FAD2 Gene Radiation and Positive Selection Contributed to Polyacetylene Metabolism Evolution in Campanulids

Authors

Tao Feng, Wuhan Botanical Garden
Ya Yang, University of Minnesota - Twin Cities
Lucas Busta, University of Nebraska - LincolnFollow
Edgar B. Cahoon, University of Nebraska-LincolnFollow
Hengchang Wang, Wuhan Botanical Garden
Shiyou Lü, Hubei UniversityFollow

ORCID IDs

0000-0002-0489-2021 (T.Feng)

0000-0002-0102-9986 (L.Busta)

0000-0002-7277-1176 (E.B.Cahoon);

0000-0003-0449-2471 (S.Lü).

Document Type

Article

Date of this Version

2019

Citation

Plant Physiology, October 2019, Vol. 181, pp. 714–728, www.plantphysiol.org

doi 10.1104/pp.19.00800

Comments

Copyright 2019 American Society of Plant Biologists. All Rights Reserved.

Link goes to free access version at publisher site.

Abstract

Polyacetylenes (PAs) are bioactive, specialized plant defense compounds produced by some species in the eudicot clade campanulids. Early steps of PA biosynthesis are catalyzed by Fatty Acid Desaturase 2 (FAD2). Canonical FAD2s catalyze desaturation, but divergent forms can catalyze hydroxylation, conjugation, acetylenation, and epoxygenation. These alternate reactions give rise to valuable unusual fatty acids, including the precursors to PAs. The extreme functional diversity of FAD2 enzymes and the origin of PA biosynthesis are poorly understood from an evolutionary perspective. We focus here on the evolution of the FAD2 gene family. We uncovered a core eudicot-wide gene duplication event giving rise to two lineages: FAD2- a and FAD2-b. Independent neofunctionalizations in both lineages have resulted in functionally diverse FAD2-LIKEs involved in unusual fatty acid biosynthesis. We found significantly accelerated rates of molecular evolution in FAD2-LIKEs and use this metric to provide a list of uncharacterized candidates for further exploration of FAD2 functional diversity. FAD2-a has expanded extensively in Asterales and Apiales, two main clades of campanulids, by ancient gene duplications. Here, we detected positive selection in both Asterales and Apiales lineages, which may have enabled the evolution of PA metabolism in campanulids. Together, these findings also imply that yet uncharacterized FAD2-a copies are involved in later steps of PA biosynthesis. This work establishes a robust phylogenetic framework in which to interpret functional data and to direct future research into the origin and evolution of PA metabolism.