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Catalase protects against nonenzymatic decarboxylations during photorespiration in Arabidopsis thaliana

Photorespiration recovers carbon that would be otherwise lost following the oxygenation reaction of rubisco and production of glycolate. Photorespiration is essential in plants and recycles glycolate into usable metabolic products through reactions spanning the chloroplast, mitochondrion, and peroxi...

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Autores principales: Bao, Han, Morency, Matt, Rianti, Winda, Saeheng, Sompop, Roje, Sanja, Weber, Andreas P. M., Walker, Berkley James
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8688901/
https://www.ncbi.nlm.nih.gov/pubmed/34977450
http://dx.doi.org/10.1002/pld3.366
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author Bao, Han
Morency, Matt
Rianti, Winda
Saeheng, Sompop
Roje, Sanja
Weber, Andreas P. M.
Walker, Berkley James
author_facet Bao, Han
Morency, Matt
Rianti, Winda
Saeheng, Sompop
Roje, Sanja
Weber, Andreas P. M.
Walker, Berkley James
author_sort Bao, Han
collection PubMed
description Photorespiration recovers carbon that would be otherwise lost following the oxygenation reaction of rubisco and production of glycolate. Photorespiration is essential in plants and recycles glycolate into usable metabolic products through reactions spanning the chloroplast, mitochondrion, and peroxisome. Catalase in peroxisomes plays an important role in this process by disproportionating H(2)O(2) resulting from glycolate oxidation into O(2) and water. We hypothesize that catalase in the peroxisome also protects against nonenzymatic decarboxylations between hydrogen peroxide and photorespiratory intermediates (glyoxylate and/or hydroxypyruvate). We test this hypothesis by detailed gas exchange and biochemical analysis of Arabidopsis thaliana mutants lacking peroxisomal catalase. Our results strongly support this hypothesis, with catalase mutants showing gas exchange evidence for an increased stoichiometry of CO(2) release from photorespiration, specifically an increase in the CO(2) compensation point, a photorespiratory‐dependent decrease in the quantum efficiency of CO(2) assimilation, increase in the (12)CO(2) released in a (13)CO(2) background, and an increase in the postillumination CO(2) burst. Further metabolic evidence suggests this excess CO(2) release occurred via the nonenzymatic decarboxylation of hydroxypyruvate. Specifically, the catalase mutant showed an accumulation of photorespiratory intermediates during a transient increase in rubisco oxygenation consistent with this hypothesis. Additionally, end products of alternative hypotheses explaining this excess release were similar between wild type and catalase mutants. Furthermore, the calculated rate of hydroxypyruvate decarboxylation in catalase mutant is much higher than that of glyoxylate decarboxylation. This work provides evidence that these nonenzymatic decarboxylation reactions, predominately hydroxypyruvate decarboxylation, can occur in vivo when photorespiratory metabolism is genetically disrupted.
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spelling pubmed-86889012021-12-30 Catalase protects against nonenzymatic decarboxylations during photorespiration in Arabidopsis thaliana Bao, Han Morency, Matt Rianti, Winda Saeheng, Sompop Roje, Sanja Weber, Andreas P. M. Walker, Berkley James Plant Direct Original Research Photorespiration recovers carbon that would be otherwise lost following the oxygenation reaction of rubisco and production of glycolate. Photorespiration is essential in plants and recycles glycolate into usable metabolic products through reactions spanning the chloroplast, mitochondrion, and peroxisome. Catalase in peroxisomes plays an important role in this process by disproportionating H(2)O(2) resulting from glycolate oxidation into O(2) and water. We hypothesize that catalase in the peroxisome also protects against nonenzymatic decarboxylations between hydrogen peroxide and photorespiratory intermediates (glyoxylate and/or hydroxypyruvate). We test this hypothesis by detailed gas exchange and biochemical analysis of Arabidopsis thaliana mutants lacking peroxisomal catalase. Our results strongly support this hypothesis, with catalase mutants showing gas exchange evidence for an increased stoichiometry of CO(2) release from photorespiration, specifically an increase in the CO(2) compensation point, a photorespiratory‐dependent decrease in the quantum efficiency of CO(2) assimilation, increase in the (12)CO(2) released in a (13)CO(2) background, and an increase in the postillumination CO(2) burst. Further metabolic evidence suggests this excess CO(2) release occurred via the nonenzymatic decarboxylation of hydroxypyruvate. Specifically, the catalase mutant showed an accumulation of photorespiratory intermediates during a transient increase in rubisco oxygenation consistent with this hypothesis. Additionally, end products of alternative hypotheses explaining this excess release were similar between wild type and catalase mutants. Furthermore, the calculated rate of hydroxypyruvate decarboxylation in catalase mutant is much higher than that of glyoxylate decarboxylation. This work provides evidence that these nonenzymatic decarboxylation reactions, predominately hydroxypyruvate decarboxylation, can occur in vivo when photorespiratory metabolism is genetically disrupted. John Wiley and Sons Inc. 2021-12-20 /pmc/articles/PMC8688901/ /pubmed/34977450 http://dx.doi.org/10.1002/pld3.366 Text en © 2021 The Authors. Plant Direct published by American Society of Plant Biologists and the Society for Experimental Biology and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by-nc/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Original Research
Bao, Han
Morency, Matt
Rianti, Winda
Saeheng, Sompop
Roje, Sanja
Weber, Andreas P. M.
Walker, Berkley James
Catalase protects against nonenzymatic decarboxylations during photorespiration in Arabidopsis thaliana
title Catalase protects against nonenzymatic decarboxylations during photorespiration in Arabidopsis thaliana
title_full Catalase protects against nonenzymatic decarboxylations during photorespiration in Arabidopsis thaliana
title_fullStr Catalase protects against nonenzymatic decarboxylations during photorespiration in Arabidopsis thaliana
title_full_unstemmed Catalase protects against nonenzymatic decarboxylations during photorespiration in Arabidopsis thaliana
title_short Catalase protects against nonenzymatic decarboxylations during photorespiration in Arabidopsis thaliana
title_sort catalase protects against nonenzymatic decarboxylations during photorespiration in arabidopsis thaliana
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8688901/
https://www.ncbi.nlm.nih.gov/pubmed/34977450
http://dx.doi.org/10.1002/pld3.366
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