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Peroxisomal hydroxypyruvate reductase is not essential for photorespiration in Arabidopsis but its absence causes an increase in the stoichiometry of photorespiratory CO2 release

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Abstract

Recycling of carbon by the photorespiratory pathway involves enzymatic steps in the chloroplast, mitochondria, and peroxisomes. Most of these reactions are essential for plants growing under ambient CO2 concentrations. However, some disruptions of photorespiratory metabolism cause subtle phenotypes in plants grown in air. For example, Arabidopsis thaliana lacking both of the peroxisomal malate dehydrogenase genes (pmdh1pmdh2) or hydroxypyruvate reductase (hpr1) are viable in air and have rates of photosynthesis only slightly lower than wild-type plants. To investigate how disruption of the peroxisomal reduction of hydroxypyruvate to glycerate influences photorespiratory carbon metabolism we analyzed leaf gas exchange in A. thaliana plants lacking peroxisomal HPR1 expression. In addition, because the lack of HPR1 could be compensated for by other reactions within the peroxisomes using reductant supplied by PMDH a triple mutant lacking expression of both peroxisomal PMDH genes and HPR1 (pmdh1pmdh2hpr1) was analyzed. Rates of photosynthesis under photorespiratory conditions (ambient CO2 and O2 concentrations) were slightly reduced in the hpr1 and pmdh1pmdh2hpr1 plants indicating other reactions can help bypass this disruption in the photorespiratory pathway. However, the CO2 compensation points (Γ) increased under photorespiratory conditions in both mutants indicating changes in photorespiratory carbon metabolism in these plants. Measurements of Γ*, the CO2 compensation point in the absence of mitochondrial respiration, and the CO2 released per Rubisco oxygenation reaction demonstrated that the increase in Γ in the hpr1 and pmdh1pmdh2hpr1 plants is not associated with changes in mitochondrial respiration but with an increase in the non-respiratory CO2 released per Rubisco oxygenation reaction.

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References

  • Badger MR, Collatz GJ (1977) Studies on the kinetic mechanism of ribulose-I, 5-bisphosphate carboxylase and oxygenase reactions, with particular reference to the effect of temperature on kinetic parameters. Carnegie Inst Washington Yearb 76:355–361

    Google Scholar 

  • Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR, Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ 24(2):253–259

    Article  CAS  Google Scholar 

  • Brooks A, Farquhar GD (1985) Effect of temperature on the CO2/O2 specificity of Rubisco and the rate of respiration in the light- estimates from gas-exchange measurement on Spinach. Planta 165(3):397–406

    Article  CAS  Google Scholar 

  • Cousins AB, Pracharoenwattana I, Zhou W, Smith SM, Badger MR (2008) Peroxisomal malate dehydrogenase is not essential for photorespiration in Arabidopsis but its absence causes an increase in the stoichiometry of photorespiratory CO2 release. Plant Physiol 148:786–795

    Article  PubMed  CAS  Google Scholar 

  • Engel N, van den Daele K, Kolukisaoglu U, Morgenthal K, Weckwerth W, Parnik T, Keerberg O, Bauwe H (2007) Deletion of glycine decarboxylase in Arabidopsis is lethal under nonphotorespiratory conditions. Plant Physiol 144(3):1328–1335

    Article  PubMed  CAS  Google Scholar 

  • Flexas MFO, Ribas-Carbo M, Diaz-Espejo A, Flórez-Sarasa ID, Medrano H (2007) Mesophyll conductance to CO2 in Arabidopsis thaliana. New Phytol 175(3):501–511

    Article  PubMed  CAS  Google Scholar 

  • Grodzinski B (1979) Study of formate production and oxidation in leaf peroxisomes during photo-respiration. Plant Physiol 63(2):289–293

    Article  PubMed  CAS  Google Scholar 

  • Halliwel B (1974) Oxidation of formate by peroxisomes and mitochondria from spinach leaves. Biochem J 138(1):77–85

    Google Scholar 

  • Halliwel B, Butt VS (1974) Oxidative decarboxylation of glycolate and glyoxylate by leaf peroxisomes. Biochem J 138(2):217–224

    Google Scholar 

  • Hourton-Cabassa C, Ambard-Bretteville F, Moreau F, de Virville JD, Remy R, des Francs-Small CC (1998) Stress induction of mitochondrial formate dehydrogenase in potato leaves. Plant Physiol 116(2):627–635

