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Formation and diversification of a paradigm biosynthetic gene cluster in plants

Author

Listed:
  • Zhenhua Liu

    (John Innes Centre)

  • Jitender Cheema

    (John Innes Centre)

  • Marielle Vigouroux

    (John Innes Centre)

  • Lionel Hill

    (John Innes Centre)

  • James Reed

    (John Innes Centre)

  • Pirita Paajanen

    (John Innes Centre)

  • Levi Yant

    (University of Nottingham)

  • Anne Osbourn

    (John Innes Centre)

Abstract

Numerous examples of biosynthetic gene clusters (BGCs), including for compounds of agricultural and medicinal importance, have now been discovered in plant genomes. However, little is known about how these complex traits are assembled and diversified. Here, we examine a large number of variants within and between species for a paradigm BGC (the thalianol cluster), which has evolved recently in a common ancestor of the Arabidopsis genus. Comparisons at the species level reveal differences in BGC organization and involvement of auxiliary genes, resulting in production of species-specific triterpenes. Within species, the thalianol cluster is primarily fixed, showing a low frequency of deleterious haplotypes. We further identify chromosomal inversion as a molecular mechanism that may shuffle more distant genes into the cluster, so enabling cluster compaction. Antagonistic natural selection pressures are likely involved in shaping the occurrence and maintenance of this BGC. Our work sheds light on the birth, life and death of complex genetic and metabolic traits in plants.

Suggested Citation

  • Zhenhua Liu & Jitender Cheema & Marielle Vigouroux & Lionel Hill & James Reed & Pirita Paajanen & Levi Yant & Anne Osbourn, 2020. "Formation and diversification of a paradigm biosynthetic gene cluster in plants," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-19153-6
    DOI: 10.1038/s41467-020-19153-6
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    Cited by:

    1. Xin-Cheng Huang & Huanying Tang & Xuefen Wei & Yuedong He & Shuaiya Hu & Jia-Yi Wu & Dingqiao Xu & Fei Qiao & Jia-Yu Xue & Yucheng Zhao, 2024. "The gradual establishment of complex coumarin biosynthetic pathway in Apiaceae," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. 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.
    3. 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.
    4. 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.
    5. 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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