IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38714-z.html
   My bibliography  Save this article

Independent rediploidization masks shared whole genome duplication in the sturgeon-paddlefish ancestor

Author

Listed:
  • Anthony K. Redmond

    (Smurfit Institute of Genetics, Trinity College Dublin)

  • Dearbhaile Casey

    (Smurfit Institute of Genetics, Trinity College Dublin)

  • Manu Kumar Gundappa

    (The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh)

  • Daniel J. Macqueen

    (The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh)

  • Aoife McLysaght

    (Smurfit Institute of Genetics, Trinity College Dublin)

Abstract

Whole genome duplication (WGD) is a dramatic evolutionary event generating many new genes and which may play a role in survival through mass extinctions. Paddlefish and sturgeon are sister lineages that both show genomic evidence for ancient WGD. Until now this has been interpreted as two independent WGD events due to a preponderance of duplicate genes with independent histories. Here we show that although there is indeed a plurality of apparently independent gene duplications, these derive from a shared genome duplication event occurring well over 200 million years ago, likely close to the Permian-Triassic mass extinction period. This was followed by a prolonged process of reversion to stable diploid inheritance (rediploidization), that may have promoted survival during the Triassic-Jurassic mass extinction. We show that the sharing of this WGD is masked by the fact that paddlefish and sturgeon lineage divergence occurred before rediploidization had proceeded even half-way. Thus, for most genes the resolution to diploidy was lineage-specific. Because genes are only truly duplicated once diploid inheritance is established, the paddlefish and sturgeon genomes are thus a mosaic of shared and non-shared gene duplications resulting from a shared genome duplication event.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38714-z
    DOI: 10.1038/s41467-023-38714-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38714-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-38714-z?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. Byrappa Venkatesh & Alison P. Lee & Vydianathan Ravi & Ashish K. Maurya & Michelle M. Lian & Jeremy B. Swann & Yuko Ohta & Martin F. Flajnik & Yoichi Sutoh & Masanori Kasahara & Shawn Hoon & Vamshidha, 2014. "Elephant shark genome provides unique insights into gnathostome evolution," Nature, Nature, vol. 505(7482), pages 174-179, January.
    2. Kenneth H. Wolfe & Denis C. Shields, 1997. "Molecular evidence for an ancient duplication of the entire yeast genome," Nature, Nature, vol. 387(6634), pages 708-713, June.
    3. Devin R. Scannell & Kevin P. Byrne & Jonathan L. Gordon & Simon Wong & Kenneth H. Wolfe, 2006. "Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts," Nature, Nature, vol. 440(7082), pages 341-345, March.
    4. Anthony K. Redmond & Aoife McLysaght, 2021. "Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    5. Byrappa Venkatesh & Alison P. Lee & Vydianathan Ravi & Ashish K. Maurya & Michelle M. Lian & Jeremy B. Swann & Yuko Ohta & Martin F. Flajnik & Yoichi Sutoh & Masanori Kasahara & Shawn Hoon & Vamshidha, 2014. "Correction: Corrigendum: Elephant shark genome provides unique insights into gnathostome evolution," Nature, Nature, vol. 513(7519), pages 574-574, September.
    6. Yoichiro Nakatani & Prashant Shingate & Vydianathan Ravi & Nisha E. Pillai & Aravind Prasad & Aoife McLysaght & Byrappa Venkatesh, 2021. "Reconstruction of proto-vertebrate, proto-cyclostome and proto-gnathostome genomes provides new insights into early vertebrate evolution," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    7. Sigbjørn Lien & Ben F. Koop & Simen R. Sandve & Jason R. Miller & Matthew P. Kent & Torfinn Nome & Torgeir R. Hvidsten & Jong S. Leong & David R. Minkley & Aleksey Zimin & Fabian Grammes & Harald Grov, 2016. "The Atlantic salmon genome provides insights into rediploidization," Nature, Nature, vol. 533(7602), pages 200-205, May.
    8. 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.
