Emergence of terpene cyclization in Artemisia annua

Melissa Salmon, Caroline Laurendon, Maria Vardakou, Jitender Cheema, Marianne Defernez, Sol Green, Juan A. Faraldos and Paul E. O’Maille ()
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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

Nature Communications, 2015, vol. 6, issue 1, 1-10

Abstract: 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.

Date: 2015
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DOI: 10.1038/ncomms7143

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