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Evolution of enzymes involved in the photorespiratory 2-phosphoglycolate cycle from cyanobacteria via algae toward plants

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Abstract

The photorespiratory pathway was shown to be essential for organisms performing oxygenic photosynthesis, cyanobacteria, algae, and plants, in the present day O2-containing atmosphere. The identification of a plant-like 2-phosphoglycolate cycle in cyanobacteria indicated that not only genes of oxygenic photosynthesis but also genes encoding photorespiratory enzymes were endosymbiotically conveyed from ancient cyanobacteria to eukaryotic oxygenic phototrophs. Here, we investigated the origin of the photorespiratory pathway in photosynthetic eukaryotes by phylogenetic analysis. We found that a mixture of photorespiratory enzymes of either cyanobacterial or α-proteobacterial origin is present in algae and higher plants. Three enzymes in eukaryotic phototrophs clustered closely with cyanobacterial homologs: glycolate oxidase, glycerate kinase, and hydroxypyruvate reductase. On the other hand, the mitochondrial enzymes of the photorespiratory cycle in algae and plants, glycine decarboxylase subunits and serine hydroxymethyltransferase, evolved from proteobacteria. Other than most genes for proteins of the photosynthetic machinery, nearly all enzymes involved in the 2-phosphogylcolate metabolism coexist in the genomes of cyanobacteria and heterotrophic bacteria.

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Abbreviations

2PG:

2-Phosphoglycolate

3PGA:

3-Phosphoglycerate

BS:

Bootstrap value

CCM:

Inorganic carbon concentrating mechanism

GDC:

Glycine decarboxylase

GGT:

Glutamate:glyoxylate aminotransferase

GK:

Bacterial-type glycerate kinase

GLYK:

Plant-type glycerate kinase

GOX:

Glycolate oxidase

HPR:

Hydroxypyruvate reductase

PDC:

Pyruvate dehydrogenase

PGP:

2-Phosphoglycolate phosphatase

Rubisco:

Ribulose 1,5-bisphosphate carboxylase/oxygenase

SGT:

Serine:glyoxylate aminotransferase

SHMT:

Serine hydroxymethyltransferase

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Acknowledgments

The work was supported by grants of the DFG (Deutsche Forschungsgemeinschaft) in the frame of Forschergruppe FOR 1186-Promics.

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  1. Universität Rostock, Institut für Biowissenschaften, Abteilung Pflanzenphysiologie, Albert-Einstein-Straße 3, 18059, Rostock, Germany

    Ramona Kern, Hermann Bauwe & Martin Hagemann

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  1. Ramona Kern
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  2. Hermann Bauwe
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  3. Martin Hagemann
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Correspondence to Martin Hagemann.

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Supplementary Tables

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Supplementary Figure S1

Maximum likelihood tree of T-proteins of glycine decarboxylase (GDC). Numbers at the node indicated bootstrap values (%) for 400 replicates. The distance scale (substitutions per site) is shown in the bottom left-hand corner. Further information (protein accession numbers and sequence similarities) is given in Supplemental Tables S1 and S2. (TIFF 4607 kb)

Supplementary Figure S2

Maximum likelihood tree of L-proteins of glycine decarboxylase (GDC) based on 30 sequences. Numbers at the node indicated bootstrap values (%) for 400 replicates. The distance scale (substitutions per site) is shown in the bottom left-hand corner. Further information (protein accession numbers and sequence similarities) is given in Supplemental Tables S1 and S2. (TIFF 4795 kb)

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Kern, R., Bauwe, H. & Hagemann, M. Evolution of enzymes involved in the photorespiratory 2-phosphoglycolate cycle from cyanobacteria via algae toward plants. Photosynth Res 109, 103–114 (2011). https://doi.org/10.1007/s11120-010-9615-z

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