IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38560-z.html
   My bibliography  Save this article

Transposon signatures of allopolyploid genome evolution

Author

Listed:
  • Adam M. Session

    (University of California
    US Department of Energy Joint Genome Institute
    Binghamton University)

  • Daniel S. Rokhsar

    (University of California
    US Department of Energy Joint Genome Institute
    Okinawa Institute for Science and Technology Graduate University
    Chan Zuckerberg BioHub)

Abstract

Hybridization brings together chromosome sets from two or more distinct progenitor species. Genome duplication associated with hybridization, or allopolyploidy, allows these chromosome sets to persist as distinct subgenomes during subsequent meioses. Here, we present a general method for identifying the subgenomes of a polyploid based on shared ancestry as revealed by the genomic distribution of repetitive elements that were active in the progenitors. This subgenome-enriched transposable element signal is intrinsic to the polyploid, allowing broader applicability than other approaches that depend on the availability of sequenced diploid relatives. We develop the statistical basis of the method, demonstrate its applicability in the well-studied cases of tobacco, cotton, and Brassica napus, and apply it to several cases: allotetraploid cyprinids, allohexaploid false flax, and allooctoploid strawberry. These analyses provide insight into the origins of these polyploids, revise the subgenome identities of strawberry, and provide perspective on subgenome dominance in higher polyploids.

Suggested Citation

  • Adam M. Session & Daniel S. Rokhsar, 2023. "Transposon signatures of allopolyploid genome evolution," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38560-z
    DOI: 10.1038/s41467-023-38560-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38560-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-38560-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. Sean P. Gordon & Bruno Contreras-Moreira & Daniel P. Woods & David L. Des Marais & Diane Burgess & Shengqiang Shu & Christoph Stritt & Anne C. Roulin & Wendy Schackwitz & Ludmila Tyler & Joel Martin &, 2017. "Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
    2. Guohong Albert Wu & Chikatoshi Sugimoto & Hideyasu Kinjo & Chika Azama & Fumimasa Mitsube & Manuel Talon & Frederick G. Gmitter & Daniel S. Rokhsar, 2021. "Diversification of mandarin citrus by hybrid speciation and apomixis," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    3. 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.
    4. Therese Mitros & Adam M. Session & Brandon T. James & Guohong Albert Wu & Mohammad B. Belaffif & Lindsay V. Clark & Shengqiang Shu & Hongxu Dong & Adam Barling & Jessica R. Holmes & Jessica E. Mattick, 2020. "Genome biology of the paleotetraploid perennial biomass crop Miscanthus," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    5. John E. Bowers & Brad A. Chapman & Junkang Rong & Andrew H. Paterson, 2003. "Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events," Nature, Nature, vol. 422(6930), pages 433-438, March.
    6. 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.
    7. Sateesh Kagale & Chushin Koh & John Nixon & Venkatesh Bollina & Wayne E. Clarke & Reetu Tuteja & Charles Spillane & Stephen J. Robinson & Matthew G. Links & Carling Clarke & Erin E. Higgins & Terry Hu, 2014. "The emerging biofuel crop Camelina sativa retains a highly undifferentiated hexaploid genome structure," Nature Communications, Nature, vol. 5(1), pages 1-11, September.
    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. John T. Lovell & Alice H. MacQueen & Sujan Mamidi & Jason Bonnette & Jerry Jenkins & Joseph D. Napier & Avinash Sreedasyam & Adam Healey & Adam Session & Shengqiang Shu & Kerrie Barry & Stacy Bonos & , 2021. "Genomic mechanisms of climate adaptation in polyploid bioenergy switchgrass," Nature, Nature, vol. 590(7846), pages 438-444, February.
    10. 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.
    11. Sean P. Gordon & Bruno Contreras-Moreira & Joshua J. Levy & Armin Djamei & Angelika Czedik-Eysenberg & Virginia S. Tartaglio & Adam Session & Joel Martin & Amy Cartwright & Andrew Katz & Vasanth R. Si, 2020. "Gradual polyploid genome evolution revealed by pan-genomic analysis of Brachypodium hybridum and its diploid progenitors," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Chao Fang & Ning Jiang & Scott J. Teresi & Adrian E. Platts & Gaurav Agarwal & Chad Niederhuth & Patrick P. Edger & Jiming Jiang, 2024. "Dynamics of accessible chromatin regions and subgenome dominance in octoploid strawberry," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

