, Volume 49, Issue 4, pp 481–496 | Cite as

CO2 sequestration in plants: lesson from divergent strategies

  • S. K. Vats
  • S. Kumar
  • P. S. Ahuja


Most organisms inhabiting earth feed directly or indirectly on the products synthesized by the reaction of photosynthesis, which at the current atmospheric CO2 levels operates only at two thirds of its peak efficiency. Restricting the photorespiratory loss of carbon and thereby improving the efficiency of photosynthesis is seen by many as a good option to enhance productivity of food crops. Research during last half a century has shown that several plant species developed CO2-concentrating mechanism (CCM) to restrict photorespiration under lower concentration of available CO2. CCMs are now known to be operative in several terrestrial and aquatic plants, ranging from most advanced higher plants to algae, cyanobacteria and diatoms. Plants with C4 pathway of photosynthesis (where four-carbon compound is the first product of photosynthesis) or crassulacean acid metabolism (CAM) may consistently operate CCM. Some plants however can undergo a shift in photosynthetic metabolism only with change in environmental variables. More recently, a shift in plant photosynthetic metabolism is reported at high altitude where improved efficiency of CO2 uptake is related to the recapture of photorespiratory loss of carbon. Of the divergent CO2 assimilation strategies operative in different oraganisms, the capacity to recapture photorespiratory CO2 could be an important approach to develop plants with efficient photosynthetic capacity.

Additional key words

aquatic carbon-concentrating mechanisms crassulacean acid metabolism C4 photosynthesis Rubisco 



carbonic anhydrase


crassulacean acid metabolism


CO2-concentrating mechanism




phosphoenolpyruvate carboxylase


phosphoenolpyruvate carboxykinase


pyruvate orthophosphate dikinase


Rubisco activase


ribulose-1,5-bisphosphate carboxylase/oxygenase


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.



The authors are thankful to the Council for Scientific and Industrial Research, New Delhi for support under the network project entitled “Exploratory studies on climate change and adaptation of species complexes (NWP-020). The manuscript bears IHBT publication number 1035.


