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Affixing the O to Rubisco: discovering the source of photorespiratory glycolate and its regulation

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Abstract

The source of glycolate in photorespiration and its control, a particularly active and controversial research topic in the 1970s, was resolved in large part by several discoveries and observations described here. George Bowes discovered that the key carboxylation enzyme Rubisco (ribulosebisphosphate carboxylase/oxygenase) is competitively inhibited by O2 and that O2 substitutes for CO2 in the initial `dark' reaction of photosynthesis to yield glycolate-P, the substrate for photorespiration. William Laing derived an equation from basic enzyme kinetics that describes the CO2, O2, and temperature dependence of photosynthesis, photorespiration, and the CO2 compensation point in C3 plants. Jerome Servaites established that photosynthesis cannot be increased by inhibiting the photorespiratory pathway prior to the release of photorespiratory CO2, and Douglas Jordan discovered substantial natural variation in the Rubisco oxygenase/carboxylase ratio. A mutant Arabidopsis plant with defective glycolate-P phosphatase, isolated by Chris Somerville, definitively established the role of O2 and Rubisco in providing photorespiratory glycolate. Selection techniques to isolate photorespiration-deficient plants were devised by Jack Widholm and by Somerville, but no plants with reduced photorespiration were found. Somerville's approach, directed mutagenesis of Arabidopsis plants, was subsequently successful in the isolation of numerous other classes of mutants and revolutionized the science of plant biology.

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References

  • Andrews TJ, Lorimer GH and Tolbert NE (1971) Incorporation of molecular oxygen into glycine and serine during photorespiration in spinach leaves. Biochemistry 10: 4777–4782

    Article  PubMed  CAS  Google Scholar 

  • Andrews TJ, Lorimer GH and Tolbert NE (1973) Ribulose diphosphate oxygenase. I. Synthesis of phosphoglycolate by fraction-1protein of leaves. Biochemistry 12: 11–18

    Article  PubMed  CAS  Google Scholar 

  • Anonymous (1971) Carbon skeletons in the cupboard. Nature New Biol 230: 193–194

    Google Scholar 

  • Bassham JA (2003) Mapping the carbon reduction cycle: a personal retrospective. Photosynth Res 76: 35–52 (this issue)

    Article  PubMed  Google Scholar 

  • Benson AA (2002) Following the path of carbon in photosynthesis: a personal story. Photosynth Res 73: 29–49

    Article  PubMed  CAS  Google Scholar 

  • Björkman O (1968) Carboxydismutase activity in shade-adapted and sun-adapted species of higher plants. Physiol Plant 21: 1–10

    Article  Google Scholar 

  • Bowes G and Ogren WL (1970) The effect of light intensity and atmosphere on ribulose diphosphate carboxylase activity. Plant Physiol (Suppl) 46: 7–7

    Google Scholar 

  • Bowes G, Ogren WL and Hageman RH (1971) Phosphoglycolate production catalyzed by ribulose diphosphate carboxylase. Biochem Biophys Res Commun 45: 716–722

    Article  PubMed  CAS  Google Scholar 

  • Chollet R and Ogren WL (1975) Regulation of photorespiration in C3 and C4 species. Bot Rev 41: 37–179

    Google Scholar 

  • Criswell JG and Shibles RM (1971) Physiological basis for genotypic variation in net photosynthesis of oat leaves. Crop Sci 11: 550–553

    Article  Google Scholar 

  • Coombs J and Whittingham CP (1966) The mechanism of inhibition of photosynthesis by high partial pressures of oxygen in Chlorella. Proc R Soc London Ser B 164: 511–520

    Article  CAS  Google Scholar 

  • Curtis PE, Ogren WL and Hageman RH (1969) Varietal effects in soybean photosynthesis and photorespiration. Crop Sci 9:323–327

    Article  Google Scholar 

  • Dornhoff GM and Shibles RM (1970) Varietal differences in net photosynthesis of soybean leaves. Crop Sci 10: 42–45

