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In BriefIN BRIEF
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The Evolution of Photorespiratory Glycolate Oxidase Activity

Nancy R. Hofmann
Nancy R. Hofmann
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Published August 2011. DOI: https://doi.org/10.1105/tpc.111.230810

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  • © 2011 American Society of Plant Biologists. All rights reserved.

The first step of photosynthetic carbon fixation is catalyzed by ribulose-1,5-bisphosphate carboxylase/oxygenase, which arose when the atmosphere contained virtually no O2. The increase of atmospheric O2 caused by oxygenic photosynthesis gave rise to photorespiratory metabolism, a process whereby O2 substitutes for CO2, causing ribulose-1,5-bisphosphate carboxylase/oxygenase to produce the toxic compound 2-phosphoglycolate, which is ultimately recycled into 3-phosphoglycerate (reviewed in Bauwe et al., 2010). This recycling process is vital for the success of photosynthetic organisms under the current levels of O2 in the atmosphere but also accounts for losses of large amounts of carbon and energy. New work from Hackenberg et al. (pages 2978–2990) advances our understanding of the evolution of photorespiration.

During the recycling of 2-phosphoglycolate to 3-phosphoglycerate, glycolate is converted into glyoxylate by glycolate oxidases (GOXs) in plants and by glycolate dehydrogenases in cyanobacteria and green algae. Hackenberg et al. searched for GOX homologs in bacteria, algae, and plants and found homologs of the well-characterized spinach (Spinacia oleracea) GOX in cyanobacteria and algae. This result corroborates the recent findings of Kern et al. (2011), who similarly report that GOX-like proteins are found in nitrogen-fixing cyanobacterial species and show that GOX in photosynthetic eukaryotes was in the genome of the cyanobacterial endosymbiont that gave rise to the plastid. However, given that green algae and cyanobacteria use glycolate dehydrogenases instead of GOX for the comparable step of photorespiration, the discovery of genes coding for GOX-like proteins in their genomes raises the questions: What are the cyanobacterial and algal GOX homologs doing? How did they acquire their photorespiratory function in land plants?

Hackenberg et al. purified GOX-related proteins from Arabidopsis thaliana, the N2-fixing cyanobacterium Nostoc PCC 7120, and the green alga Chlamydomonas reinhardtii. They found that whereas all three proteins displayed oxidase activity, the Nostoc and C. reinhardtii proteins preferred L-lactate over glycolate and thus are lactate oxidases (LOXs).

A LOX-null Nostoc mutant did not display the growth impairment typical of photorespiratory mutants. Instead, LOX appears needed for nitrogen fixation in the presence of oxygen. Hackenberg et al. speculate that LOX functions as an oxygen scavenger that allows the bacteria to use atmospheric nitrogen as their nitrogen source even in high-oxygen atmospheres.

Given the close relationship between nitrogen-fixing cyanobacteria and the plastid endosymbiont, it is reasonable to imagine that after endosymbiosis the plastid-encoded LOX evolved GOX activity and acquired a role in photorespiration, replacing glycolate dehydrogenases. Based on comparisons of the LOX and GOX sequences (see figure), the authors were able to mutate Nostoc LOX such that its GOX activity increased at the same time as its LOX activity decreased, making it resemble a GOX. This shows that once LOX was present in the plant genome, it would have been evolutionarily easy to acquire a fully functional GOX protein. The eventual origin of GOX-based photorespiration in the charophyte green algal lineage may have played an important role in the subsequent appearance of land-adapted plants.

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Alignment of the active sites of GOX, LOX, and related proteins. The gray residues are those likely involved in substrate binding. Arrows mark amino acid mutations in Nostoc LOX that together switched its activity to GOX. (From Figure 2 of Hackenberg et al. [2011].)

Footnotes

  • www.plantcell.org/cgi/doi/10.1105/tpc.111.230810

References

  1. ↵
    1. Bauwe H.,
    2. Hagemann M.,
    3. Fernie A.R.
    (2010). Photorespiration: players, partners and origin. Trends Plant Sci. 15: 330–336.
    OpenUrlCrossRefPubMed
  2. ↵
    1. Hackenberg C.,
    2. Kern R.,
    3. Hüge J.,
    4. Stal L.J.,
    5. Tsuji Y.,
    6. Kopka J.,
    7. Shiraiwa Y.,
    8. Bauwe H.,
    9. Hagemann M.
    (2011). Cyanobacterial lactate oxidases serve as essential partners in N2-fixation and evolved into photorespiratory glycolate oxidases in plants. Plant Cell 23: 2978–2990.
    OpenUrlAbstract/FREE Full Text
  3. ↵
    1. Kern R.,
    2. Bauwe H.,
    3. Hagemann M.
    (2011). Evolution of enzymes involved in the photorespiratory 2-phosphoglycolate cycle from cyanobacteria via algae toward plants. Photosynth. Res. 109: 103–114.
    OpenUrlCrossRefPubMed
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The Evolution of Photorespiratory Glycolate Oxidase Activity
Nancy R. Hofmann
The Plant Cell Aug 2011, 23 (8) 2805; DOI: 10.1105/tpc.111.230810

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The Evolution of Photorespiratory Glycolate Oxidase Activity
Nancy R. Hofmann
The Plant Cell Aug 2011, 23 (8) 2805; DOI: 10.1105/tpc.111.230810
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The Plant Cell Online: 23 (8)
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Vol. 23, Issue 8
Aug 2011
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