  1. Andersson, I., Taylor, T.C.: Structural framework for catalysis and regulation in ribulose-1,5-bisphosphate carboxylase/oxygenase. — Arch. Biochem. Biophys. 414: 130–140, 2003.PubMedCrossRefGoogle Scholar
  2. Andrews, T.J., Whitney, S.M.: Manipulating ribulose bisphosphate carboxylase/oxygenase in the chloroplasts of higher plants. — Arch. Biochem. Biophys. 414: 159–169, 2003.Google Scholar
  3. Badger, M.R.: The role of carbonic anhydrases in photosynthetic CO2 concentrating mechanisms. — Photosynth. Res. 73: 83–94, 2003.CrossRefGoogle Scholar
  4. Badger, M.R., Hanson, D., Price, G.D.: Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria. — Funct. Plant Biol. 29: 161–173, 2002.CrossRefGoogle Scholar
  5. Badger, M.R., Price, G.D.: The role of carbonic anhydrase in photosynthesis. — Ann. Rev. Plant Physiol. Plant Mol. Biol. 45: 369–392, 1994.CrossRefGoogle Scholar
  6. Bainbridge, G., Madgwick, P., Parmar, S., Mitchell, R., Paul, M., Pitts, J., Keys, A.J., Parry, M.A.J.: Engineering Rubisco to change its catalytic properties. — J. Exp. Bot. 46: 1269–1276, 1995.Google Scholar
  7. Bandyopadhyay, A., Datta, K., Zhang, J., Yang, W., Raychaudhuri, S., Miyao, M., Datta, S.K.: Enhanced photosynthesis rate in genetically engineered indica rice expressing pepc gene cloned from maize. — Plant Sci. 172: 1204–1209, 2007.CrossRefGoogle Scholar
  8. Baroli, I., Niyogi, K.K.: Molecular genetics of xanthophyll-dependent photoprotection in green algae and plants. — Phil. Trans. R. Soc. Lond. 355: 1385–1393, 2000.CrossRefGoogle Scholar
  9. Beardall, J., Giordano, M.: Ecological implications of microalgal and cyanobacterial CO2 concentrating mechanisms, and their regulation. — Funct. Plant Biol. 29: 335–347, 2002.CrossRefGoogle Scholar
  10. Billings, W.D., Clebsch, E.E.C., Mooney, H.A.: Effects of low concentrations of carbon dioxide on photosynthesis rates of two races of Oxyria. — Science 133: 1834, 1961.PubMedCrossRefGoogle Scholar
  11. Blankenship, R.E.: Origin and early evolution of photosynthesis. — Photosynth. Res. 33: 91–111, 1992.PubMedCrossRefGoogle Scholar
  12. Borland, A.M., Griffiths, H., Maxwell, C., Broadmeadow, M.S.J., Griffiths, M.N., Barnes, J.D.: On the ecophysiology of the Clusiaceae in Trinidad: expression of CAM in Clusia minor L. during the transition from wet to dry season and characterization of three endemic species. — New Phytol. 122: 349–357, 1992.CrossRefGoogle Scholar
  13. Bowes, G., Ogren, W.L., Hageman, R.H.: Phospohglycolate production catalyzed by ribulose diphosphate carboxylase. — Biochem. Biophys. Res. Commun. 45: 716–722, 1971.PubMedCrossRefGoogle Scholar
  14. Bowes, G., Rao, S.K., Estavillo, G.M., Reiskind, J.B.: C4 mechanisms in aquatic angiosperms: comparisons with terrestrial C4 systems. — Funct. Plant Biol. 29: 379–392, 2002.CrossRefGoogle Scholar
  15. Bowes, G., Salvucci, M.E.: Plasticity in the photosynthetic carbon metabolism of submersed aquatic macrophytes. — Aquat. Bot. 34: 233–266, 1989.CrossRefGoogle Scholar
  16. Browse, J.A., Dromgoole, F.I., Brown, J.M.A.: Photosynthesis in the aquatic macrophyte Egeria densa. I. 14CO2 fixation at natural CO2 concentrations. — Aust. J. Plant Physiol. 4: 169–176, 1977.CrossRefGoogle Scholar
  17. Casati, P., Lara, M., Andreo, C.: Induction of a C4-like mechanism of CO2 fixation in Egeria densa, a submerged aquatic species. — Plant Physiol. 123: 1611–1622, 2000.PubMedCrossRefGoogle Scholar
  18. Chollet, R., Vidal, J., O’Leary, M.H.: Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. — Ann. Rev. Plant Physiol. Plant Mol. Biol. 47: 273–298, 1996.CrossRefGoogle Scholar
  19. Cheng, S.H., Moore, B.D., Edwards, G.E., Ku, M.S.B.: Photosynthesis in Flaveria brownii, a C4-Like species leaf anatomy, characteristics of CO2 exchange, compartmentation of photosynthetic enzymes, and metabolism of CO2. — Plant Physiol. 87: 867–873, 1988.PubMedCrossRefGoogle Scholar