    Article  Google Scholar 

  • Forrester ML, Krotkov G and Nelson CD (1966) Effect of oxygen on photosynthesis, photorespiration, and respiration in detached leaves. II. Soybean. Plant Physiol 41:422–427

    PubMed  CAS  Google Scholar 

  • Hageman RH, Leng ER and Dudley JW (1967) A biochemical approach to corn breeding. In: Norman AG (ed) Advances in Agronomy, Vol 19, pp 45–86. Academic Press, New York

    Google Scholar 

  • Hatch MD (2002) C4 photosynthesis: discovery and resolution. Photosynth Res 73: 251–256

    Article  PubMed  CAS  Google Scholar 

  • Jordan DB and Ogren WL (1981a) A sensitive assay procedure for simultaneous determination of ribulose-1,5–bisphosphate carboyxlase and oxygenase activities. Plant Physiol 67: 237–245

    PubMed  CAS  Google Scholar 

  • Jordan DB and Ogren WL (1981b) Species variation in the specificity of ribulose bisphosphate carboxylase/oxygenase. Nature 291: 513–515

    Article  CAS  Google Scholar 

  • Krogmann D (2000) The golden age of biochemical research in photosynthesis. Photosynth Res 63: 109–121

    Article  PubMed  CAS  Google Scholar 

  • Laing WA, Ogren WL and Hageman RH (1974) Regulation of soybean net photosynthetic CO2 fixation by the interaction of CO2, O2 and ribulose 1,5–diphosphate carboxylase. Plant Physiol 54: 678–685

    PubMed  CAS  Google Scholar 

  • Laing WA, Ogren WL and Hageman RH (1975) Bicarbonate stabilization of ribulose 1,5–diphosphate carboxylase. Biochemistry 14: 2269–2275

    Article  PubMed  CAS  Google Scholar 

  • Lorimer GH (2001) Letter to the editor. Plant Physiol 127: 3–3

    Article  PubMed  CAS  Google Scholar 

  • Lorimer GH and Andrews TJ (1973) Plant photorespiration - an inevitable consequence of the existence of atmospheric oxygen. Nature 243: 349–383

    Article  Google Scholar 

  • Lorimer GH, Andrews TJ, and Tolbert NE (1972) Oxidative activity associated with ribulose-1,5–diphosphate carboxylase. Fed Abstr 31: 461–461

    Google Scholar 

  • Ludwig LJ and Canvin DT (1971) An open gas-exchange system for the simultaneous measurement of the CO2 and 14CO2 fluxes from leaves. Can J Bot 49: 1299–1313

    CAS  Google Scholar 

  • Ogren WL (1971) Oxygen regulation of photosynthesis, photorespiration, and crop productivity. Proc Can Soc Plant Physiol 11: 15–16

    Google Scholar 

  • Ogren WL (1976) Improving the photosynthetic efficiency of soybean. In: Hill LD (ed) World Soybean Research, pp 253–261. Interstate Press, Danville, Illinois

    Google Scholar 

  • Ogren WL (1984) Photorespiration: Pathways, regulation and modification. Annu Rev Plant Physiol 35: 415–442

    Article  CAS  Google Scholar 

  • Ogren WL and Bowes G (1971) Ribulose diphosphate carboyxlase regulates soybean photorespiration. Nature New Biol 230: 159–160

    PubMed  CAS  Google Scholar 

  • Ogren WL and Chollet R (1982) Photorespiration. In: Govindjee (ed) Photosynthesis, Vol II, pp 191–230. Academic Press, New York

    Google Scholar 

  • Pearlstein RM (ed) (1971) Proceedings of the International Conference on the Photosynthetic Unit held in Gatlinburg, Tennessee, May 18-21, 1970. Photochem Photobiol 14: 231–473

  • Pennisi E (2000) Arabidopsis comes of age. Science 290: 32–35

    Article  PubMed  CAS  Google Scholar 

  • Pon NG, Rabin BR and Calvin M (1963) Mechanism of the carboxydismutase reaction. I. The effect of preliminary incubation of substrates, metal ion and enzyme on activity. Biochem Z 338: 7–19

