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

Xiaofei Yang, Shenghan Gao, Li Guo, Bo Wang, Yanyan Jia, Jian Zhou, Yizhuo Che, Peng Jia, Jiadong Lin, Tun Xu, Jianyong Sun and Kai Ye ()
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Xiaofei Yang: Xi’an Jiaotong University
Shenghan Gao: Xi’an Jiaotong University
Li Guo: 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
Peng Jia: Xi’an Jiaotong University
Jiadong Lin: Xi’an Jiaotong University
Tun Xu: Xi’an Jiaotong University
Jianyong Sun: Xi’an Jiaotong University
Kai Ye: Xi’an Jiaotong University

Nature Communications, 2021, vol. 12, issue 1, 1-14

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-021-26330-8

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