  20. Chu, C., Dai, Z., Ku, M.S.B., Edwards, G.E.: Induction of Crassulacean Acid Metabolism in the facultative halophyte Mesembryanthemum crystallinum by abscisic acid. — Plant Physiol. 3: 1253–1260, 1993.Google Scholar
  21. Colman, B., Huertas, I.E., Bhatti, S., Dason, J.S.: The diversity of inorganic carbon acquisition mechanisms in eukaryotic microalgae. — Funct. Plant Biol. 29: 261–270, 2002.CrossRefGoogle Scholar
  22. Datta, S.K.: Rice biotechnology: A need for developing countries. — AgBioForum 7: 31–35, 2004.Google Scholar
  23. Decker, J.P.: Some effects of temperature and carbon dioxide concentration on photosynthesis of mimules. — Plant Physiol. 34: 103–106, 1959.PubMedCrossRefGoogle Scholar
  24. de Mattos, E.A., Lüttge, U.: Chlorophyll fluorescence and organic acid oscillations during transition from CAM to C3-photosynthesis in Clusia minor L. (Clusiaceae). — Ann. Bot. 88: 457–463, 2001.CrossRefGoogle Scholar
  25. Dencic, S.: Designing a wheat ideotype with increased sink capacity. — Plant Breed. 112: 311–317, 1994.CrossRefGoogle Scholar
  26. Dever, L.V., Blackwell, R.D., Fullwood, N.J., Lacuesta, M., Leegood, R.C., Onek, L.A., Pearson, M., Lea, P.J.: The isolation and characterization of mutants of the C4 photosynthetic pathway. — J. Exp. Bot. 46: 1363–1376, 1995.Google Scholar
  27. Dhingra, A., Portis, A. R., Daniell, H.: Enhanced translation of a chloroplast-expressed RbcS gene restores small subunit levels and photosynthesis in nuclear RbcS antisense plants. — Proc. Natl. Acad. Sci. 101: 6315–6320, 2004.PubMedCrossRefGoogle Scholar
  28. Dodd, A.N., Borland, A.M., Haslam, R.P., Griffiths, H., Maxwell, K.: Crassulacean acid metabolism: plastic, fantastic. — J. Exp. Bot. 53: 569–580, 2002.PubMedCrossRefGoogle Scholar
  29. Edwards, G.E., Sheta, E., Moore, B., Dai, Z., Fransceschi, V.R., Cheng, S.H., Lin, C.H., Ku, M.S.B.: Photosynthetic characteristics of cassava (Manihot esculenta Crantz), a C3 species with chlorenchymatous bundle sheath cells. — Plant Cell Physiol. 31: 1199–1206, 1990.Google Scholar
  30. Ehleringer, J.R., Sage, R.F., Flanagan, L.B., Pearcy, R.W.: Climate change and the evolution of C4 photosynthesis. — Trends Ecol. Evol. 6: 95–99, 1991.PubMedCrossRefGoogle Scholar
  31. Ellis, R.J.: The most abundant protein in the world. — Trends Biochem. Sci. 4: 241–244, 1979.CrossRefGoogle Scholar
  32. El-Sharkawy, M.A.: Pioneering research on C4 leaf anatomical, physiological, and agronomic characteristics of tropical monocot and dicot plant species: Implications for crop water relations and productivity in comparison to C3 cropping systems. — Photosynthetica 47: 163–183, 2009.CrossRefGoogle Scholar
  33. Evans, J.R.: Photosynthetic acclimation and nitrogen partitioning within a lucerne canopy. I. Canopy Characteristics. — Aust. J. Plant Physiol. 20: 55–67, 1993.CrossRefGoogle Scholar
  34. Feller, U., Crafts-Brandner, S.J., Salvucci, M.E.: Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activasemediated activation of Rubisco. — Plant Physiol. 116: 539–546, 1998.PubMedCrossRefGoogle Scholar
  35. Friend, A.D., Woodward, F.I.: Evolutionary and ecophysiological responses of mountain plants to the growing season environment. — Adv. Ecol. Res. 20: 59–124, 1990.CrossRefGoogle Scholar
  36. Furbank, R.T., Jenkins, C.L.D., Hatch, M.D.: CO2 concentrating mechanism of C4 photosynthesis: permeability of isolated bundle sheath cells to inorganic carbon. — Plant Physiol. 91: 1364–1371, 1989.PubMedCrossRefGoogle Scholar
  37. Furbank, R.T., Jenkin, C.L.D., Hatch, M.D.: C4 photosynthesis: quantum requirement, C4 acid overcycling and Q-cycle involvement. — Aust. J. Plant Physiol. 17: 1–7, 1990.CrossRefGoogle Scholar
  38. Galmes, J., Flexas, J., Keys, A.J., Cifre, J., Mitchell, R.A.C., Madgwick, P.J., Haslam, R.P., Medrano, H., Parry, M.A.J.: Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves. — Plant Cell Environ. 28: 571–579, 2005.CrossRefGoogle Scholar
  39. Gehlen, J., Panstruga, R., Smets, H., Merkelbach, S., Kleines, M., Porsch, P., Fladung, M., Becker, I., Rademacher, T., Häusler R.E., Hirsch, H.J.: Effects of altered phosphoenolpyruvate carboxylase activities on the transgenic C3 plant Solanum tuberosum. — Plant Mol. Biol. 32: 831–848, 1996.PubMedCrossRefGoogle Scholar
