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Emergence of terpene cyclization in Artemisia annua

Author

Listed:
  • Melissa Salmon

    (John Innes Centre, Norwich Research Park)

  • Caroline Laurendon

    (John Innes Centre, Norwich Research Park)

  • Maria Vardakou

    (John Innes Centre, Norwich Research Park)

  • Jitender Cheema

    (John Innes Centre, Computational and Systems Biology, Norwich Research Park)

  • Marianne Defernez

    (Institute of Food Research, Analytical Sciences Unit, Norwich Research Park)

  • Sol Green

    (Plant and Food Research, 120 Mt Albert Road, Sandringham)

  • Juan A. Faraldos

    (School of Chemistry, Cardiff University)

  • Paul E. O’Maille

    (John Innes Centre, Norwich Research Park
    Institute of Food Research, Food & Health Programme, Norwich Research Park)

Abstract

The emergence of terpene cyclization was critical to the evolutionary expansion of chemical diversity yet remains unexplored. Here we report the first discovery of an epistatic network of residues that controls the onset of terpene cyclization in Artemisia annua. We begin with amorpha-4,11-diene synthase (ADS) and (E)-β-farnesene synthase (BFS), a pair of terpene synthases that produce cyclic or linear terpenes, respectively. A library of ~27,000 enzymes is generated by breeding combinations of natural amino-acid substitutions from the cyclic into the linear producer. We discover one dominant mutation is sufficient to activate cyclization, and together with two additional residues comprise a network of strongly epistatic interactions that activate, suppress or reactivate cyclization. Remarkably, this epistatic network of equivalent residues also controls cyclization in a BFS homologue from Citrus junos. Fitness landscape analysis of mutational trajectories provides quantitative insights into a major epoch in specialized metabolism.

Suggested Citation

  • Melissa Salmon & Caroline Laurendon & Maria Vardakou & Jitender Cheema & Marianne Defernez & Sol Green & Juan A. Faraldos & Paul E. O’Maille, 2015. "Emergence of terpene cyclization in Artemisia annua," Nature Communications, Nature, vol. 6(1), pages 1-10, May.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms7143
    DOI: 10.1038/ncomms7143
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    Cited by:

    1. Janani Durairaj & Elena Melillo & Harro J Bouwmeester & Jules Beekwilder & Dick de Ridder & Aalt D J van Dijk, 2021. "Integrating structure-based machine learning and co-evolution to investigate specificity in plant sesquiterpene synthases," PLOS Computational Biology, Public Library of Science, vol. 17(3), pages 1-21, March.

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