    Article  PubMed  CAS  Google Scholar 

  • Jordan DB, Ogren WL (1981) Species variation in the specificity of ribulose-biphosphate carboxylase-oxygenase. Nature 291(5815):513–515

    Article  CAS  Google Scholar 

  • Jordan DB, Ogren WL (1984) The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase oxygenase—dependence on ribulosebisphosphate concentration, pH and temperature. Planta 161(4):308–313

    Article  CAS  Google Scholar 

  • Kisaki T, Tolbert NE (1969) Glycolate and glyoxylate metabolism by isolated peroxisomes or chloroplasts. Plant Physiol 44(2):242–250

    Article  PubMed  CAS  Google Scholar 

  • Kleczkowski LA, Edwards GE, Blackwell RD, Lea PJ, Givan CV (1990) Enzymology of the reduction of hydroxypyruvate and glyocylate in a mutant of barley lacking peroxisomal hyrdoxypyruvate reductase. Plant Physiol 94:819–825

    Article  PubMed  CAS  Google Scholar 

  • Mano S, Nishimura M (2005) Plant peroxisomes. Plant Horm 72:111–154

    Article  CAS  Google Scholar 

  • Maxwell K, Badger MR, Osmond CB (1998) A comparison of CO2 and O2 exchange patterns and the relationship with chlorophyll fluorescence during photosynthesis in C3 and CAM plants. Aust J Plant Physiol 25(1):45–52

    Article  Google Scholar 

  • Murray AJS, Blackwell RD, Joy KW, Lea PJ (1987) Photorespiratory-N donors, aminotransferase specificity and photosynthesis in a mutant of barley deficient in serine: glyoxylate aminotransferase activity. Planta 172(1):106–113

    Article  CAS  Google Scholar 

  • Murray AJS, Blackwell RD, Lea PJ (1989) Metabolism of hydroxypyruvate in a mutant of barley lacking nadh-dependent hydroxypyruvate reductase, an important photorespiratory enzyme-activity. Plant Physiol 91(1):395–400

    Article  PubMed  CAS  Google Scholar 

  • Ort DR, Baker NR (2002) A photoprotective role for O2 as an alternative electron sink in photosynthesis? Curr Opin Plant Biol 5:193–198

    Article  PubMed  CAS  Google Scholar 

  • Pracharoenwattana I, Cornah JE, Smith SM (2007) Arabidopsis peroxisomal malate dehydrogenase functions in beta-oxidation but not in the glyoxylate cycle. Plant Journal 50(3):381–390

    Article  PubMed  CAS  Google Scholar 

  • Pracharoenwattana I, Zhou WX, Smith SM (2010) Fatty acid beta-oxidation in germinating Arabidopsis seeds is supported by peroxisomal hydroxypyruvate reductase when malate dehydrogenase is absent. Plant Mol Biol 72(1–2):101–109

    Article  PubMed  CAS  Google Scholar 

  • Reumann S (2000) The structural properties of plant peroxisomes and their metabolic significance. Biol Chem 381(8):639–648

    Article  PubMed  CAS  Google Scholar 

  • Reumann S, Weber APM (2006) Plant peroxisomes respire in the light: Some gaps of the photorespiratory C2 cycle have become filled—Others remain. Biochim Biophys Acta 1763(12):1496–1510

    Article  PubMed  CAS  Google Scholar 

  • Ruuska S, Andrews TJ, Badger MR, Hudson GS, Laisk A, Price GD, von Caemmerer S (1998) The interplay between limiting processes in C3 photosynthesis studied by rapid-response gas exchange using transgenic tobacco impaired in photosynthesis. Aust J Plant Physiol 25(8):859–870

    Article  CAS  Google Scholar 

  • Ruuska S, Badger MR, Andrews TJ, von Caemmerer S (2000) Photosynthetic electron sinks in transgenic tobacco with reduced amounts of Rubisco: little evidence for significant Mehler reaction. J Exp Bot 51:357–368

    Article  PubMed  CAS  Google Scholar 

  • Sage RF, Way DA, Kubien DS (2008) Rubisco, Rubisco activase, and global climate change. J Exp Bot 59(7):1581–1595

    Article  PubMed  CAS  Google Scholar 

  • Schneidereit J, Hausler RE, Fiene G, Kaiser WM, Weber APM (2006) Antisense repression reveals a crucial role of the plastidic 2-oxoglutarate/malate translocator DiT1 at the interface between carbon and nitrogen metabolism. Plant J 45(2):206–224

