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

Nature Communications, vol. 12, pp. 6030

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.

Authors 11

  1. First Affiliated Hospital of Xi'an Jiaotong University · Xi'an Jiaotong University

    Affiliation as printed

    Genome Institute, The First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, Shaanxi, China

    MOE Key Lab for Intelligent Networks & Networks Security, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China

    School of Computer Science and Technology, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China

    School of Computer Science and Technology, Faculty of Electronic and Information Engineering, Xi’an Jiaotong University, Xi’an, Shaanxi, China

  2. Xi'an Jiaotong University

    Affiliation as printed

    MOE Key Lab for Intelligent Networks & Networks Security, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China

    School of Automation Science and Engineering, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China

    MOE Key Lab for Intelligent Networks & Networks Security, Faculty of Electronic and Information Engineering, Xi’an Jiaotong University, Xi’an, Shaanxi, China

  3. Xi'an Jiaotong University

    Affiliation as printed

    MOE Key Lab for Intelligent Networks & Networks Security, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China

    School of Automation Science and Engineering, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China

    School of Life Science and Technology, Xi'an Jiaotong University, Xi'an, Shaanxi, China

    MOE Key Lab for Intelligent Networks & Networks Security, Faculty of Electronic and Information Engineering, Xi’an Jiaotong University, Xi’an, Shaanxi, China

  4. Xi'an Jiaotong University

    Affiliation as printed

    School of Automation Science and Engineering, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China

    School of Automation Science and Engineering, Faculty of Electronic and Information Engineering, Xi’an Jiaotong University, Xi’an, Shaanxi, China

  5. Xi'an Jiaotong University

    Affiliation as printed

    School of Automation Science and Engineering, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China

    School of Automation Science and Engineering, Faculty of Electronic and Information Engineering, Xi’an Jiaotong University, Xi’an, Shaanxi, China

  6. Henan Normal University

    Affiliation as printed

    College of Life Sciences, Henan Normal University, Xinxiang, Henan, China

  7. Xi'an Jiaotong University

    Affiliation as printed

    MOE Key Lab for Intelligent Networks & Networks Security, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China

    School of Automation Science and Engineering, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China

    MOE Key Lab for Intelligent Networks & Networks Security, Faculty of Electronic and Information Engineering, Xi’an Jiaotong University, Xi’an, Shaanxi, China

  8. Xi'an Jiaotong University

    Affiliation as printed

    MOE Key Lab for Intelligent Networks & Networks Security, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China

    School of Automation Science and Engineering, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China

    School of Automation Science and Engineering, Faculty of Electronic and Information Engineering, Xi’an Jiaotong University, Xi’an, Shaanxi, China

  9. Leiden University · Xi'an Jiaotong University

    Affiliation as printed

    Faculty of Science, Leiden University, Leiden, The Netherlands

    MOE Key Lab for Intelligent Networks & Networks Security, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China

    School of Automation Science and Engineering, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China

    MOE Key Lab for Intelligent Networks & Networks Security, Faculty of Electronic and Information Engineering, Xi’an Jiaotong University, Xi’an, Shaanxi, China

  10. Xi'an Jiaotong University

    Affiliation as printed

    MOE Key Lab for Intelligent Networks & Networks Security, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China

    School of Automation Science and Engineering, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China

    MOE Key Lab for Intelligent Networks & Networks Security, Faculty of Electronic and Information Engineering, Xi’an Jiaotong University, Xi’an, Shaanxi, China

  11. Leiden University · First Affiliated Hospital of Xi'an Jiaotong University · Xi'an Jiaotong University

    Affiliation as printed

    Faculty of Science, Leiden University, Leiden, The Netherlands. kaiye@xjtu.edu.cn

    Genome Institute, The First Affiliated Hospital of Xi'an Jiaotong University, Xi'an, Shaanxi, China. kaiye@xjtu.edu.cn

    MOE Key Lab for Intelligent Networks & Networks Security, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China. kaiye@xjtu.edu.cn

    School of Automation Science and Engineering, Faculty of Electronic and Information Engineering, Xi'an Jiaotong University, Xi'an, Shaanxi, China. kaiye@xjtu.edu.cn

    School of Life Science and Technology, Xi'an Jiaotong University, Xi'an, Shaanxi, China. kaiye@xjtu.edu.cn

    Genome Institute, The First Affiliated Hospital of Xi’an Jiaotong University, Xi’an, Shaanxi, China

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References 117