Plant and Animal Glycolate Oxidases Have a Common Eukaryotic Ancestor and Convergently Duplicated to Evolve Long-Chain 2-Hydroxy Acid Oxidases

Eßer, Christian; Kuhn, Anke; Groth, Georg; Lercher, Martin J.; Maurino, Verónica G.

doi:10.1093/molbev/msu041

Cited by 53 publications

(71 citation statements)

References 54 publications

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“…Our genetic analysis indicated that the lack of GOX3, HAOX1, and HAOX2 does not influence the photorespiratory phenotype of cat2-2, which is in line with their substrate preferences and tissue-specific expression (Hodges et al, 2013;Esser et al, 2014;Engqvist et al, 2015). GOX1 and GOX2, on the other hand, metabolize glycolate in vitro with similar kinetic parameters and have been assumed to equally support the photorespiratory pathway.…”

Section: Lack Of Gox1 But Not Gox2 Attenuates the Photorespiratory supporting

confidence: 54%

“…This could be largely explained by their substrate specificities and expression patterns. HAOX1 and HAOX2 preferentially metabolize medium-and longchain hydroxyacids (Esser et al, 2014), and their absence did not significantly affect the extractable leaf GOX activity (Supplemental Fig. S7).…”

Section: Discussionmentioning

confidence: 98%

“…GOX3, on the other hand, is mainly expressed in roots where it converts glycolate and L-lactate with similar efficiency, making it an important player in lactate metabolism (Engqvist et al, 2015). HAOX1 and HAOX2 act predominantly on medium-and long-chain hydroxy acids, show a negligible activity toward glycolate (Esser et al, 2014), and are mainly expressed in seeds (Hodges et al, 2013).…”

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confidence: 99%

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Lack of GLYCOLATE OXIDASE1, but Not GLYCOLATE OXIDASE2, Attenuates the Photorespiratory Phenotype of CATALASE2-Deficient Arabidopsis

et al. 2016

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The genes coding for the core metabolic enzymes of the photorespiratory pathway that allows plants with C3-type photosynthesis to survive in an oxygen-rich atmosphere, have been largely discovered in genetic screens aimed to isolate mutants that are unviable under ambient air. As an exception, glycolate oxidase (GOX) mutants with a photorespiratory phenotype have not been described yet in C3 species. Using Arabidopsis (Arabidopsis thaliana) mutants lacking the peroxisomal CATALASE2 (cat2-2) that display stunted growth and cell death lesions under ambient air, we isolated a second-site loss-of-function mutation in GLYCOLATE OXIDASE1 (GOX1) that attenuated the photorespiratory phenotype of cat2-2. Interestingly, knocking out the nearly identical GOX2 in the cat2-2 background did not affect the photorespiratory phenotype, indicating that GOX1 and GOX2 play distinct metabolic roles. We further investigated their individual functions in single gox1-1 and gox2-1 mutants and revealed that their phenotypes can be modulated by environmental conditions that increase the metabolic flux through the photorespiratory pathway. High light negatively affected the photosynthetic performance and growth of both gox1-1 and gox2-1 mutants, but the negative consequences of severe photorespiration were more pronounced in the absence of GOX1, which was accompanied with lesser ability to process glycolate. Taken together, our results point toward divergent functions of the two photorespiratory GOX isoforms in Arabidopsis and contribute to a better understanding of the photorespiratory pathway.The increase in atmospheric CO 2 levels linked to global warming, which entails unpredictable climate conditions, poses an unprecedented pressure on modern agriculture (Lobell and Gourdji, 2012; Wheeler and von Braun, 2013). However, apart from its greenhouse properties, CO 2 and its photosynthetic assimilation into biomass are the primary foundation of life on Earth. Thus, atmospheric CO 2 content has a direct effect on agricultural production, and even a modest CO 2 increase might in theory result in higher crop yields, especially in plants with C3-type photosynthesis (Walker et al., 2016). In contrast to C4 and CAM-type plants, C3 plants do not possess carbon concentrating mechanisms, and the first stable CO 2 assimilation product is 3-phosphoglycerate that is further processed in the Calvin-Benson cycle to fuel sugar synthesis. C4 plants initially incorporate CO 2 into four-carbon acids that are subsequently decarboxylated in the vicinity of the primary CO 2 -assimilating enzyme Rubisco. The C4-type photosynthesis evolved independently over 60 times (Sage et al., 2011), reflecting the need to counteract the highly promiscuous nature of Rubisco that apart from carboxylation of ribulose-1,5-bisphosphate also catalyzes its oxygenation to 2-phosphoglycolate (PG). This oxygenation reaction initiates the photorespiratory pathway that recycles PG back to 3-phosphoglycerate with the release of CO 2 in a series of enzymatic steps distributed between chl...