    Article  PubMed  CAS  Google Scholar 

  • Sharkey TD (1988) Estimating the rate of photorespiration in leaves. Physiol Plant 73(1):147–152

    Article  CAS  Google Scholar 

  • Somerville CR, Ogren WL (1982) Genetic-modification of photo-respiration. Trends Biochem Sci 7(5):171–174

    Article  CAS  Google Scholar 

  • Takahashi S, Bauwe H, Badger M (2007) Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem II by suppression of repair but not acceleration of damage processes in Arabidopsis. Plant Physiol 144(1):487–494

    Article  PubMed  CAS  Google Scholar 

  • Timm S, Nunes-Nesi A, Pamik T, Morgenthal K, Wienkoop S, Keerberg O, Weckwerth W, Kleczkowski LA, Fernie AR, Bauwe H (2008) A cytosolic pathway for the conversion of hydroxypyruvate to glycerate during photorespiration in Arabidopsis. Plant Cell 20(10):2848–2859

    Article  PubMed  CAS  Google Scholar 

  • Tolbert NE (1997) The C2 oxidative photosynthetic carbon cycle. Annu Rev Plant Physiol Plant Mol Biol 48:1–25

    Article  PubMed  CAS  Google Scholar 

  • von Caemmerer S (2000) Biochemical models of leaf photosynthesis. CSIRO Publishing, Collingwood

    Google Scholar 

  • von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387

    Article  Google Scholar 

  • Wallsgrove RM, Keys AJ, Lea PJ, Miflin BJ (1983) Photosynthesis, photo-respiration and nitrogen-metabolism. Plant Cell Environ 6(4):301–309

    CAS  Google Scholar 

  • Walton NJ, Butt VS (1981) Metabolism and decarboxylation of glycolate and serine in leaf peroxisomes. Planta 153(3):225–231

    Article  CAS  Google Scholar 

  • Wingler A, Lea PJ, Leegood RC (1999) Photorespiratory metabolism of glyoxylate and formate in glycine-accumulating mutants of barley and Amaranthus edulis. Planta 207(4):518–526

    Article  CAS  Google Scholar 

  • Wingler A, Lea P, Quick W, Leegood R (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc Lond B 355:1517–1529

    Article  CAS  Google Scholar 

  • Yamori W, Suzuki K, Noguchi K, Nakai M, Terashima I (2006) Effects of Rubisco kinetics and Rubisco activation state on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. Plant Cell Environ 29(8):1659–1670

    Article  PubMed  CAS  Google Scholar 

  • Zelitch I (1972a) Alternate pathways of glycolate synthesis and their relation to photorespiration in tobacco and maize leaves. Plant Physiol 49:58

    Article  Google Scholar 

  • Zelitch I (1972b) The photooxidation of glyoxylate by envelope-free spinach chloroplasts and its relation to photorespiration. Arch Biochem Biophys 150(2):698–707

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported in part by the Australian Research Council Grants FF0457721 and CE0561495 (SMS), the Centres of Excellence Program of the Government of Western Australia (SMS & MRB), and NSF ARRA funds 0842182 and instrumentation obtained through an NSF Major Research Instrumentation grant (#0923562) (ABC).

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Authors and Affiliations

  1. School of Biological Sciences, Molecular Plant Sciences, Washington State University, Pullman, WA, 99164-4236, USA

    Asaph B. Cousins & Berkley J. Walker

  2. Australian Research Council Centre of Excellence In Plant Energy Biology, Molecular Plant Physiology Group, Research School of Biological Sciences, Australian National University, Canberra, ACT, 2601, Australia

    Murray R. Badger

  3. Australian Research Council Centre of Excellence in Plant Energy Biology, and Centre of Excellence for Plant Metabolomics, The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    Itsara Pracharoenwattana & Steven M. Smith

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  1. Asaph B. Cousins
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  2. Berkley J. Walker
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  3. Itsara Pracharoenwattana
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  4. Steven M. Smith
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  5. Murray R. Badger
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Correspondence to Asaph B. Cousins.

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Cousins, A.B., Walker, B.J., Pracharoenwattana, I. et al. Peroxisomal hydroxypyruvate reductase is not essential for photorespiration in Arabidopsis but its absence causes an increase in the stoichiometry of photorespiratory CO2 release. Photosynth Res 108, 91–100 (2011). https://doi.org/10.1007/s11120-011-9651-3

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