IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-022-34828-y.html
   My bibliography  Save this article

Comparative analysis of genome-scale, base-resolution DNA methylation profiles across 580 animal species

Author

Listed:
  • Johanna Klughammer

    (CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences
    Ludwig-Maximilians-Universität München)

  • Daria Romanovskaia

    (CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences)

  • Amelie Nemc

    (CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences)

  • Annika Posautz

    (University of Veterinary Medicine Vienna)

  • Charlotte A. Seid

    (Northeastern University Marine Science Center)

  • Linda C. Schuster

    (CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences)

  • Melissa C. Keinath

    (University of Kentucky)

  • Juan Sebastian Lugo Ramos

    (Max Planck Institute for Evolutionary Biology)

  • Lindsay Kosack

    (CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences)

  • Ann Evankow

    (Northeastern University Marine Science Center)

  • Dieter Printz

    (St. Anna Kinderkrebsforschung)

  • Stefanie Kirchberger

    (St. Anna Kinderkrebsforschung)

  • Bekir Ergüner

    (CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences)

  • Paul Datlinger

    (CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences)

  • Nikolaus Fortelny

    (CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences)

  • Christian Schmidl

    (CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences)

  • Matthias Farlik

    (CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences)

  • Kaja Skjærven

    (Institute of Marine Research (IMR))

  • Andreas Bergthaler

    (CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences
    Medical University of Vienna, Center for Pathophysiology Infectiology and Immunology, Institute of Hygiene and Applied Immunology)

  • Miriam Liedvogel

    (Max Planck Institute for Evolutionary Biology
    Institute of Avian Research, An der Vogelwarte)

  • Denise Thaller

    (University of Veterinary Medicine Vienna)

  • Pamela A. Burger

    (University of Veterinary Medicine Vienna)

  • Marcela Hermann

    (Department of Medical Biochemistry)

  • Martin Distel

    (St. Anna Kinderkrebsforschung)

  • Daniel L. Distel

    (Northeastern University Marine Science Center)

  • Anna Kübber-Heiss

    (University of Veterinary Medicine Vienna)

  • Christoph Bock

    (CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences
    Medical University of Vienna, Institute of Artificial Intelligence, Center for Medical Data Science)

Abstract

Methylation of cytosines is a prototypic epigenetic modification of the DNA. It has been implicated in various regulatory mechanisms across the animal kingdom and particularly in vertebrates. We mapped DNA methylation in 580 animal species (535 vertebrates, 45 invertebrates), resulting in 2443 genome-scale DNA methylation profiles of multiple organs. Bioinformatic analysis of this large dataset quantified the association of DNA methylation with the underlying genomic DNA sequence throughout vertebrate evolution. We observed a broadly conserved link with two major transitions—once in the first vertebrates and again with the emergence of reptiles. Cross-species comparisons focusing on individual organs supported a deeply conserved association of DNA methylation with tissue type, and cross-mapping analysis of DNA methylation at gene promoters revealed evolutionary changes for orthologous genes. In summary, this study establishes a large resource of vertebrate and invertebrate DNA methylomes, it showcases the power of reference-free epigenome analysis in species for which no reference genomes are available, and it contributes an epigenetic perspective to the study of vertebrate evolution.

