Chapter 15 Structure, Function, and Post-translational Regulation of C4 Pyruvate Orthophosphate Dikinase

Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 32)

Summary

Pyruvate orthophosphate dikinase is a cardinal enzyme of the C4 pathway. Its role in C4 photosynthesis is to catalyze the regeneration of PEP, the primary carboxylation substrate from pyruvate, Pi, and ATP in the chloroplast stroma of leaf-mesophyll cells. It is the most abundant of C4 enzymes, comprising up to 10% of the soluble protein of C4 leaves, and thus may exert a limitation on the rate of CO2 assimilation into the C4-cycle. Studies dating back to the 1970s documented its biochemical properties as related to its role in C4 photosynthetic process. Later studies originating in the early 1980s discovered how the enzyme is regulated in a light/dark manner by reversible phosphorylation of an active-site threonine. A bifunctional protein kinase/protein phosphatase with unprecedented properties, the PPDK Regulatory Protein (RP), was identified as the enzyme catalyzing this reversible phosphorylation event. However, the gene encoding this unusual enzyme had eluded cloning for some two decades until modern cloning methods allowed its recent isolation from maize. Although the enzyme properties of C4-PPDK are well understood, the molecular basis of its post-translational light/dark regulation by RP is poorly understood. Because of the significance of PPDK regulation to the C4-photosynthetic process, this chapter addresses the current state-of-knowledge on how C4-PPDK is post-translationally regulated by its companion regulatory enzyme, RP. This includes proposed models that describe how phosphorylation of PPDK by RP leads to complete inactivation of enzyme activity and the mechanism regulating the direction of RP’s opposing PPDK-dephosphorylation and PPDK-phosphorylation activities. Also reviewed are the recent bioinformatic analyses of the RP polypeptide primary structure. These revealed that vascular plant RP represents a fundamentally new and novel kind of protein kinase with evolutionary origins in PPDK-containing anaerobic bacteria.

Keywords

Regulatory Protein Reversible Phosphorylation Pyruvate Orthophosphate Dikinase Eukaryotic Protein Kinase Regulatory Protein Activity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

aa

amino acid;

GFP

green fluorescent protein;

NADP MDH

NADP malate dehydrogenase;

NADP ME

NADP malic enzyme;

ORF

open reading frame;

Pi

inorganic phosphate;

PPi

pyrophosphate;

PEP

phospho­enolpyruvate;

PEPc

PEP carboxylase;

PPDK

pyruvate orthophosphate dikinase;

Pyr

pyruvate;

RP

regulatory protein;

Notes

Acknowledgments

This work was supported by U.S. National Science Foundation Grant Nos. IOS-0642190 to C.J.C.

