Evolution of a Secondary Metabolic Pathway from Primary Metabolism: Shikimate and quinate biosynthesis in plants
Date
2018-06
Authors
Carrington, Yuriko
Guo, Jia
Le, Cuong H.
Fillo, Alexander
Kwon, Junsu
Tran, Lan T.
Ehlting, Jurgen
Journal Title
Journal ISSN
Volume Title
Publisher
the Plant Journal
Abstract
The shikimate pathway synthesizes aromatic amino acids essential for protein biosynthesis. Shikimate dehydrogenase (SDH) is a central enzyme of this primary metabolic pathway, producing shikimate. The structurally similar quinate is a secondary metabolite synthesized by quinate dehydrogenase (QDH). SDH and QDH belong to the same gene family, which diverged into two phylogenetic clades after a defining gene
duplication just prior to the angiosperm/gymnosperm split. Non-seed plants that diverged before this duplication harbour only a single gene of this family. Extant representatives from the chlorophytes (Chlamydomonas reinhardtii), bryophytes (Physcomitrella patens) and lycophytes (Selaginella moellendorfii) encoded almost exclusively SDH activity in vitro. A reconstructed ancestral sequence representing the node just prior to the gene duplication also encoded SDH activity. Quinate dehydrogenase activity was gained only in seed plants following gene duplication. Quinate dehydrogenases of gymnosperms, represented here by Pinus taeda, may be reminiscent of an evolutionary intermediate since they encode equal SDH and QDH
activities. The second copy in P. taeda maintained specificity for shikimate similar to the activity found in the angiosperm SDH sister clade. The codon for a tyrosine residue within the active site displayed a signature of positive selection at the node defining the QDH clade, where it changed to a glycine. Replacing the tyrosine with a glycine in a highly shikimate-specific angiosperm SDH was sufficient to gain some QDH function. Thus, very few mutations were necessary to facilitate the evolution of QDH genes.
Description
Keywords
molecular evolution, secondary metabolism, shikimate/quinate dehydrogenase, Rhodopirellula baltica, Chlamydomonas reinhardtii, Physcomitrella patens, Selaginella moellendorfii, Pinus taeda, Populus trichocarpa
Citation
Carrington, Y., Guo, J., Le, C.H., Fillo, A., Kwon, J., Tran, L.T. & Ehlting, J. (2018). Evolution of a secondary metabolic pathway from primary metabolism: shikimate and quinate biosynthesis in plants. The Plant Journal, 95(5), 823-833. https://doi.org/10.1111/tpj.13990