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J Exp Bot. 2016 May;67(10):3165-75. doi: 10.1093/jxb/erw118. Epub 2016 Mar 19.

Photorespiratory glycolate oxidase is essential for the survival of the red alga Cyanidioschyzon merolae under ambient CO2 conditions.

Author information

  • 1Institute of Plant Biochemistry, Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich Heine University, Universitätsstraße 1, 40225 Düsseldorf, Germany.
  • 2University Rostock, Department Plant Physiology, Albert-Einstein-Straße 3, 18059 Rostock, Germany.
  • 3Division of Symbiosis and Cell Evolution, National Institute of Genetics, 1111 Yata, Mishima 411-8540, Shizuoka, Japan.
  • 4Division of Symbiosis and Cell Evolution, National Institute of Genetics, 1111 Yata, Mishima 411-8540, Shizuoka, Japan Japan Science and Technology Agency, CREST, 4-1-8 Honcho, Kawaguchi 332-0012, Saitama, Japan.
  • 5Institute of Plant Biochemistry, Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich Heine University, Universitätsstraße 1, 40225 Düsseldorf, Germany andreas.weber@hhu.de.

Abstract

Photorespiration is essential for all organisms performing oxygenic photosynthesis. The evolution of photorespiratory metabolism began among cyanobacteria and led to a highly compartmented pathway in plants. A molecular understanding of photorespiration in eukaryotic algae, such as glaucophytes, rhodophytes, and chlorophytes, is essential to unravel the evolution of this pathway. However, mechanistic detail of the photorespiratory pathway in red algae is scarce. The unicellular red alga Cyanidioschyzon merolae represents a model for the red lineage. Its genome is fully sequenced, and tools for targeted gene engineering are available. To study the function and importance of photorespiration in red algae, we chose glycolate oxidase (GOX) as the target. GOX catalyses the conversion of glycolate into glyoxylate, while hydrogen peroxide is generated as a side-product. The function of the candidate GOX from C. merolae was verified by the fact that recombinant GOX preferred glycolate over L-lactate as a substrate. Yellow fluorescent protein-GOX fusion proteins showed that GOX is targeted to peroxisomes in C. merolae The GOX knockout mutant lines showed a high-carbon-requiring phenotype with decreased growth and reduced photosynthetic activity compared to the wild type under ambient air conditions. Metabolite analyses revealed glycolate and glycine accumulation in the mutant cells after a shift from high CO2 conditions to ambient air. In summary, or results demonstrate that photorespiratory metabolism is essential for red algae. The use of a peroxisomal GOX points to a high photorespiratory flux as an ancestral feature of all photosynthetic eukaryotes.

KEYWORDS:

Evolution; glycolate oxidase; knockout mutant; metabolites; photorespiration; red alga.

PMID:
26994474
PMCID:
PMC4867895
DOI:
10.1093/jxb/erw118
[PubMed - in process]
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