IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43740-y.html
   My bibliography  Save this article

Maternal dominance contributes to subgenome differentiation in allopolyploid fishes

Author

Listed:
  • Min-Rui-Xuan Xu

    (Jiujiang University)

  • Zhen-Yang Liao

    (Chinese Academy of Agricultural Sciences)

  • Jordan R. Brock

    (Michigan State University)

  • Kang Du

    (Texas State University)

  • Guo-Yin Li

    (Zhoukou Normal University)

  • Zhi-Qiang Chen

    (Glbizzia Biosciences)

  • Ying-Hao Wang

    (Chinese Academy of Agricultural Sciences)

  • Zhong-Nan Gao

    (Jiujiang University)

  • Gaurav Agarwal

    (Michigan State University)

  • Kevin H-C Wei

    (University of California Berkeley
    University of British Columbia)

  • Feng Shao

    (Southwest University, School of Life Sciences)

  • Shuai Pang

    (Glbizzia Biosciences)

  • Adrian E. Platts

    (Michigan State University)

  • Jozefien Velde

    (Max Planck Institute for Plant Breeding Research)

  • Hong-Min Lin

    (Jiujiang University)

  • Scott J. Teresi

    (Michigan State University)

  • Kevin Bird

    (Michigan State University)

  • Chad E. Niederhuth

    (Michigan State University)

  • Jin-Gen Xu

    (Jiujiang Academy of Agricultural Sciences)

  • Guo-Hua Yu

    (Jiujiang University)

  • Jian-Yuan Yang

    (Jiujiang University)

  • Si-Fa Dai

    (Jiujiang University)

  • Andrew Nelson

    (Boyce Thompson Institute)

  • Ingo Braasch

    (Michigan State University)

  • Xiao-Gu Zhang

    (Jiujiang University)

  • Manfred Schartl

    (Texas State University
    University of Würzburg)

  • Patrick P. Edger

    (Michigan State University)

  • Min-Jin Han

    (Southwest University)

  • Hua-Hao Zhang

    (Jiujiang University)

