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Horseshoe crab genomes reveal the evolutionary fates of genes and microRNAs after three rounds (3R) of whole genome duplication

Wenyan Nong, Zhe Qu, Yiqian Li, Tom Barton-Owen, Annette Y.P. Wong, Ho Yin Yip, Hoi Ting Lee, Satya Narayana, Tobias Baril, Thomas Swale, Jianquan Cao, Ting Fung Chan, Hoi Shan Kwan, Ngai Sai Ming, Gianni Panagiotou, Pei-Yuan Qian, Jian-Wen Qiu, Kevin Y. Yip, Noraznawati Ismail, Siddhartha Pati, Akbar John, Stephen S. Tobe, William G. Bendena, Siu Gin Cheung, Alexander Hayward, Jerome H. L. Hui
doi: https://doi.org/10.1101/2020.04.16.045815
Wenyan Nong
1School of Life Sciences, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, China
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Zhe Qu
1School of Life Sciences, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, China
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Yiqian Li
1School of Life Sciences, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, China
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Tom Barton-Owen
1School of Life Sciences, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, China
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Annette Y.P. Wong
1School of Life Sciences, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, China
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Ho Yin Yip
1School of Life Sciences, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, China
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Hoi Ting Lee
1School of Life Sciences, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, China
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Satya Narayana
1School of Life Sciences, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, China
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Tobias Baril
2University of Exeter, United Kingdom
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Thomas Swale
3Dovetail Genomics, United States of America
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Jianquan Cao
1School of Life Sciences, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, China
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Ting Fung Chan
4State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong Kong, China
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Hoi Shan Kwan
5School of Life Sciences, The Chinese University of Hong Kong, China
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Ngai Sai Ming
4State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong Kong, China
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Gianni Panagiotou
6School of Biological Sciences, The University of Hong Kong, China
16Leibniz Institute of Natural Product Research and Infection Biology – Hans Knöll Institute. Jena, Germany
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Pei-Yuan Qian
7Department of Ocean Science and Hong Kong Branch of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Hong Kong University of Science and Technology, China
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Jian-Wen Qiu
8Department of Biology, Hong Kong Baptist University, China
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Kevin Y. Yip
9Department of Computer Science and Engineering, The Chinese University of Hong Kong, Hong Kong
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Noraznawati Ismail
10Institute of Marine Biotechnology, Universiti Malaysia Terengganu, Malaysia
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Siddhartha Pati
11Department of Bioscience and Biotechnology, Fakir Mohan University, Balasore, India
17Institute of Tropical Biodiversity and Sustainable Development, University Malaysia Terengganu, 20130 Kuala Nerus, Terengganu, Malaysia
18Research Division, Association for Biodiversity Conservation and Research (ABC), Odisha-756003, India
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Akbar John
12Institute of Oceanography and Maritime Studies (INOCEM), Kulliyyah of Science, International Islamic University, Malaysia
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Stephen S. Tobe
13Department of Cell and Systems Biology, University of Toronto, Canada
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William G. Bendena
14Department of Biology, Queen’s University, Canada
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Siu Gin Cheung
15Department of Chemistry, City University of Hong Kong, China
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Alexander Hayward
2University of Exeter, United Kingdom
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Jerome H. L. Hui
1School of Life Sciences, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, China
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  • For correspondence: jeromehui@cuhk.edu.hk
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Abstract

Whole genome duplication (WGD) has occurred in relatively few sexually reproducing invertebrates. Consequently, the WGD that occurred in the common ancestor of horseshoe crabs ~135 million years ago provides a rare opportunity to decipher the evolutionary consequences of a duplicated invertebrate genome. Here, we present a high-quality genome assembly for the mangrove horseshoe crab Carcinoscorpius rotundicauda (1.7Gb, N50 = 90.2Mb, with 89.8% sequences anchored to 16 pseudomolecules, 2n = 32), and a resequenced genome of the tri-spine horseshoe crab Tachypleus tridentatus (1.7Gb, N50 = 109.7Mb). Analyses of gene families, microRNAs, and synteny show that horseshoe crabs have undergone three rounds (3R) of WGD, and that these WGD events are shared with spiders. Comparison of the genomes of C. rotundicauda and T. tridentatus populations from several geographic locations further elucidates the diverse fates of both coding and noncoding genes. Together, the present study represents a cornerstone for a better understanding of the consequences of invertebrate WGD events on evolutionary fates of genes and microRNAs at individual and population levels, and highlights the genetic diversity with practical values for breeding programs and conservation of horseshoe crabs.

Competing Interest Statement

The authors have declared no competing interest.

  • List of abbreviations

    3R
    three rounds;
    WGD
    whole genome duplication;
    AUR
    arm usage ratio;
    OAP
    overall arm preference
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    Horseshoe crab genomes reveal the evolutionary fates of genes and microRNAs after three rounds (3R) of whole genome duplication
    Wenyan Nong, Zhe Qu, Yiqian Li, Tom Barton-Owen, Annette Y.P. Wong, Ho Yin Yip, Hoi Ting Lee, Satya Narayana, Tobias Baril, Thomas Swale, Jianquan Cao, Ting Fung Chan, Hoi Shan Kwan, Ngai Sai Ming, Gianni Panagiotou, Pei-Yuan Qian, Jian-Wen Qiu, Kevin Y. Yip, Noraznawati Ismail, Siddhartha Pati, Akbar John, Stephen S. Tobe, William G. Bendena, Siu Gin Cheung, Alexander Hayward, Jerome H. L. Hui
    bioRxiv 2020.04.16.045815; doi: https://doi.org/10.1101/2020.04.16.045815
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    Horseshoe crab genomes reveal the evolutionary fates of genes and microRNAs after three rounds (3R) of whole genome duplication
    Wenyan Nong, Zhe Qu, Yiqian Li, Tom Barton-Owen, Annette Y.P. Wong, Ho Yin Yip, Hoi Ting Lee, Satya Narayana, Tobias Baril, Thomas Swale, Jianquan Cao, Ting Fung Chan, Hoi Shan Kwan, Ngai Sai Ming, Gianni Panagiotou, Pei-Yuan Qian, Jian-Wen Qiu, Kevin Y. Yip, Noraznawati Ismail, Siddhartha Pati, Akbar John, Stephen S. Tobe, William G. Bendena, Siu Gin Cheung, Alexander Hayward, Jerome H. L. Hui
    bioRxiv 2020.04.16.045815; doi: https://doi.org/10.1101/2020.04.16.045815

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