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Three chromosome-scale Papaver genomes reveal punctuated patchwork evolution of the morphinan and noscapine biosynthesis pathway

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  • Xiaofei Yang

    (Xi’an Jiaotong University
    Xi’an Jiaotong University
    The First Affiliated Hospital of Xi’an Jiaotong University)

  • Shenghan Gao

    (Xi’an Jiaotong University
    Xi’an Jiaotong University)

  • Li Guo

    (Xi’an Jiaotong University
    Xi’an Jiaotong University
    Xi’an Jiaotong University)

  • Bo Wang

    (Xi’an Jiaotong University)

  • Yanyan Jia

    (Xi’an Jiaotong University)

  • Jian Zhou

    (Henan Normal University)

  • Yizhuo Che

    (Xi’an Jiaotong University
    Xi’an Jiaotong University)

  • Peng Jia

    (Xi’an Jiaotong University
    Xi’an Jiaotong University)

  • Jiadong Lin

    (Xi’an Jiaotong University
    Xi’an Jiaotong University
    Leiden University)

  • Tun Xu

    (Xi’an Jiaotong University
    Xi’an Jiaotong University)

  • Jianyong Sun

    (Xi’an Jiaotong University)

  • Kai Ye

    (Xi’an Jiaotong University
    The First Affiliated Hospital of Xi’an Jiaotong University
    Xi’an Jiaotong University
    Xi’an Jiaotong University)

Abstract

For millions of years, plants evolve plenty of structurally diverse secondary metabolites (SM) to support their sessile lifestyles through continuous biochemical pathway innovation. While new genes commonly drive the evolution of plant SM pathway, how a full biosynthetic pathway evolves remains poorly understood. The evolution of pathway involves recruiting new genes along the reaction cascade forwardly, backwardly, or in a patchwork manner. With three chromosome-scale Papaver genome assemblies, we here reveal whole-genome duplications (WGDs) apparently accelerate chromosomal rearrangements with a nonrandom distribution towards SM optimization. A burst of structural variants involving fusions, translocations and duplications within 7.7 million years have assembled nine genes into the benzylisoquinoline alkaloids gene cluster, following a punctuated patchwork model. Biosynthetic gene copies and their total expression matter to morphinan production. Our results demonstrate how new genes have been recruited from a WGD-induced repertoire of unregulated enzymes with promiscuous reactivities to innovate efficient metabolic pathways with spatiotemporal constraint.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26330-8
    DOI: 10.1038/s41467-021-26330-8
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    1. Fangyuan Zhang & Fei Qiu & Junlan Zeng & Zhichao Xu & Yueli Tang & Tengfei Zhao & Yuqin Gou & Fei Su & Shiyi Wang & Xiuli Sun & Zheyong Xue & Weixing Wang & Chunxian Yang & Lingjiang Zeng & Xiaozhong , 2023. "Revealing evolution of tropane alkaloid biosynthesis by analyzing two genomes in the Solanaceae family," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Xiaofei Yang & Shenghan Gao & Tun Xu & Bo Wang & Yanyan Jia & Kai Ye, 2023. "Reply to “Subgenome-aware analyses suggest a reticulate allopolyploidization origin in three Papaver genomes”," Nature Communications, Nature, vol. 14(1), pages 1-2, December.
    3. Theresa Catania & Yi Li & Thilo Winzer & David Harvey & Fergus Meade & Anna Caridi & Andrew Leech & Tony R. Larson & Zemin Ning & Jiyang Chang & Yves Peer & Ian A. Graham, 2022. "A functionally conserved STORR gene fusion in Papaver species that diverged 16.8 million years ago," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    4. Ren-Gang Zhang & Chaoxia Lu & Guang-Yuan Li & Jie Lv & Longxin Wang & Zhao-Xuan Wang & Zhe Chen & Dan Liu & Ye Zhao & Tian-Le Shi & Wei Zhang & Zhao-Hui Tang & Jian-Feng Mao & Yong-Peng Ma & Kai-Hua J, 2023. "Subgenome-aware analyses suggest a reticulate allopolyploidization origin in three Papaver genomes," Nature Communications, Nature, vol. 14(1), pages 1-6, December.
    5. 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.
    6. Jiadong Hu & Shi Qiu & Feiyan Wang & Qing Li & Chun-Lei Xiang & Peng Di & Ziding Wu & Rui Jiang & Jinxing Li & Zhen Zeng & Jing Wang & Xingxing Wang & Yuchen Zhang & Shiyuan Fang & Yuqi Qiao & Jie Din, 2023. "Functional divergence of CYP76AKs shapes the chemodiversity of abietane-type diterpenoids in genus Salvia," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    7. Abigail E. Bryson & Emily R. Lanier & Kin H. Lau & John P. Hamilton & Brieanne Vaillancourt & Davis Mathieu & Alan E. Yocca & Garret P. Miller & Patrick P. Edger & C. Robin Buell & Björn Hamberger, 2023. "Uncovering a miltiradiene biosynthetic gene cluster in the Lamiaceae reveals a dynamic evolutionary trajectory," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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