IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-46080-7.html
   My bibliography  Save this article

Genomic evidence for rediploidization and adaptive evolution following the whole-genome triplication

Author

Listed:
  • Xiao Feng

    (Sun Yat-sen University)

  • Qipian Chen

    (Sun Yat-sen University
    Chinese Academy of Agricultural Sciences)

  • Weihong Wu

    (Sun Yat-sen University)

  • Jiexin Wang

    (Sun Yat-sen University)

  • Guohong Li

    (Sun Yat-sen University)

  • Shaohua Xu

    (Sun Yat-sen University)

  • Shao Shao

    (Sun Yat-sen University)

  • Min Liu

    (Sun Yat-sen University)

  • Cairong Zhong

    (Hainan Academy of Forestry (Hainan Academy of Mangrove))

  • Chung-I Wu

    (Sun Yat-sen University)

  • Suhua Shi

    (Sun Yat-sen University)

  • Ziwen He

    (Sun Yat-sen University)

Abstract

Whole-genome duplication (WGD), or polyploidy, events are widespread and significant in the evolutionary history of angiosperms. However, empirical evidence for rediploidization, the major process where polyploids give rise to diploid descendants, is still lacking at the genomic level. Here we present chromosome-scale genomes of the mangrove tree Sonneratia alba and the related inland plant Lagerstroemia speciosa. Their common ancestor has experienced a whole-genome triplication (WGT) approximately 64 million years ago coinciding with a period of dramatic global climate change. Sonneratia, adapting mangrove habitats, experienced extensive chromosome rearrangements post-WGT. We observe the WGT retentions display sequence and expression divergence, suggesting potential neo- and sub-functionalization. Strong selection acting on three-copy retentions indicates adaptive value in response to new environments. To elucidate the role of ploidy changes in genome evolution, we improve a model of the polyploidization–rediploidization process based on genomic evidence, contributing to the understanding of adaptive evolution during climate change.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46080-7
    DOI: 10.1038/s41467-024-46080-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-46080-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-46080-7?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. 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. Lichan Tu & Ping Su & Zhongren Zhang & Linhui Gao & Jiadian Wang & Tianyuan Hu & Jiawei Zhou & Yifeng Zhang & Yujun Zhao & Yuan Liu & Yadi Song & Yuru Tong & Yun Lu & Jian Yang & Cao Xu & Meirong Jia , 2020. "Genome of Tripterygium wilfordii and identification of cytochrome P450 involved in triptolide biosynthesis," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    3. Enrique Ibarra-Laclette & Eric Lyons & Gustavo Hernández-Guzmán & Claudia Anahí Pérez-Torres & Lorenzo Carretero-Paulet & Tien-Hao Chang & Tianying Lan & Andreanna J. Welch & María Jazmín Abraham Juár, 2013. "Architecture and evolution of a minute plant genome," Nature, Nature, vol. 498(7452), pages 94-98, June.
    4. Yuzhou Zhang & Guanghui Xiao & Xiaojuan Wang & Xixi Zhang & Jiří Friml, 2019. "Evolution of fast root gravitropism in seed plants," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    5. Guiling Sun & Yuxing Xu & Hui Liu & Ting Sun & Jingxiong Zhang & Christian Hettenhausen & Guojing Shen & Jinfeng Qi & Yan Qin & Jing Li & Lei Wang & Wei Chang & Zhenhua Guo & Ian T. Baldwin & Jianqian, 2018. "Large-scale gene losses underlie the genome evolution of parasitic plant Cuscuta australis," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
    6. Jeremy Schmutz & Steven B. Cannon & Jessica Schlueter & Jianxin Ma & Therese Mitros & William Nelson & David L. Hyten & Qijian Song & Jay J. Thelen & Jianlin Cheng & Dong Xu & Uffe Hellsten & Gregory , 2010. "Genome sequence of the palaeopolyploid soybean," Nature, Nature, vol. 463(7278), pages 178-183, January.
    7. Anna M. Selmecki & Yosef E. Maruvka & Phillip A. Richmond & Marie Guillet & Noam Shoresh & Amber L. Sorenson & Subhajyoti De & Roy Kishony & Franziska Michor & Robin Dowell & David Pellman, 2015. "Polyploidy can drive rapid adaptation in yeast," Nature, Nature, vol. 519(7543), pages 349-352, March.
    8. Liangsheng Zhang & Fei Chen & Xingtan Zhang & Zhen Li & Yiyong Zhao & Rolf Lohaus & Xiaojun Chang & Wei Dong & Simon Y. W. Ho & Xing Liu & Aixia Song & Junhao Chen & Wenlei Guo & Zhengjia Wang & Yingy, 2020. "The water lily genome and the early evolution of flowering plants," Nature, Nature, vol. 577(7788), pages 79-84, January.
