian chromosomes and the nuclear architecture of mouse meiotic prophase spermatocytes. . Biol. Res. 47::16. https://doi.org/10.1186/0717-6287-47-16
    [Crossref] [Google Scholar]
  147. 147.
    Farré M, Micheletti D, Ruiz-Herrera A. 2013.. Recombination rates and genomic shuffling in human and chimpanzee—a new twist in the chromosomal speciation theory. . Mol. Biol. Evol. 30::853–64. https://doi.org/10.1093/molbev/mss272
    [Crossref] [Google Scholar]
  148. 148.
    Gregory T. 2024.. Animal genome size database. http://www.genomesize.com
    [Google Scholar]
/content/journals/10.1146/annurev-animal-111523-102233
Loading
Evolution of 3D Chromatin Folding
Annual Review of Animal Biosciences 13, 49 (2025); https://doi.org/10.1146/annurev-animal-111523-102233
/content/journals/10.1146/annurev-animal-111523-102233
/content/journals/10.1146/annurev-animal-111523-102233
Loading

Data & Media loading...

Supplemental Materials

  • Supplemental Table 1

file format download

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error