    PubMed  CAS  Google Scholar 

  • Portis AR and Salvucci M (20002) The discovery of Rubisco activase-yet another story of serendipity. Photosynth Res 73: 257–264

    Article  Google Scholar 

  • Pritchard GG, Whittingham CP and Griffin WJ (1963) The effect of isonicotinyl hydrazide on the photosynthetic incorporation of radioactive carbon dioxide into ethanol-soluble compounds of Chlorella. J Exp Bot 14: 281–289

    CAS  Google Scholar 

  • Richardson KE and Tolbert NE (1961) Phosphoglycolic acid phosphatase. J Biol Chem 236: 1285–1290

    PubMed  CAS  Google Scholar 

  • Servaites JC and Ogren WL (1977a) Rapid isolation of mesophyll cells from leaves of soybean for photosynthetic studies. Plant Physiol 59: 587–590

    PubMed  CAS  Google Scholar 

  • Servaites JC and Ogren WL (1977b) Chemical inhibition of the glycolate pathway in soybean leaf cells. Plant Physiol 60: 461–466

    Google Scholar 

  • Somerville CR (2001a) An early Arabidopsis demonstration. Resolving a few issues concerning photorespiration. Plant Physiol 125: 20–24

    Article  PubMed  CAS  Google Scholar 

  • Somerville CR (2001b) Letter to the editor. Plant Physiol 127: 3–3

    Article  CAS  Google Scholar 

  • Somerville CR and Ogren WL (1979) A phosphoglycolate phosphatase-deficient mutant in Arabidopsis. Nature 280: 833–836

    Article  CAS  Google Scholar 

  • Tolbert NE (1971) Microbodies - peroxisomes and glyoxysomes. Annu Rev Plant Physiol 22: 45–74

    Article  CAS  Google Scholar 

  • Tolbert NE (1973) Compartmentation and control in microbodies. Symp Soc Exp Biol 27: 215–239

    PubMed  CAS  Google Scholar 

  • Tregunna EB, Krotkov G and Nelson CD (1966) Effect of oxygen on the rate of photorespiration in detached tobacco leaves. Physiol Plant 19: 723–733

    Article  Google Scholar 

  • Widholm JM and Ogren WL (1969) Photorespiratory-induced senescence of higher plants under conditions of low carbon dioxide. Proc Natl Acad Sci USA 63: 668–675

    Article  PubMed  CAS  Google Scholar 

  • Wildman SG (2002) Along the trail from fraction 1 protein to Rubisco (ribulose bis phosphate carboxylase oxygenase). Photosynth Res 73: 243–250

    Article  PubMed  CAS  Google Scholar 

  • Zelitch I (1965) The relation of glycolic acid synthesis to the primary photosynthetic carboxylation reaction in leaves. J Biol Chem 240: 1869–1876

    PubMed  CAS  Google Scholar 

  • Zelitch I (1966) Increased rate of net photosynthetic carbon dioxide uptake caused by the inhibition of glycolate oxidase. Plant Physiol 41: 1623–1631

    PubMed  CAS  Google Scholar 

  • Zelitch I (2001) Travels in a world of small science. Photosynth Res 67: 157–176

    Article  PubMed  CAS  Google Scholar 

  • Zelitch I and Day PR (1968) Variation in photorespiration. The effect of genetic differences in photorespiration on net photosynthesis in tobacco. Plant Physiol 43: 1838–1841

    Article  PubMed  CAS  Google Scholar 

Download references

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  1. Formerly United States Department of Agriculture Scientist University of Illinois at Urbana, USA

    William L. Ogren

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  1. William L. Ogren
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Ogren, W.L. Affixing the O to Rubisco: discovering the source of photorespiratory glycolate and its regulation. Photosynthesis Research 76, 53–63 (2003). https://doi.org/10.1023/A:1024913925002

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