    9. Peng Xu & Jian Xu & Guangjian Liu & Lin Chen & Zhixiong Zhou & Wenzhu Peng & Yanliang Jiang & Zixia Zhao & Zhiying Jia & Yonghua Sun & Yidi Wu & Baohua Chen & Fei Pu & Jianxin Feng & Jing Luo & Jing C, 2019. "The allotetraploid origin and asymmetrical genome evolution of the common carp Cyprinus carpio," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    10. Yi-Cun Chen & Zhen Li & Yun-Xiao Zhao & Ming Gao & Jie-Yu Wang & Ke-Wei Liu & Xue Wang & Li-Wen Wu & Yu-Lian Jiao & Zi-Long Xu & Wen-Guang He & Qi-Yan Zhang & Chieh-Kai Liang & Yu-Yun Hsiao & Di-Yang , 2020. "The Litsea genome and the evolution of the laurel family," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    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. Adam M. Session & Daniel S. Rokhsar, 2023. "Transposon signatures of allopolyploid genome evolution," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Yuuki Y. Watanabe & Nicholas L. Payne, 2023. "Thermal sensitivity of metabolic rate mirrors biogeographic differences between teleosts and elasmobranchs," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    4. Hong-Yan Wang & Jian-Yang Chen & Yanan Li & Xianghui Zhang & Xiang Liu & Yifang Lu & Hang He & Yubang Li & Hongxi Chen & Qun Liu & Yingyi Huang & Zhao Jia & Shuo Li & Yangqing Zhang & Shenglei Han & S, 2024. "Single-cell RNA sequencing illuminates the ontogeny, conservation and diversification of cartilaginous and bony fish lymphocytes," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    5. 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.
    6. Shan Nan Chen & Zhen Gan & Jing Hou & Yue Cong Yang & Lin Huang & Bei Huang & Su Wang & Pin Nie, 2022. "Identification and establishment of type IV interferon and the characterization of interferon-υ including its class II cytokine receptors IFN-υR1 and IL-10R2," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    7. Eduardo Vieira de Souza & Angie L. Bookout & Christopher A. Barnes & Brendan Miller & Pablo Machado & Luiz A. Basso & Cristiano V. Bizarro & Alan Saghatelian, 2024. "Rp3: Ribosome profiling-assisted proteogenomics improves coverage and confidence during microprotein discovery," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    8. 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.
    9. Pierre Genest & Léo Trespeuch, 2022. "Internet users’ perception about the impact of the pandemic on sports sponsorship [La perception des internautes face à l'impact de la pandémie sur le mécénat sportif]," Working Papers hal-03945701, HAL.
    10. J. Colgren & S. A. Nichols, 2022. "MRTF specifies a muscle-like contractile module in Porifera," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    11. Colizza, Vittoria & Flammini, Alessandro & Maritan, Amos & Vespignani, Alessandro, 2005. "Characterization and modeling of protein–protein interaction networks," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 352(1), pages 1-27.
    12. 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.
    13. Taikui Zhang & Weichen Huang & Lin Zhang & De-Zhu Li & Ji Qi & Hong Ma, 2024. "Phylogenomic profiles of whole-genome duplications in Poaceae and landscape of differential duplicate retention and losses among major Poaceae lineages," Nature Communications, Nature, vol. 15(1), pages 1-27, December.
    14. Ricard V. Solé & Romualdo Pastor-Satorras & Eric D. Smith & Thomas Kepler, 2001. "A Model of Large-Scale Proteome Evolution," Working Papers 01-08-041, Santa Fe Institute.
    15. Nathan V. Whelan & Kenneth M. Halanych, 2023. "Available data do not rule out Ctenophora as the sister group to all other Metazoa," Nature Communications, Nature, vol. 14(1), pages 1-3, December.
    16. 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.
    17. Liang Ma & Ke-Wei Liu & Zhen Li & Yu-Yun Hsiao & Yiying Qi & Tao Fu & Guang-Da Tang & Diyang Zhang & Wei-Hong Sun & Ding-Kun Liu & Yuanyuan Li & Gui-Zhen Chen & Xue-Die Liu & Xing-Yu Liao & Yu-Ting Ji, 2023. "Diploid and tetraploid genomes of Acorus and the evolution of monocots," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    18. Andreas Wagner, 2001. "The Yeast Protein Interaction Network Evolves Rapidly and Contains Few Redundant Duplicate Genes," Working Papers 01-04-022, Santa Fe Institute.
    19. Jianxiang Ma & Pengchuan Sun & Dandan Wang & Zhenyue Wang & Jiao Yang & Ying Li & Wenjie Mu & Renping Xu & Ying Wu & Congcong Dong & Nawal Shrestha & Jianquan Liu & Yongzhi Yang, 2021. "The Chloranthus sessilifolius genome provides insight into early diversification of angiosperms," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    20. Tsonis, Anastasios A & Heller, Fred L & Tsonis, Panagiotis A, 2002. "Probing the linearity and nonlinearity in DNA sequences," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 312(3), pages 458-468.

    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_s41467-023-38714-z. 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.