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Transposon signatures of allopolyploid genome evolution

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  • 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
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    1. 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.
    2. 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.
    3. 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.
    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. 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.
    6. 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.
    7. 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.
    8. 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.
    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. 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.
    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.
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