Abstract

Teleost fishes, which are the largest and most diverse group of living vertebrates, have a rich history of ancient and recent polyploidy. Previous studies of allotetraploid common carp and goldfish (cyprinids) reported a dominant subgenome, which is more expressed and exhibits biased gene retention. However, the underlying mechanisms contributing to observed ‘subgenome dominance’ remains poorly understood. Here we report high-quality genomes of twenty-one cyprinids to investigate the origin and subsequent subgenome evolution patterns following three independent allopolyploidy events. We identify the closest extant relatives of the diploid progenitor species, investigate genetic and epigenetic differences among subgenomes, and conclude that observed subgenome dominance patterns are likely due to a combination of maternal dominance and transposable element densities in each polyploid. These findings provide an important foundation to understanding subgenome dominance patterns observed in teleost fishes, and ultimately the role of polyploidy in contributing to evolutionary innovations.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43740-y
    DOI: 10.1038/s41467-023-43740-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43740-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-43740-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. Jesse R. Dixon & Inkyung Jung & Siddarth Selvaraj & Yin Shen & Jessica E. Antosiewicz-Bourget & Ah Young Lee & Zhen Ye & Audrey Kim & Nisha Rajagopal & Wei Xie & Yarui Diao & Jing Liang & Huimin Zhao , 2015. "Chromatin architecture reorganization during stem cell differentiation," Nature, Nature, vol. 518(7539), pages 331-336, February.
    2. 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.
    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. 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.
    5. 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.
    6. Yuannian Jiao & Norman J. Wickett & Saravanaraj Ayyampalayam & André S. Chanderbali & Lena Landherr & Paula E. Ralph & Lynn P. Tomsho & Yi Hu & Haiying Liang & Pamela S. Soltis & Douglas E. Soltis & S, 2011. "Ancestral polyploidy in seed plants and angiosperms," Nature, Nature, vol. 473(7345), pages 97-100, May.
    7. 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.
    8. Robert VanBuren & Ching Man Wai & Xuewen Wang & Jeremy Pardo & Alan E. Yocca & Hao Wang & Srinivasa R. Chaluvadi & Guomin Han & Douglas Bryant & Patrick P. Edger & Joachim Messing & Mark E. Sorrells &, 2020. "Exceptional subgenome stability and functional divergence in the allotetraploid Ethiopian cereal teff," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    9. 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.
    10. Yun Sung Cho & Li Hu & Haolong Hou & Hang Lee & Jiaohui Xu & Soowhan Kwon & Sukhun Oh & Hak-Min Kim & Sungwoong Jho & Sangsoo Kim & Young-Ah Shin & Byung Chul Kim & Hyunmin Kim & Chang-uk Kim & Shu-Ji, 2013. "The tiger genome and comparative analysis with lion and snow leopard genomes," Nature Communications, Nature, vol. 4(1), pages 1-7, December.
    11. Camille Berthelot & Frédéric Brunet & Domitille Chalopin & Amélie Juanchich & Maria Bernard & Benjamin Noël & Pascal Bento & Corinne Da Silva & Karine Labadie & Adriana Alberti & Jean-Marc Aury & Alex, 2014. "The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates," Nature Communications, Nature, vol. 5(1), pages 1-10, May.
    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. Adam M. Session & Daniel S. Rokhsar, 2023. "Transposon signatures of allopolyploid genome evolution," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. Ivelin Iliev Rizov, 2016. "European Coexistence Bureau (ECoB) - Best Practice Document for coexistence of genetically modified cotton with conventional and organic farming," JRC Research Reports JRC101485, Joint Research Centre.
    9. Haomiao Yu & Yuan Yuan & Sijiao Wang & Guoming Wu & Haishen Xu & Jianglan Wei & Le Ju & Yulin Huang & Hui Chen, 2021. "Interspecies Evolution and Networks Investigation of the Auxin Response Protein (AUX/IAA) Family Reveals the Adaptation Mechanisms of Halophytes Crops in Nitrogen Starvation Agroecological Environment," Agriculture, MDPI, vol. 11(8), pages 1-23, August.
    10. Ryuichiro Nakato & Toyonori Sakata & Jiankang Wang & Luis Augusto Eijy Nagai & Yuya Nagaoka & Gina Miku Oba & Masashige Bando & Katsuhiko Shirahige, 2023. "Context-dependent perturbations in chromatin folding and the transcriptome by cohesin and related factors," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    11. Khalid H. Bhat & Saurabh Priyadarshi & Sarah Naiyer & Xinyan Qu & Hammad Farooq & Eden Kleiman & Jeffery Xu & Xue Lei & Jose F. Cantillo & Robert Wuerffel & Nicole Baumgarth & Jie Liang & Ann J. Feene, 2023. "An Igh distal enhancer modulates antigen receptor diversity by determining locus conformation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    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. Andre S. Chanderbali & Lingling Jin & Qiaoji Xu & Yue Zhang & Jingbo Zhang & Shuguang Jian & Emily Carroll & David Sankoff & Victor A. Albert & Dianella G. Howarth & Douglas E. Soltis & Pamela S. Solt, 2022. "Buxus and Tetracentron genomes help resolve eudicot genome history," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    14. 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.
    15. Julia Minderjahn & Alexander Fischer & Konstantin Maier & Karina Mendes & Margit Nuetzel & Johanna Raithel & Hanna Stanewsky & Ute Ackermann & Robert Månsson & Claudia Gebhard & Michael Rehli, 2022. "Postmitotic differentiation of human monocytes requires cohesin-structured chromatin," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    16. Xiaowen Shi & Hua Yang & Chen Chen & Jie Hou & Tieming Ji & Jianlin Cheng & James A. Birchler, 2022. "Dosage-sensitive miRNAs trigger modulation of gene expression during genomic imbalance in maize," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    17. Abhijit Chakraborty & Jeffrey G. Wang & Ferhat Ay, 2022. "dcHiC detects differential compartments across multiple Hi-C datasets," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    18. Fei Shen & Shixiao Xu & Qi Shen & Changwei Bi & Martin A. Lysak, 2023. "The allotetraploid horseradish genome provides insights into subgenome diversification and formation of critical traits," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    19. Pedro Madrigal & Siwei Deng & Yuliang Feng & Stefania Militi & Kim Jee Goh & Reshma Nibhani & Rodrigo Grandy & Anna Osnato & Daniel Ortmann & Stephanie Brown & Siim Pauklin, 2023. "Epigenetic and transcriptional regulations prime cell fate before division during human pluripotent stem cell differentiation," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    20. 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.

    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_s41467-023-43740-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.