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Section: Lack Of Gox1 But Not Gox2 Attenuates the Photorespiratory supporting

confidence: 54%

Section: Discussionmentioning

confidence: 98%

mentioning

confidence: 99%

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Lack of GLYCOLATE OXIDASE1, but Not GLYCOLATE OXIDASE2, Attenuates the Photorespiratory Phenotype of CATALASE2-Deficient Arabidopsis

et al. 2016

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“…The gene family of L-2-hydroxy acid oxidases (L-2-HAOX) encodes members that exhibit L-lactate oxidase activity (Esser et al, 2014). Glycolate oxidase (GOX), a crucial enzyme of plant photorespiration, belongs to the L-2-HAOX family.…”

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confidence: 99%

GLYCOLATE OXIDASE3, a Glycolate Oxidase Homolog of Yeast l-Lactate Cytochrome c Oxidoreductase, Supports l-Lactate Oxidation in Roots of Arabidopsis

et al. 2015

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In roots of Arabidopsis (Arabidopsis thaliana), L-lactate is generated by the reduction of pyruvate via L-lactate dehydrogenase, but this enzyme does not efficiently catalyze the reverse reaction. Here, we identify the Arabidopsis glycolate oxidase (GOX) paralogs GOX1, GOX2, and GOX3 as putative L-lactate-metabolizing enzymes based on their homology to CYB2, the L-lactate cytochrome c oxidoreductase from the yeast Saccharomyces cerevisiae. We found that GOX3 uses L-lactate with a similar efficiency to glycolate; in contrast, the photorespiratory isoforms GOX1 and GOX2, which share similar enzymatic properties, use glycolate with much higher efficiencies than L-lactate. The key factor making GOX3 more efficient with L-lactate than GOX1 and GOX2 is a 5-to 10-fold lower K m for the substrate. Consequently, only GOX3 can efficiently metabolize L-lactate at low intracellular concentrations. Isotope tracer experiments as well as substrate toxicity tests using GOX3 loss-offunction and overexpressor plants indicate that L-lactate is metabolized in vivo by GOX3. Moreover, GOX3 rescues the lethal growth phenotype of a yeast strain lacking CYB2, which cannot grow on L-lactate as a sole carbon source. GOX3 is predominantly present in roots and mature to aging leaves but is largely absent from young photosynthetic leaves, indicating that it plays a role predominantly in heterotrophic rather than autotrophic tissues, at least under standard growth conditions. In roots of plants grown under normoxic conditions, loss of function of GOX3 induces metabolic rearrangements that mirror wild-type responses under hypoxia. Thus, we identified GOX3 as the enzyme that metabolizes L-lactate to pyruvate in vivo and hypothesize that it may ensure the sustainment of low levels of L-lactate after its formation under normoxia.

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“…This enzyme is a member of the ␣-hydroxy-acid oxidase superfamily, which includes short-chain and long-chain hydroxy-acid oxidases, lactate oxidase, and the flavin-binding domain of yeast flavocytochrome b 2 (1). It appears that plant and animal GOXs (short-chain ␣-hydroxy-acid oxidases) arose from a common eukaryotic GOX ancestor that originated from a bacterial lactate oxidase (2). In mammals, GOX is responsible for the production of oxalate (3), and therefore it is a potential site for therapeutic agents to treat primary hyperoxaluria (4), a genetic disorder that leads to large kidney stones due to calcium oxalate deposition.…”

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confidence: 99%

Experimental Evidence for a Hydride Transfer Mechanism in Plant Glycolate Oxidase Catalysis

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Mauve

Boex-Fontvieille

et al. 2015

Journal of Biological Chemistry

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Background: Uncertainty remains about the nature of transition states along the reductive half-reaction of glycolate oxidase. Results: Deuterated glycolate and solvent slow down plant glycolate oxidase catalysis to a modest extent. Conclusion: Isotope effects support a hydride transfer mechanism and indicate glycolate deprotonation to be only partially rate-limiting. Significance: Understanding the catalytic mechanism of the enzyme is crucial for designing drugs/herbicides to inhibit its activity.

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Plant and Animal Glycolate Oxidases Have a Common Eukaryotic Ancestor and Convergently Duplicated to Evolve Long-Chain 2-Hydroxy Acid Oxidases

Cited by 53 publications

References 54 publications

Lack of GLYCOLATE OXIDASE1, but Not GLYCOLATE OXIDASE2, Attenuates the Photorespiratory Phenotype of CATALASE2-Deficient Arabidopsis

Lack of GLYCOLATE OXIDASE1, but Not GLYCOLATE OXIDASE2, Attenuates the Photorespiratory Phenotype of CATALASE2-Deficient Arabidopsis

GLYCOLATE OXIDASE3, a Glycolate Oxidase Homolog of Yeast l-Lactate Cytochrome c Oxidoreductase, Supports l-Lactate Oxidation in Roots of Arabidopsis

Experimental Evidence for a Hydride Transfer Mechanism in Plant Glycolate Oxidase Catalysis

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