Skip to main content
OSTI.GOVU.S. Department of Energy Office of Scientific and Technical Information
U.S. Department of Energy
Office of Scientific and Technical Information
 

Catalase protects against nonenzymatic decarboxylations during photorespiration in Arabidopsis thaliana

Journal Article · · Plant Direct
DOI:https://doi.org/10.1002/pld3.366· OSTI ID:1836851
 [1];  [2];  [3];  [4];  [4];  [5];  [6]
  1. Department of Energy‐Plant Research Laboratory Michigan State University East Lansing MI USA
  2. Department of Energy‐Plant Research Laboratory Michigan State University East Lansing MI USA, Department of Plant Biology Michigan State University East Lansing MI USA
  3. Faculty of Agriculture Universitas Singaperbangsa Karawang Karawang Indonesia, Department of Plant Science Wageningen University Wageningen The Netherlands
  4. Institute of Biological Chemistry Washington State University Pullman WA USA
  5. Institute of Plant Biochemistry, Cluster of Excellence on Plant Sciences Heinrich‐Heine‐University Düsseldorf Germany
  6. Department of Energy‐Plant Research Laboratory Michigan State University East Lansing MI USA, Department of Plant Biology Michigan State University East Lansing MI USA, Institute of Plant Biochemistry, Cluster of Excellence on Plant Sciences Heinrich‐Heine‐University Düsseldorf Germany
+ Show Author Affiliations
Abstract

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.

Research Organization:
Michigan State University, East Lansing, MI (United States)
Sponsoring Organization:
Alexander von Humboldt Foundation; Division of Molecular and Cellular Biosciences; German Research Foundation (DFG); National Science Foundation (NSF); USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)
Grant/Contract Number:
FG02-91ER20021
OSTI ID:
1836851
Alternate ID(s):
OSTI ID: 1836852
OSTI ID: 1904594
Journal Information:
Plant Direct, Journal Name: Plant Direct Journal Issue: 12 Vol. 5; ISSN 2475-4455
Publisher:
Wiley Blackwell (John Wiley & Sons)Copyright Statement
Country of Publication:
United Kingdom
Language:
English

References (45)

The effect of temperature on glycollate decarboxylation in leaf peroxisomes journal January 1977
Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves journal December 1981
Glyoxylate decarboxylation during photorespiration journal January 1978
A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species journal June 1980
Reactivity of glyoxylate with hydrogen perioxide and simulation of the glycolate pathway of C3 plants and Euglena journal January 1985
Hydrogen peroxide production and the release of carbon dioxide during glycollate oxidation in leaf peroxisomes journal January 1976
Peroxisomal hydroxypyruvate reductase is not essential for photorespiration in Arabidopsis but its absence causes an increase in the stoichiometry of photorespiratory CO2 release journal May 2011
Determination of catalase activity by means of the Clark oxygen electrode journal May 1967
Diversity of properties among catalases journal May 2002
Glycine decarboxylase controls photosynthesis and plant growth journal September 2012
Photorespiration: players, partners and origin journal June 2010
Fiji: an open-source platform for biological-image analysis journal June 2012
In vivo stoichiometry of photorespiratory metabolism journal January 2016
Oxidative decarboxylation of glycollate and glyoxylate by leaf peroxisomes journal February 1974
Impact of mesophyll diffusion on estimated global land CO2 fertilization journal October 2014
Photorespiration mutants of Arabidopsis thaliana deficient in serine-glyoxylate aminotransferase activity journal May 1980
Redox Regulation in Photosynthetic Organisms: Signaling, Acclimation, and Practical Implications journal April 2009
Application of a Fluorescent Derivatization Reagent 9-Chloromethyl Anthracene on Determination of Carboxylic Acids by HPLC journal April 2012
Why are literature data for H2O2 contents so variable? A discussion of potential difficulties in the quantitative assay of leaf extracts journal February 2008
Influence of temperature on measurements of the CO2 compensation point: differences between the Laisk and O2-exchange methods journal February 2013
The glucose 6-phosphate shunt around the Calvin–Benson cycle journal November 2015
The Genetic Dissection of a Short-Term Response to Low CO2 Supports the Possibility for Peroxide-Mediated Decarboxylation of Photorespiratory Intermediates in the Peroxisome journal November 2012
Organelle pH in the Arabidopsis Endomembrane System journal September 2013
The metabolic origins of non-photorespiratory CO2 release during photosynthesis: a metabolic flux analysis journal February 2021
Peroxisomal Malate Dehydrogenase Is Not Essential for Photorespiration in Arabidopsis But Its Absence Causes an Increase in the Stoichiometry of Photorespiratory CO 2 Release journal August 2008
Alteration of the Alkaloid Profile in Genetically Modified Tobacco Reveals a Role of Methylenetetrahydrofolate Reductase in Nicotine N -Demethylation journal December 2012
The Response of Cyclic Electron Flow around Photosystem I to Changes in Photorespiration and Nitrate Assimilation journal March 2014
An Early Arabidopsis Demonstration. Resolving a Few Issues Concerning Photorespiration: Fig. 1. journal January 2001
Oxygen Exchange in Leaves in the Light journal August 1980
A Cytosolic Pathway for the Conversion of Hydroxypyruvate to Glycerate during Photorespiration in Arabidopsis journal October 2008
Conditional oxidative stress responses in the Arabidopsis photorespiratory mutant cat2 demonstrate that redox state is a key modulator of daylength-dependent gene expression, and define photoperiod as a crucial factor in the regulation of H2O2-induced cel: Photoperiod and H2O2signalling journal September 2007
Nitrate and ammonium lead to distinct global dynamic phosphorylation patterns when resupplied to nitrogen‐starved Arabidopsis seedlings journal January 2012
Dependence of the Post-Illumination Burst of CO2 on Temperature, Light, CO2, and O2 Concentration in Wheat (Triticum aestivum) journal August 1979
Estimating the rate of photorespiration in leaves journal May 1988
Protein phosphorylation and photorespiration journal March 2013
Steady-state models of photosynthesis: Steady-state models of photosynthesis journal April 2013
Temperature response of in vivo  Rubisco kinetics and mesophyll conductance in Arabidopsis thaliana : comparisons to Nicotiana tabacum journal August 2013
Improved method for measuring the apparent CO 2 photocompensation point resolves the impact of multiple internal conductances to CO 2 to net gas exchange: Photocompensation point measurements journal June 2015
An improved approach for measuring the impact of multiple CO 2 conductances on the apparent photorespiratory CO 2 compensation point through slope-intercept regression: Compensation point journal April 2016
Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field journal January 2019
Photorespiration and the postillumination CO 2 burst journal August 1971
The Costs of Photorespiration to Food Production Now and in the Future journal April 2016
O NE -C ARBON M ETABOLISM IN H IGHER P LANTS journal June 2001
Metabolite Profiling in Arabidopsisthaliana with Moderately Impaired Photorespiration Reveals Novel Metabolic Links and Compensatory Mechanisms of Photorespiration journal June 2021
13C Isotope Labelling to Follow the Flux of Photorespiratory Intermediates journal February 2021

Similar Records

Further studies on O sub 2 -resistant photosynthesis and photorespiration in a tobacco mutant with enhanced catalase activity
Journal Article · Wed Jan 31 23:00:00 EST 1990 · Plant Physiology; (USA) · OSTI ID:5946061

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
C3 photosynthesis
Calvin cycle
metabolism
photorespiration
photosynthesis -carbon reactions
redox homeostasis/redox reactions