Evolution of alternative biosynthetic pathways for vitamin C following plastid acquisition in photosynthetic eukaryotes

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Cite this article as: eLife 2015;4:e06369 doi: 10.7554/eLife.06369

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Abstract

Ascorbic acid (vitamin C) is an enzyme co-factor in eukaryotes that also plays a critical role in protecting photosynthetic eukaryotes against damaging reactive oxygen species derived from the chloroplast. Many animal lineages, including primates, have become ascorbate auxotrophs due to the loss of the terminal enzyme in their biosynthetic pathway, L-gulonolactone oxidase (GULO). The alternative pathways found in land plants and Euglena use a different terminal enzyme, L-galactonolactone dehydrogenase (GLDH). The evolutionary processes leading to these differing pathways and their contribution to the cellular roles of ascorbate remain unclear. Here we present molecular and biochemical evidence demonstrating that GULO was functionally replaced with GLDH in photosynthetic eukaryote lineages following plastid acquisition. GULO has therefore been lost repeatedly throughout eukaryote evolution. The formation of the alternative biosynthetic pathways in photosynthetic eukaryotes uncoupled ascorbate synthesis from hydrogen peroxide production and likely contributed to the rise of ascorbate as a major photoprotective antioxidant.

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Author details

Glen Wheeler

Marine Biological Association, Plymouth, United Kingdom

For correspondence
glw@mba.ac.uk

Competing interests
The authors declare that no competing interests exist.
Takahiro Ishikawa

Department of Life Science and Biotechnology, Shimane University, Matsue, Japan

Competing interests
The authors declare that no competing interests exist.
Varissa Pornsaksit

Department of Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Nicholas Smirnoff

Department of Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, United Kingdom

Competing interests
The authors declare that no competing interests exist.

Reviewing Editor

Joerg Bohlmann, University of British Columbia, Canada

Publication history

Received: January 7, 2015
Accepted: March 12, 2015
Accepted Manuscript published: March 13, 2015 (version 1)
Version of Record published: April 15, 2015 (version 2)

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.