    9. Alexander A. Myburg & Dario Grattapaglia & Gerald A. Tuskan & Uffe Hellsten & Richard D. Hayes & Jane Grimwood & Jerry Jenkins & Erika Lindquist & Hope Tice & Diane Bauer & David M. Goodstein & Inna D, 2014. "The genome of Eucalyptus grandis," Nature, Nature, vol. 510(7505), pages 356-362, June.
    10. 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.
    11. 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.
    12. James C. Zachos & Gerald R. Dickens & Richard E. Zeebe, 2008. "An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics," Nature, Nature, vol. 451(7176), pages 279-283, January.
    13. Jeremy Schmutz & Steven B. Cannon & Jessica Schlueter & Jianxin Ma & Therese Mitros & William Nelson & David L. Hyten & Qijian Song & Jay J. Thelen & Jianlin Cheng & Dong Xu & Uffe Hellsten & Gregory , 2010. "Erratum: Genome sequence of the palaeopolyploid soybean," Nature, Nature, vol. 465(7294), pages 120-120, May.
    14. Lichan Tu & Ping Su & Zhongren Zhang & Linhui Gao & Jiadian Wang & Tianyuan Hu & Jiawei Zhou & Yifeng Zhang & Yujun Zhao & Yuan Liu & Yadi Song & Yuru Tong & Yun Lu & Jian Yang & Cao Xu & Meirong Jia , 2020. "Author Correction: Genome of Tripterygium wilfordii and identification of cytochrome P450 involved in triptolide biosynthesis," Nature Communications, Nature, vol. 11(1), pages 1-1, December.
    15. Tegan Armarego-Marriott, 2020. "Doubled genome an asset," Nature Climate Change, Nature, vol. 10(3), pages 184-184, March.
    16. Kirsten E Eilertson & James G Booth & Carlos D Bustamante, 2012. "SnIPRE: Selection Inference Using a Poisson Random Effects Model," PLOS Computational Biology, Public Library of Science, vol. 8(12), pages 1-14, December.
    17. Bo Liu & Jian Yan & Weihua Li & Lijuan Yin & Ping Li & Hanxia Yu & Longsheng Xing & Minling Cai & Hengchao Wang & Mengxin Zhao & Jin Zheng & Feng Sun & Zhenzhen Wang & Zhaoyang Jiang & Qiaojing Ou & S, 2020. "Mikania micrantha genome provides insights into the molecular mechanism of rapid growth," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    18. Shengyi Liu & Yumei Liu & Xinhua Yang & Chaobo Tong & David Edwards & Isobel A. P. Parkin & Meixia Zhao & Jianxin Ma & Jingyin Yu & Shunmou Huang & Xiyin Wang & Junyi Wang & Kun Lu & Zhiyuan Fang & Ia, 2014. "The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes," Nature Communications, Nature, vol. 5(1), pages 1-11, September.
    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. Justine K. Kitony & Kelly Colt & Bradley W. Abramson & Nolan T. Hartwick & Semar Petrus & Emadeldin H. E. Konozy & Nisa Karimi & Levi Yant & Todd P. Michael, 2024. "Chromosome-level baobab genome illuminates its evolutionary trajectory and environmental adaptation," 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. David Wickell & Li-Yaung Kuo & Hsiao-Pei Yang & Amra Dhabalia Ashok & Iker Irisarri & Armin Dadras & Sophie de Vries & Jan de Vries & Yao-Moan Huang & Zheng Li & Michael S. Barker & Nolan T. Hartwick , 2021. "Underwater CAM photosynthesis elucidated by Isoetes genome," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    2. 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.
    3. Hai Anh Tran & Hyun Jo & Thi Cuc Nguyen & Jeong-Dong Lee & Hak Soo Seo & Jong Tae Song, 2024. "Genome-Wide Association Analysis for Submergence Tolerance at the Early Vegetative and Germination Stages in Wild Soybean ( Glycine soja )," Agriculture, MDPI, vol. 14(9), pages 1-17, September.
    4. Yukari Nagatoshi & Kenta Ikazaki & Yasufumi Kobayashi & Nobuyuki Mizuno & Ryohei Sugita & Yumiko Takebayashi & Mikiko Kojima & Hitoshi Sakakibara & Natsuko I. Kobayashi & Keitaro Tanoi & Kenichiro Fuj, 2023. "Phosphate starvation response precedes abscisic acid response under progressive mild drought in plants," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Octavio R. Salazar & Ke Chen & Vanessa J. Melino & Muppala P. Reddy & Eva Hřibová & Jana Čížková & Denisa Beránková & Juan Pablo Arciniegas Vega & Lina María Cáceres Leal & Manuel Aranda & Lukasz Jare, 2024. "SOS1 tonoplast neo-localization and the RGG protein SALTY are important in the extreme salinity tolerance of Salicornia bigelovii," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    6. Wolfgang Goettel & Hengyou Zhang & Ying Li & Zhenzhen Qiao & He Jiang & Dianyun Hou & Qijian Song & Vincent R. Pantalone & Bao-Hua Song & Deyue Yu & Yong-qiang Charles An, 2022. "POWR1 is a domestication gene pleiotropically regulating seed quality and yield in soybean," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    