Primary carbon partitioning in red algae and green plants
Final Report Abstract
In this project, we could show that in the red and green lineage of photosynthetic organisms that have plastids of primary endosymbiotic orgin, also known as the Archaeplastida, the export of carbon from the chloroplast occurs through plastidial phosphate translocators, which have evolved from sugar nucleotide transporters of the eukaryotic endomembrane system. That is, the main carbon exporters of red and green algae and of land plants are of host-origin. Our work further showed that out of the three paralogous phosphate translocator genes in red algae, only one, TPT, has been transferred into the genome of the malaria parasite P. falsiparum through endosymbiotic gene transfer. Surprisingly, in the new genomic context, this protein has evolved a novel function, namely the ability to transport phosphoenolpyruvate. That is, in P. falsiparum, transport functions that are realized by distinct proteins in the red and green lineages are mediated by single broad-spectrum protein in the malaria parasite. Red algal transporters have narrower substrate specificity than their greenlineage counterparts and they display higher affinity towards their substrates. We propose that this enables more efficient transport of recently assimilated carbon from the chloroplast, which is required in the absence of a plastidal starch pool that can serve as a buffer for carbohydrates that cannot be exported from the stroma to the cytoplasm. Surprisingly, the third lineage of the Archaeplastida, the glaucophytes, have not yet evolved plastidial phosphate translocators, which indicates that this class of proteins evolved only after the split of the red and green lineages from the last common ancestor of the Archaeplastida. Instead, glaucophytes use a protein of bacterial origin, UhpC-like transporter, for the export of carbon from the chloroplasts. This protein has likely been acquired very early during endosymbiosis by horizontal gene transfer from a chlamydia-like bacterium. In the red and green algae, the transporter function has been replaced by phosphate translocators of eukaryotic origin but the gene has been maintained in algal genomes. In land plants, it is no longer detectable, though. Overall, our work has shed new light on the biochemistry of carbon partitioning between chloroplast and cytoplasm in red and green algae and in glaucophytes. It has further provided novel insights into the evolution of the metabolic connection between chloroplast and host cell during the process of endosymbiosis.
Publications
- (2008) Functional characterization of the plastidic phosphate translocator gene family from the thermo-acidophilic red alga Galdieria sulphuraria reveals specific adaptations of primary carbon partitioning in green plants and red algae. Plant Physiol 148: 1487-1496
Linka M, Jamai A, Weber APM
- (2010) Phylogenetic and biochemical evidence supports the recruitment of an ADP-glucose translocator for the export of photosynthate during plastid endosymbiosis. Mol Biol Evol 27(12): 2691- 2701
Colleoni C, Linka M, Deschamps P, Handford MG, Dupree P, Weber APM, *Ball SG
- (2010) The carbon and energy sources of the non-photosynthetic plastid in the malaria parasite. FEBS Lett 584(3): 549-554
Lim L, Linka M, Weber APM, McFadden GI
- (2012) Metabolic integration of the chloroplast during endosymbiosis - molecular characterization of envelope transport proteins. Endocytobiosis Cell Res 23: 96-102
Bräutigam A, Facchinelli F, Weber APM
- (2013) Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339(6124):1207-1210
Schönknecht G, Chen WH, Ternes CM, Barbier GG, Shrestha RP, Stanke M, Bräutigam A, Baker BJ, Banfield JF, Garavito RM, Carr K, Wilkerson C, Rensing SA, Gagneul D, Dickenson NE, Oesterhelt C, Lercher MJ, Weber APM
(See online at https://doi.org/10.1126/science.1231707) - (2013) Metabolic effectors secreted by bacterial pathogens: essential facilitators of plastid endosymbiosis? Plant Cell 25(1):7-21
Ball SG, Subtil A, Bhattacharya D, Moustafa A, Weber APM, Gehre L, Colleoni C, Arias MC, Cenci U, Dauvillé D