    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. José Cerca & Bent Petersen & José Miguel Lazaro-Guevara & Angel Rivera-Colón & Siri Birkeland & Joel Vizueta & Siyu Li & Qionghou Li & João Loureiro & Chatchai Kosawang & Patricia Jaramillo Díaz & Gon, 2022. "The genomic basis of the plant island syndrome in Darwin’s giant daisies," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. 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.
    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. 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.
    6. Xiao Feng & Qipian Chen & Weihong Wu & Jiexin Wang & Guohong Li & Shaohua Xu & Shao Shao & Min Liu & Cairong Zhong & Chung-I Wu & Suhua Shi & Ziwen He, 2024. "Genomic evidence for rediploidization and adaptive evolution following the whole-genome triplication," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    7. Yanting Shen & Wanying Li & Ying Zeng & Zhipeng Li & Yiqiong Chen & Jixiang Zhang & Hong Zhao & Lingfang Feng & Dongming Ma & Xiaolu Mo & Puyue Ouyang & Lili Huang & Zheng Wang & Yuannian Jiao & Hong-, 2022. "Chromosome-level and haplotype-resolved genome provides insight into the tetraploid hybrid origin of patchouli," Nature Communications, Nature, vol. 13(1), pages 1-15, 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. 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.
    10. Chow-Lih Yew & Takashi Tsuchimatsu & Rie Shimizu-Inatsugi & Shinsuke Yasuda & Masaomi Hatakeyama & Hiroyuki Kakui & Takuma Ohta & Keita Suwabe & Masao Watanabe & Seiji Takayama & Kentaro K. Shimizu, 2023. "Dominance in self-compatibility between subgenomes of allopolyploid Arabidopsis kamchatica shown by transgenic restoration of self-incompatibility," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    11. Tiziana Maria Sirangelo & Richard Andrew Ludlow & Tatiana Chenet & Luisa Pasti & Natasha Damiana Spadafora, 2023. "Multi-Omics and Genome Editing Studies on Plant Cell Walls to Improve Biomass Quality," Agriculture, MDPI, vol. 13(4), pages 1-19, March.
    12. 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.
    13. Dadong Dai & Chuanshuai Xie & Yayi Zhou & Dexin Bo & Shurong Zhang & Shengqiang Mao & Yucheng Liao & Simeng Cui & Zhaolu Zhu & Xueyu Wang & Fanling Li & Donghai Peng & Jinshui Zheng & Ming Sun, 2023. "Unzipped chromosome-level genomes reveal allopolyploid nematode origin pattern as unreduced gamete hybridization," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    14. Thao Nguyen & Eli J. Costa & Tim Deibert & Jose Reyes & Felix C. Keber & Miroslav Tomschik & Michael Stadlmeier & Meera Gupta & Chirag K. Kumar & Edward R. Cruz & Amanda Amodeo & Jesse C. Gatlin & Mar, 2022. "Differential nuclear import sets the timing of protein access to the embryonic genome," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    15. 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.
    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. Sainger, Manish & Jaiwal, Anjali & Sainger, Poonam Ahlawat & Chaudhary, Darshna & Jaiwal, Ranjana & Jaiwal, Pawan K., 2017. "Advances in genetic improvement of Camelina sativa for biofuel and industrial bio-products," Renewable and Sustainable Energy Reviews, Elsevier, vol. 68(P1), pages 623-637.
    18. Aiping Song & Jiangshuo Su & Haibin Wang & Zhongren Zhang & Xingtan Zhang & Yves Peer & Fei Chen & Weimin Fang & Zhiyong Guan & Fei Zhang & Zhenxing Wang & Likai Wang & Baoqing Ding & Shuang Zhao & Li, 2023. "Analyses of a chromosome-scale genome assembly reveal the origin and evolution of cultivated chrysanthemum," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    19. 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.
    20. Reiko Akiyama & Takao Goto & Toshiaki Tameshige & Jiro Sugisaka & Ken Kuroki & Jianqiang Sun & Junichi Akita & Masaomi Hatakeyama & Hiroshi Kudoh & Tanaka Kenta & Aya Tonouchi & Yuki Shimahara & Jun S, 2023. "Seasonal pigment fluctuation in diploid and polyploid Arabidopsis revealed by machine learning-based phenotyping method PlantServation," Nature Communications, Nature, vol. 14(1), pages 1-16, 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_s41467-023-38560-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.