References

  1. Ashton AR, Burnell JN and Hatch MD (1984) Regulation of C4 photosynthesis: inactivation of pyruvate, Pi dikinase by ADP dependent phosphorylation and activation by phosphorolysis. Arch Biochem Biophys 230: 492–503.PubMedCrossRefGoogle Scholar
  2. Ashton AR, Burnell JN, Furbank RT, Jenkins CLD and Hatch MD (1990) Enzymes of C4 photosynthesis. In: Lea PJ (ed) Methods in Plant Biochemistry, Vol 3, pp 39–72. Academic Press, San DiegoGoogle Scholar
  3. Bringaud F, Baltz D and Baltz T (1998) Functional and molecular characterization of a glycosomal PPi dependent enzyme in trypanosomatids: Pyruvate, phosphate dikinase. Proc Natl Acad Sci USA 95: 7963–7968PubMedCrossRefGoogle Scholar
  4. Budde RJA, Holbrook GP and Chollet R (1985) Studies on the dark/light regulation of maize leaf pyruvate, orthophosphate dikinase by reversible phosphorylation. Arch Biochem Biophys 242: 283–290PubMedCrossRefGoogle Scholar
  5. Burnell JN (1984) Regulation of C4 photosynthesis: catalytic dephosphorylation and Pi-mediated activation of pyruvate Pi dikinase. Biochem Biophys Res Comm 120: 559–565PubMedCrossRefGoogle Scholar
  6. Burnell JN (1990) A comparative study of the cold-sensitivity of pyruvate, Pi dikinase in Flaveria species. Plant Cell Physiol 31: 295–297Google Scholar
  7. Burnell JN and Chastain CJ (2006) Cloning and expression of maize-leaf pyruvate, Pi dikinase regulatory protein gene. Biochem Biophys Res Comm (2006) 345: 675–680PubMedCrossRefGoogle Scholar
  8. Burnell JN and Hatch MD (1983) Dark/light regulation of pyruvate, Pi dikinase in C4 plants: evidence that the same protein catalyses activation and inactivation. Biochem Biophys Res Comm 111: 288–293PubMedCrossRefGoogle Scholar
  9. Burnell JN and Hatch MD (1985a) Regulation of C4 photosynthesis: purification and properties of the protein catalyzing ADP-mediated inactivation and Pi-mediated activation of pyruvate, Pi dikinase. Arch Biochem Biophys 237: 490–503PubMedCrossRefGoogle Scholar
  10. Burnell JN and Hatch MD (1985b) Light-dark modulation of leaf pyruvate, Pi dikinase. Trends Biochem Sci 10: 288–291CrossRefGoogle Scholar
  11. Carroll LJ, Dunaway-Mariano D, Smith CM, Chollet R (1990) Determination of the catalytic pathway of C4-leaf pyruvate,orthophosphate dikinase from maize. FEBS Lett 274: 178–180.PubMedCrossRefGoogle Scholar
  12. Chastain CJ and Chollet R (2003) Regulation of pyruvate,orthophosphate dikinase by ADP/Pi-dependent reversible phosphorylation in C3 and C4 plants. Plant Physiol Biochem 41: 523–532CrossRefGoogle Scholar
  13. Chastain CJ, Lee ME, Moorman MA, Shameekumar P and Chollet R (1997) Site-directed mutagenesis of maize recombinant C4-pyruvate, orthophosphate dikinase at the phosphorylatable target threonine residue. FEBS Lett 413: 169–173PubMedCrossRefGoogle Scholar
  14. Chastain CJ, Botschner M, Harrington GS, Thompson BJ, Mills SE, Sarath G and Chollet R (2000) Further analysis of maize C4-pyruvate,orthophosphate dikinase phosphorylation by its bifunctional regulatory protein using selective substitutions of the regulatory Thr-456 and catalytic His-458 residues. Arch Biochem Biophys 375: 165–170PubMedCrossRefGoogle Scholar
  15. Chastain CJ, Fries JP, Vogel J., Randklev CL, Vossen AP, Dittmer SK, Watkins EE, Fiedler LJ, Wacker SA, Meinhover KC, Sarath G and Chollet R. (2002) Pyruvate, orthophosphate dikinase in leaves and ­chloroplasts of C3 plants undergoes light/dark-induced reversible phosphorylation. Plant Physiol 128: 1368–1378PubMedCrossRefGoogle Scholar
  16. Chastain CJ, Xu W, Parsley K, Sarath G, Hibberd JM and Chollet R (2008) The pyruvate, orthophosphate dikinase regulatory proteins of Arabidopsis possess a novel, unprecedented Ser/Thr protein kinase primary structure. Plant J 53: 854–63PubMedCrossRefGoogle Scholar