7. Shichen Li & Zhihui Sun & Qing Sang & Chao Qin & Lingping Kong & Xin Huang & Huan Liu & Tong Su & Haiyang Li & Milan He & Chao Fang & Lingshuang Wang & Shuangrong Liu & Bin Liu & Baohui Liu & Xiangdon, 2023. "Soybean reduced internode 1 determines internode length and improves grain yield at dense planting," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    8. Isaac Njaci & Bernice Waweru & Nadia Kamal & Meki Shehabu Muktar & David Fisher & Heidrun Gundlach & Collins Muli & Lucy Muthui & Mary Maranga & Davies Kiambi & Brigitte L. Maass & Peter M. F. Emmrich, 2023. "Chromosome-level genome assembly and population genomic resource to accelerate orphan crop lablab breeding," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    9. 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.
    10. Jerzy H. Czembor & Elzbieta Czembor & Marcin Krystek & Juliusz Pukacki, 2023. "AgroGenome: Interactive Genomic-Based Web Server Developed Based on Data Collected for Accessions Stored in Polish Genebank," Agriculture, MDPI, vol. 13(1), pages 1-16, January.
    11. Adam M. Session & Daniel S. Rokhsar, 2023. "Transposon signatures of allopolyploid genome evolution," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    12. Nikolaj Lervad Hansen & Louise Kjaerulff & Quinn Kalby Heck & Victor Forman & Dan Staerk & Birger Lindberg Møller & Johan Andersen-Ranberg, 2022. "Tripterygium wilfordii cytochrome P450s catalyze the methyl shift and epoxidations in the biosynthesis of triptonide," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    13. Weidong Wang & Liyang Chen & Kevin Fengler & Joy Bolar & Victor Llaca & Xutong Wang & Chancelor B. Clark & Tomara J. Fleury & Jon Myrvold & David Oneal & Maria Magdalena Dyk & Ashley Hudson & Jesse Mu, 2021. "A giant NLR gene confers broad-spectrum resistance to Phytophthora sojae in soybean," Nature Communications, Nature, vol. 12(1), pages 1-8, December.
    14. Jiaqi Sun & Shiyu Huang & Qing Lu & Shuo Li & Shizhen Zhao & Xiaojian Zheng & Qian Zhou & Wenxiao Zhang & Jie Li & Lili Wang & Ke Zhang & Wenyu Zheng & Xianzhong Feng & Baohui Liu & Fanjiang Kong & Fe, 2023. "UV-B irradiation-activated E3 ligase GmILPA1 modulates gibberellin catabolism to increase plant height in soybean," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    15. Yifeng Zhang & Jie Gao & Lin Ma & Lichan Tu & Tianyuan Hu & Xiaoyi Wu & Ping Su & Yujun Zhao & Yuan Liu & Dan Li & Jiawei Zhou & Yan Yin & Yuru Tong & Huan Zhao & Yun Lu & Jiadian Wang & Wei Gao & Luq, 2023. "Tandemly duplicated CYP82Ds catalyze 14-hydroxylation in triptolide biosynthesis and precursor production in Saccharomyces cerevisiae," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    16. Jessen V. Bredeson & Jessica B. Lyons & Ibukun O. Oniyinde & Nneka R. Okereke & Olufisayo Kolade & Ikenna Nnabue & Christian O. Nwadili & Eva Hřibová & Matthew Parker & Jeremiah Nwogha & Shengqiang Sh, 2022. "Chromosome evolution and the genetic basis of agronomically important traits in greater yam," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    17. Aron Park & Se-Hee Kang & Byeong-Hee Kang & Sreeparna Chowdhury & Seo-Young Shin & Won-Ho Lee & Jeong-Dong Lee & Sungwoo Lee & Yu-Mi Choi & Bo-Keun Ha, 2023. "Identification of a Novel KTi-1 Allele Associated with Reduced Trypsin Inhibitor Activity in Soybean Accessions," Agriculture, MDPI, vol. 13(11), pages 1-14, October.
    18. Rahul Kumar & Prashant Swapnil & Mukesh Meena & Shweta Selpair & Bal Govind Yadav, 2022. "Plant Growth-Promoting Rhizobacteria (PGPR): Approaches to Alleviate Abiotic Stresses for Enhancement of Growth and Development of Medicinal Plants," Sustainability, MDPI, vol. 14(23), pages 1-16, November.
    19. Wei Sun & Qinggang Yin & Huihua Wan & Ranran Gao & Chao Xiong & Chong Xie & Xiangxiao Meng & Yaolei Mi & Xiaotong Wang & Caixia Wang & Weiqiang Chen & Ziyan Xie & Zheyong Xue & Hui Yao & Peng Sun & Xu, 2023. "Characterization of the horse chestnut genome reveals the evolution of aescin and aesculin biosynthesis," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    20. Fei Shen & Yajuan Qin & Rui Wang & Xin Huang & Ying Wang & Tiangang Gao & Junna He & Yue Zhou & Yuannian Jiao & Jianhua Wei & Lei Li & Xiaozeng Yang, 2023. "Comparative genomics reveals a unique nitrogen-carbon balance system in Asteraceae," Nature Communications, Nature, vol. 14(1), pages 1-14, 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:15:y:2024:i:1:d:10.1038_s41467-024-46080-7. 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.