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

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 Takahashi, Hiroshi Uchiyama, Atsushi Toyoda, Shoko Hikosaka, Eiji Goto, Kazuki Saito and Mami Yamazaki ()
Additional contact information
Amit Rai: Chiba University
Hideki Hirakawa: Kazusa DNA Research Institute
Ryo Nakabayashi: RIKEN Center for Sustainable Resource Science
Shinji Kikuchi: Chiba University
Koki Hayashi: Chiba University
Megha Rai: Chiba University
Hiroshi Tsugawa: RIKEN Center for Sustainable Resource Science
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
Hiroshi Uchiyama: Nihon University
Atsushi Toyoda: National Institute of Genetics
Shoko Hikosaka: Chiba University
Eiji Goto: Chiba University
Kazuki Saito: Chiba University
Mami Yamazaki: Chiba University

Nature Communications, 2021, vol. 12, issue 1, 1-19

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-020-20508-2

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