  17. Edwards GE, Nakamoto H, Burnell JN and Hatch MD (1985) Pyruvate Pi dikinase and NADP-malate dehydrogenase in C4 photosynthesis. Properties and mechanism of light/dark regulation. Annu Rev Plant Physiol 36: 255–286CrossRefGoogle Scholar
  18. Furbank RT, Chitty JA, Jenkins CLD, Taylor WC, Trevanion SJ, Caemmerer SV and Ashton AR (1997) Genetic manipulation of key photosynthetic enzymes in the C4 plant Flaveria bidentis. Aust J Plant Physiol 24: 477–485CrossRefGoogle Scholar
  19. Hampp R, Goller M and Ziegler H (1982) Adenylate levels, energy charge, and phosphorylation potential during dark-light and light-dark transition in chloroplasts, mitochondria, and cytosol of mesophyll protoplasts from Avena sativa L. Plant Physiol 69: 448–455PubMedCrossRefGoogle Scholar
  20. Hanks SK and Hunter T (1995) The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 9: 576–596PubMedGoogle Scholar
  21. Hardie DG (1999) Plant protein serine/threonine kinases: classification and functions. Annu Rev Plant Physiol Plant Mol Biol 50: 97–131PubMedCrossRefGoogle Scholar
  22. Herzberg O, Chen CCH, Kapadia G, McGuire M, Carroll LJ, Noh SJ and Dunaway-Mariano D (1996) Swiveling-domain mechanism for enzymatic phosphotransfer between remote reaction sites. Proc Natl Acad Sci USA 93: 2652–2657PubMedCrossRefGoogle Scholar
  23. Hulo N, Bairoch A, Bulliard V, Cerutti L, De Castro E, Langendijk-Genevaux PS, Pagni M and Sigrist CJA (2006) The PROSITE database. Nucleic Acids Res 34: D227–D230PubMedCrossRefGoogle Scholar
  24. Jenkins CLD and Hatch MD (1985) Properties and reaction mechanism of C4 leaf pyruvate, Pi dikinase. Arch Biochem Biophys 239: 53–62PubMedCrossRefGoogle Scholar
  25. Kubien DS, von Caemmerer S, Furbank RT and Sage R (2003) C4 photosynthesis at low temperature. A study using transgenic plants with reduced amounts of Rubisco. Plant Physiol 132: 1577–1585PubMedCrossRefGoogle Scholar
  26. Lim K, Read RJ, Chen CC, Tempczyk A, Wei M, Ye D, Wu C, Dunaway-Mariano D and Herzberg O (2007) Swiveling domain mechanism in pyruvate phosphate dikinase. Biochemistry 46:14845–14853PubMedCrossRefGoogle Scholar
  27. Lin Y, Lusin JD, Ye D, Dunaway-Mariano D and Ames JB (2006) Examination of the structure, stability, and catalytic potential in the engineered phosphoryl carrier domain of pyruvate phosphate dikinase. Biochemistry 45: 1702–1711PubMedCrossRefGoogle Scholar
  28. Majeran W, Cai Y and van Wijk KJ (2005) Functional differentiation of bundle sheath and mesophyll maize chloroplasts determined by comparative proteomics. Plant Cell 17: 3111–3140PubMedCrossRefGoogle Scholar
  29. Marshall JS, Ashton AR, Govers F and Hardham AR (2001) Isolation and characterization of four genes encoding pyruvate, phosphate dikinase in the oomycete plant pathogen Phytophthora cinnamomi. Curr Genet 40: 73–81PubMedCrossRefGoogle Scholar
  30. Maylan AN and Allison WS (2002) Properties of noncatalytic sites of thioredoxin-activated chloroplast coupling factor 1. Biochem Biophys Acta 1554: 153–158CrossRefGoogle Scholar
  31. Naidu SL and Long SP (2004) Potential mechanisms of low-temperature tolerance of C4 photosynthesis in Miscanthus x giganteus: an in vivo analysis. Planta 220: 145–155PubMedCrossRefGoogle Scholar
  32. Nakamoto H and Edwards GE (1986) Light activation of pyruvate,Pi dikinase and NADP-malate dehydrogenase in mesophyll protoplasts of maize. Effect of DCMU, antimycin A, CCCP, and phlorizin. Plant Physiol 82: 312–315PubMedCrossRefGoogle Scholar
