Phylogenetic and biochemical evidence supports the recruitment of an ADP-glucose translocator for the export of photosynthate during plastid endosymbiosis.
The acquisition of photosynthesis by eukaryotic cells through enslavement of a cyanobacterium represents one of the most remarkable turning points in the history of life on Earth. In addition to endosymbiotic gene transfer, the acquisition of a protein import apparatus and the coordination of gene expression between host and endosymbiont genomes, the establishment of a metabolic connection was crucial for a functional endosymbiosis. It was previously hypothesized that the first metabolic connection between both partners of endosymbiosis was achieved through insertion of a host-derived metabolite transporter into the cyanobacterial plasma membrane. Reconstruction of starch metabolism in the common ancestor of photosynthetic eukaryotes suggested that adenosine diphosphoglucose (ADP-Glc), a bacterial-specific metabolite, was likely to be the photosynthate, which was exported from the early cyanobiont. However, extant plastid transporters that have evolved from host-derived endomembrane transporters do not transport ADP-Glc but simple phosphorylated sugars in exchange for orthophosphate. We now show that those eukaryotic nucleotide sugar transporters, which define the closest relatives to the common ancestor of extant plastid envelope carbon translocators, possess an innate ability for transporting ADP-Glc. Such an unexpected ability would have been required to establish plastid endosymbiosis.
Colleoni
Christophe
C
Unité de Glycobiologie Structurale et Fonctionnelle, UMR 8576 CNRS-USTL, Université des Sciences et Technologies de Lille, Villeneuve d'Ascq Cedex, France.
Linka
Marc
M
Deschamps
Philippe
P
Handford
Michael G
MG
Dupree
Paul
P
Weber
Andreas P M
AP
Ball
Steven G
SG
D000245:Adenosine Diphosphate Glucose / Q000378:metabolism; D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism; D000458:Cyanobacteria / Q000235:genetics / Q000378:metabolism; D033704:Nucleotide Transport Proteins / Q000235:genetics* / Q000378:metabolism; D010788:Photosynthesis / Q000235:genetics*; D010802:Phylogeny; D018087:Plastids / Q000235:genetics / Q000378:metabolism*; D021381:Protein Transport; D012441:Saccharomyces cerevisiae / Q000235:genetics / Q000378:metabolism; D013213:Starch / Q000378:metabolism; D013559:Symbiosis
D033704:Nucleotide Transport Proteins; D000245:Adenosine Diphosphate Glucose; D013213:Starch