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

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.DOI: http://dx.doi.org/10.7554/eLife.06369.001

Gigaspora margarita with and without its endobacterium shows adaptive responses to oxidative stress

“…Fungi synthesize a range of ascorbate analogues, including 6-deoxy-L-ascorbate, ascorbate glycosides, and the five-carbon analogue, D-erythroascorbate (Loewus 1999). However, molecular information on the involved genes is limited to yeast, and the description of the pathways leading to the different fungal ASC analogues is incomplete (Wheeler et al 2015). Since at least two enzymes, D-arabinono-1,4-lactone oxidase (ALO1) and L-gulonolactone oxidase (GULO), are known to be involved in ascorbate biosynthesis in fungi, as a first step we used TBLASTN to look for homologues in the transcriptome of R. irregularis (Tisserant et al 2013;Lin et al 2014) and of G. margarita (Salvioli et al2016).…”

“…In plants, ascorbate plays a critical role in protecting cells against damaging ROS produced by the chloroplast during photosynthesis (Wheeler et al 2015); however, our knowledge of the biosynthesis and role of ascorbate in fungi is much more limited. Fungi synthesize a range of ascorbate analogues, including 6-deoxy-L-ascorbate, ascorbate glycosides, and the five-carbon analogue, D-erythroascorbate (Loewus 1999).…”

Biochemistry and Physiology of Reactive Oxygen Species in Euglena

“…The enzyme ascorbate peroxidase (APX) was initially identified in E.gracilis, and given the EC number 1.11.1.11 on the basis of the detailed enzymological properties of this organism (Shigeoka et al 1980a, b). Thereafter, APX was found to be widely distributed in plants, eukaryotic algae, and protozoa that have acquired the ability to synthesize AsA (Asada 1992b;Shigeoka et al 2002;Wheeler et al 2015). As shown in Fig.…”

Integrative Approaches to Enhance Understanding of Plant Metabolic Pathway Structure and Regulation

“…Thereafter, comparison of these gene inventories with metabolite profiles of the species under evaluation allows the construction of putative metabolic pathway structures that can be further tested via reverse genetics or heterologous expression, as described in "Integrating Metabolite and Transcript Data" above. Important insights into pathway evolution can be gained from such approaches, as illustrated by the recent cross-kingdom comparison of ascorbate biosynthesis (Wheeler et al, 2015).…”