Suggested Citation

  • Johanna Klughammer & Daria Romanovskaia & Amelie Nemc & Annika Posautz & Charlotte A. Seid & Linda C. Schuster & Melissa C. Keinath & Juan Sebastian Lugo Ramos & Lindsay Kosack & Ann Evankow & Dieter , 2023. "Comparative analysis of genome-scale, base-resolution DNA methylation profiles across 580 animal species," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-022-34828-y
    DOI: 10.1038/s41467-022-34828-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-34828-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-34828-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Veronika N. Laine & Toni I. Gossmann & Kyle M. Schachtschneider & Colin J. Garroway & Ole Madsen & Koen J. F. Verhoeven & Victor de Jager & Hendrik-Jan Megens & Wesley C. Warren & Patrick Minx & Richa, 2016. "Evolutionary signals of selection on cognition from the great tit genome and methylome," Nature Communications, Nature, vol. 7(1), pages 1-9, April.
    2. Christoph Bock & Martina Paulsen & Sascha Tierling & Thomas Mikeska & Thomas Lengauer & Jörn Walter, 2006. "CpG Island Methylation in Human Lymphocytes Is Highly Correlated with DNA Sequence, Repeats, and Predicted DNA Structure," PLOS Genetics, Public Library of Science, vol. 2(3), pages 1-10, March.
    3. Matthew D. Schultz & Yupeng He & John W. Whitaker & Manoj Hariharan & Eran A. Mukamel & Danny Leung & Nisha Rajagopal & Joseph R. Nery & Mark A. Urich & Huaming Chen & Shin Lin & Yiing Lin & Inkyung J, 2015. "Human body epigenome maps reveal noncanonical DNA methylation variation," Nature, Nature, vol. 523(7559), pages 212-216, July.
    4. Adam M. Session & Yoshinobu Uno & Taejoon Kwon & Jarrod A. Chapman & Atsushi Toyoda & Shuji Takahashi & Akimasa Fukui & Akira Hikosaka & Atsushi Suzuki & Mariko Kondo & Simon J. van Heeringen & Ian Qu, 2016. "Genome evolution in the allotetraploid frog Xenopus laevis," Nature, Nature, vol. 538(7625), pages 336-343, October.
    5. Alexander Meissner & Tarjei S. Mikkelsen & Hongcang Gu & Marius Wernig & Jacob Hanna & Andrey Sivachenko & Xiaolan Zhang & Bradley E. Bernstein & Chad Nusbaum & David B. Jaffe & Andreas Gnirke & Rudol, 2008. "Genome-scale DNA methylation maps of pluripotent and differentiated cells," Nature, Nature, vol. 454(7205), pages 766-770, August.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Min-Rui-Xuan Xu & Zhen-Yang Liao & Jordan R. Brock & Kang Du & Guo-Yin Li & Zhi-Qiang Chen & Ying-Hao Wang & Zhong-Nan Gao & Gaurav Agarwal & Kevin H-C Wei & Feng Shao & Shuai Pang & Adrian E. Platts , 2023. "Maternal dominance contributes to subgenome differentiation in allopolyploid fishes," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    2. Qiang Zhang & Sai Ma & Zhengzhi Liu & Bohan Zhu & Zirui Zhou & Gaoshan Li & J. Javier Meana & Javier González-Maeso & Chang Lu, 2023. "Droplet-based bisulfite sequencing for high-throughput profiling of single-cell DNA methylomes," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    3. Camilla S. Colding-Christensen & Ellen S. Kakulidis & Javier Arroyo-Gomez & Ivo A. Hendriks & Connor Arkinson & Zita Fábián & Agnieszka Gambus & Niels Mailand & Julien P. Duxin & Michael L. Nielsen, 2023. "Profiling ubiquitin signalling with UBIMAX reveals DNA damage- and SCFβ-Trcp1-dependent ubiquitylation of the actin-organizing protein Dbn1," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    4. Jinling Zhang & Xuebin Zhu & Yuhong Li & Lingyan Zhu & Shiming Li & Guoying Zheng & Qi Ren & Yonghong Xiao & Fumin Feng, 2016. "Correlation of CpG Island Methylation of the Cytochrome P450 2E1/2D6 Genes with Liver Injury Induced by Anti-Tuberculosis Drugs: A Nested Case-Control Study," IJERPH, MDPI, vol. 13(8), pages 1-9, August.