  33. Nakamoto H and Young PS (1990) Light activation of pyruvate, orthophosphate dikinase in maize mesophyll chloroplasts: a role of adenylate energy charge. Plant Cell Physiol 31: 1–6Google Scholar
  34. Nakanishi T, Nakatsu T, Matsuoka M, Sakata K and Kato H (2005) Crystal structures of pyruvate phosphate dikinase from maize revealed an alternative conformation in the swiveling-domain motion. Biochemistry 44: 1136–1144PubMedCrossRefGoogle Scholar
  35. Ohta S, Usami S, Ueki J, Kumashiro T, Komari T and Burnell JN (1997) Identification of the amino acid residues responsible for cold tolerance in Flaveria brownii pyruvate,orthophosphate dikinase. FEBS Lett 403: 5–9PubMedCrossRefGoogle Scholar
  36. Pocalyko DJ, Carroll LJ, Martin BM, Babbitt PC and Dunaway-Mariano D (1990) Analysis of sequence homologies in plant and bacterial pyruvate phosphate dikinase enzyme I of the bacterial phosphoenolpyruvate: sugar phosphotransferase system and other PEP-utilizing enzymes. Identification of potential catalytic and regulatory motifs. Biochemistry 29: 10757–10765PubMedCrossRefGoogle Scholar
  37. Roeske CA and Chollet R (1987) Chemical modification of the bifunctional regulatory protein of maize leaf pyruvate, orthophosphate dikinase: evidence for two distinct active sites. J Biol Chem. 262: 12575–12582PubMedGoogle Scholar
  38. Roeske CA and Chollet R (1989) Role of metabolites in the reversible light activation of pyruvate,orthophosphate dikinase in Zea mays mesophyll cells in vivo. Plant Physiol 90: 330–337PubMedCrossRefGoogle Scholar
  39. Scheeff ED and Bourne PE (2005) Structural evolution of the protein kinase-like superfamily. PLoS Comput Biol 5: 359–381Google Scholar
  40. Sheen J (1991) Molecular mechanisms underlying the differential expression of maize pyruvate, orthophosphate dikinase genes. Plant Cell 3: 225–245PubMedGoogle Scholar
  41. Shirahashi K, Hayakawa S and Sugiyama T (1978) Cold lability of pyruvate, orthophosphate dikinase in the maize leaf. Plant Physiol 62: 826–830PubMedCrossRefGoogle Scholar
  42. Smith CM, Duff SMG and Chollet R (1994) Partial purification and characterization of maize-leaf pyruvate, orthophosphate dikinase regulatory protein: a low-abundance, mesophyll-chloroplast stromal protein. Arch Biochem Biophys 308: 200–206PubMedCrossRefGoogle Scholar
  43. Tjaden B, Plagens A, Dörr C, Siebers B and Hensel R (2006) Phosphoenolpyruvate synthetase and pyruvate, phosphate dikinase of Thermoproteus tenax: key pieces in the puzzle of archaeal carbohydrate metabolism. Mol Microbiol 60: 287–298PubMedCrossRefGoogle Scholar
  44. Usuda H (1988) Adenine nucleotide levels, the redox state of the NADP system, and assimilatory force in nonaqueously purified mesophyll chloroplasts from maize leaves under different light intensities. Plant Physiol 88: 1461–1468PubMedCrossRefGoogle Scholar
  45. von Caemmerer S and Furbank RT (1999) Modeling C4 photosynthesis. In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 173–211. Academic Press, San DiegoCrossRefGoogle Scholar
  46. Wang D, Portis AR, Moose SP and Long S (2008) Cool C4 photosynthesis: pyruvate Pi dikinase expression and activity corresponds to the exceptional cold tolerance of carbon assimilation in Miscanthus x giganteus. Plant Physiol 148: 557–567PubMedCrossRefGoogle Scholar
  47. Yamamoto E, Sugiyama T and Miyachi S (1974) Action spectrum for light activation of pyruvate, phosphate dikinase in maize leaves. Plant Cell Physiol 15: 987–992Google Scholar

Copyright information

© Springer Netherlands 2010

Authors and Affiliations

  1. 1.Department of BiosciencesMinnesota State University-MoorheadMoorheadUSA

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