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Chromosome-level genome assembly of Ophiorrhiza pumila reveals the evolution of camptothecin biosynthesis

Author

Listed:
  • Amit Rai

    (Chiba University
    Chiba University
    RIKEN Center for Sustainable Resource Science)

  • Hideki Hirakawa

    (Kazusa DNA Research Institute)

  • Ryo Nakabayashi

    (RIKEN Center for Sustainable Resource Science)

  • Shinji Kikuchi

    (Chiba University
    Chiba University)

  • Koki Hayashi

    (Chiba University)

  • Megha Rai

    (Chiba University)

  • Hiroshi Tsugawa

    (RIKEN Center for Sustainable Resource Science
    RIKEN Center for Integrative Medical Sciences)

  • Taiki Nakaya

    (Chiba University)

  • Tetsuya Mori

    (RIKEN Center for Sustainable Resource Science)

  • Hideki Nagasaki

    (Kazusa DNA Research Institute)

  • Runa Fukushi

    (Chiba University)

  • Yoko Kusuya

    (Chiba University)

  • Hiroki Takahashi

    (Chiba University
    Chiba University)

  • Hiroshi Uchiyama

    (Nihon University)

  • Atsushi Toyoda

    (National Institute of Genetics)

  • Shoko Hikosaka

    (Chiba University
    Chiba University)

  • Eiji Goto

    (Chiba University
    Chiba University)

  • Kazuki Saito

    (Chiba University
    Chiba University
    RIKEN Center for Sustainable Resource Science)

  • Mami Yamazaki

    (Chiba University
    Chiba University)

Abstract

Plant genomes remain highly fragmented and are often characterized by hundreds to thousands of assembly gaps. Here, we report chromosome-level reference and phased genome assembly of Ophiorrhiza pumila, a camptothecin-producing medicinal plant, through an ordered multi-scaffolding and experimental validation approach. With 21 assembly gaps and a contig N50 of 18.49 Mb, Ophiorrhiza genome is one of the most complete plant genomes assembled to date. We also report 273 nitrogen-containing metabolites, including diverse monoterpene indole alkaloids (MIAs). A comparative genomics approach identifies strictosidine biogenesis as the origin of MIA evolution. The emergence of strictosidine biosynthesis-catalyzing enzymes precede downstream enzymes’ evolution post γ whole-genome triplication, which occurred approximately 110 Mya in O. pumila, and before the whole-genome duplication in Camptotheca acuminata identified here. Combining comparative genome analysis, multi-omics analysis, and metabolic gene-cluster analysis, we propose a working model for MIA evolution, and a pangenome for MIA biosynthesis, which will help in establishing a sustainable supply of camptothecin.

Suggested Citation

  • Amit Rai & Hideki Hirakawa & Ryo Nakabayashi & Shinji Kikuchi & Koki Hayashi & Megha Rai & Hiroshi Tsugawa & Taiki Nakaya & Tetsuya Mori & Hideki Nagasaki & Runa Fukushi & Yoko Kusuya & Hiroki Takahas, 2021. "Chromosome-level genome assembly of Ophiorrhiza pumila reveals the evolution of camptothecin biosynthesis," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-020-20508-2
    DOI: 10.1038/s41467-020-20508-2
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    Cited by:

    1. Xiaofei Yang & Shenghan Gao & Li Guo & Bo Wang & Yanyan Jia & Jian Zhou & Yizhuo Che & Peng Jia & Jiadong Lin & Tun Xu & Jianyong Sun & Kai Ye, 2021. "Three chromosome-scale Papaver genomes reveal punctuated patchwork evolution of the morphinan and noscapine biosynthesis pathway," Nature Communications, Nature, vol. 12(1), pages 1-14, December.

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