    5. Jessen V. Bredeson & Austin B. Mudd & Sofia Medina-Ruiz & Therese Mitros & Owen Kabnick Smith & Kelly E. Miller & Jessica B. Lyons & Sanjit S. Batra & Joseph Park & Kodiak C. Berkoff & Christopher Plo, 2024. "Conserved chromatin and repetitive patterns reveal slow genome evolution in frogs," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    6. Iryna Ivasyk & Leonora Olivos-Cisneros & Stephany Valdés-Rodríguez & Marie Droual & Hosung Jang & Robert J. Schmitz & Daniel J. C. Kronauer, 2023. "DNMT1 mutant ants develop normally but have disrupted oogenesis," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    7. Maria Moiron & Kimberley J. Mathot & Niels J. Dingemanse, 2016. "A multi-level approach to quantify speed-accuracy trade-offs in great tits (Parus major)," Behavioral Ecology, International Society for Behavioral Ecology, vol. 27(5), pages 1539-1546.
    8. Heiner Kuhl & Kang Du & Manfred Schartl & Lukáš Kalous & Matthias Stöck & Dunja K. Lamatsch, 2022. "Equilibrated evolution of the mixed auto-/allopolyploid haplotype-resolved genome of the invasive hexaploid Prussian carp," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    9. Zhen Huang & Ivanete De O. Furo & Jing Liu & Valentina Peona & Anderson J. B. Gomes & Wan Cen & Hao Huang & Yanding Zhang & Duo Chen & Ting Xue & Qiujin Zhang & Zhicao Yue & Quanxi Wang & Lingyu Yu & , 2022. "Recurrent chromosome reshuffling and the evolution of neo-sex chromosomes in parrots," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    10. Sandhya Malla & Kanchan Kumari & Carlos A. García-Prieto & Jonatan Caroli & Anna Nordin & Trinh T. T. Phan & Devi Prasad Bhattarai & Carlos Martinez-Gamero & Eshagh Dorafshan & Stephanie Stransky & Da, 2024. "The scaffolding function of LSD1 controls DNA methylation in mouse ESCs," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    11. Amir D. Hay & Noah J. Kessler & Daniel Gebert & Nozomi Takahashi & Hugo Tavares & Felipe K. Teixeira & Anne C. Ferguson-Smith, 2023. "Epigenetic inheritance is unfaithful at intermediately methylated CpG sites," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    12. Olga A. Balashova & Alexios A. Panoutsopoulos & Olesya Visina & Jacob Selhub & Paul S. Knoepfler & Laura N. Borodinsky, 2024. "Noncanonical function of folate through folate receptor 1 during neural tube formation," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    13. Andrea L Liebl & Jeff S Wesner & Andrew F Russell & Aaron W Schrey, 2021. "Methylation patterns at fledging predict delayed dispersal in a cooperatively breeding bird," PLOS ONE, Public Library of Science, vol. 16(6), pages 1-13, June.
    14. Adam M. Session & Daniel S. Rokhsar, 2023. "Transposon signatures of allopolyploid genome evolution," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    15. Anthony K. Redmond & Dearbhaile Casey & Manu Kumar Gundappa & Daniel J. Macqueen & Aoife McLysaght, 2023. "Independent rediploidization masks shared whole genome duplication in the sturgeon-paddlefish ancestor," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    16. Yurika Matsui & Mohamed Nadhir Djekidel & Katherine Lindsay & Parimal Samir & Nina Connolly & Gang Wu & Xiaoyang Yang & Yiping Fan & Beisi Xu & Jamy C. Peng, 2023. "SNIP1 and PRC2 coordinate cell fates of neural progenitors during brain development," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    17. Fang Liu & Eivind Tøstesen & Jostein K Sundet & Tor-Kristian Jenssen & Christoph Bock & Geir Ivar Jerstad & William G Thilly & Eivind Hovig, 2007. "The Human Genomic Melting Map," PLOS Computational Biology, Public Library of Science, vol. 3(5), pages 1-13, May.
    18. Jamie L. Endicott & Paula A. Nolte & Hui Shen & Peter W. Laird, 2022. "Cell division drives DNA methylation loss in late-replicating domains in primary human cells," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    19. Yinwen Zhang & Hosung Jang & Rui Xiao & Ioanna Kakoulidou & Robert S. Piecyk & Frank Johannes & Robert J. Schmitz, 2021. "Heterochromatin is a quantitative trait associated with spontaneous epiallele formation," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    20. John K. Barrows & Baicheng Lin & Colleen E. Quaas & George Fullbright & Elizabeth N. Wallace & David T. Long, 2022. "BRD4 promotes resection and homology-directed repair of DNA double-strand breaks," Nature Communications, Nature, vol. 13(1), pages 1-10, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-022-34828-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.