  40. Grams, T.E.E., Thiel, S.: A light induced switch from C3-photosynthesis to Crassulacean acid metabolism is mediated by UV-A/blue light. — J. Exp. Bot. 53: 1475–1483, 2002.PubMedCrossRefGoogle Scholar
  41. Guralnick, L.J., Ku, M.S.B., Edwards, G.E., Strand, D., Hockema, B., Earnest, J.: Induction of PEP carboxylase and Crassulacean acid metabolism by gibberellic acid in Mesembryanthemum crystallinum. — Plant Cell Physiol. 42: 236–239, 2001.PubMedCrossRefGoogle Scholar
  42. Haag-Kerwer, A., Franco, A.C., Lüttge, U.: The effect of temperature and light on gas exchange and acid accumulation in the C3-CAM plant Clusia minor L. — J. Exp. Bot. 43: 345–352, 1992.CrossRefGoogle Scholar
  43. Hanson, D., Andrews, T.J., Badger, M.R.: Variability of the pyrenoid-based CO2 concentrating mechanism in hornworts (Anthocerotophyta). — Funct. Plant Biol. 29: 407–416, 2002.CrossRefGoogle Scholar
  44. Hatch, M.D., Burnell, J.N.: Carbonic anhydrase activity in leaves and its role in the first step of C4 photosynthesis. — Plant Physiol. 93: 380–383, 1990.CrossRefGoogle Scholar
  45. Häusler, R.E., Rademacher, T., Li, J., Lipka, V., Fischer, K.L., Schubert, S., Kreuzaler, F., Hirsch, H.J.: Single and double overexpression of C-4-cycle genes had differential effects on the pattern of endogenous enzymes, attenuation of photorespiration and on contents of UV protectants in transgenic potato and tobacco plants. — J. Exp. Bot. 52: 1785–1803, 2001.PubMedCrossRefGoogle Scholar
  46. Häusler, R.E., Hirsch, H.J., Kreuzaler, F., Peterhansel, C.: Overexpression of C4-cycle enzymes in transgenic C3 plants: a biotechnological approach to improve C3 photosynthesis [Review]. — J. Exp. Bot. 53: 591–607, 2002.PubMedCrossRefGoogle Scholar
  47. Havaux, M., Niyogi, K.K.: The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. — Proc. Natl. Acad. Sci. 96: 8762–8767, 1999.PubMedCrossRefGoogle Scholar
  48. Henkes, S., Sonnewald, U., Badur, R., Flachmann, R., Stitt, M.: A small decrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism. — Plant Cell 13: 535–551, 2001.PubMedCrossRefGoogle Scholar
  49. Herring, R.J.: Opposition to transgenic technologies: ideology, interests and collective action frames. — Nat. Rev. Genet. 9: 458–463, 2008.PubMedCrossRefGoogle Scholar
  50. Holaday, A.S., Bowes, G.: C4 acid metabolism and dark CO2 fixation in a submerged aquatic macrophyte (Hydrilla verticillata). — Plant Physiol. 65: 331–335, 1980.PubMedCrossRefGoogle Scholar
  51. Holtum, J.A.M.: Crassulacean acid metabolism: plastic in expression, complexity of control — J. Exp. Bot. 53: 657–661, 2002.Google Scholar
  52. Hudspeth, R.L., Grula, J.W., Dai, Z., Edwards, G.E., Ku, M.S.B.: Expression of maize phosphoenolpyruvate carboxylase in transgenic tobacco. — Plant Physiol. 98: 458–464, 1992.PubMedCrossRefGoogle Scholar
  53. Huertas, I.E., Colman, B., Espie, G.S.: Inorganic carbon acquisition and its energization in eustigmatophyte algae. — Funct. Plant Biol. 29: 271–277, 2002.CrossRefGoogle Scholar
  54. Innes, P., Blackwell, R.D.: Some effects of leaf posture on the yield and water economy of winter wheat. — J. Agric. Sci. 101: 367–376, 1983.CrossRefGoogle Scholar
  55. Ishimaru, K., Ishikawa, I., Matsuoka, M., Ohsugi, R.: Analysis of a C4 maize pyruvate, orthophosphate dikinase expressed in C3 transgenic Arabidopsis plants. — Plant Sci. 129: 57–64, 1997.CrossRefGoogle Scholar
  56. Jiao, D.M., Li, X., Ji, B.H.: Photoprotective effects of high level expression of C4 phosphoenolpruvate carboxylase in transgenic rice during photoinhibition. — Photosynthetica 43: 501–508, 2005.CrossRefGoogle Scholar
  57. Kaplan, A., Reinhold, L.: CO2 concentrating mechanisms in photosynthetic microorganisms. — Ann. Rev. Plant Physiol. Plant Mol. Biol. 50: 539–570, 1999.CrossRefGoogle Scholar
  58. Kaplan, A., Helman, Y., Tchernov, D., Reinhold, L.: Acclimation of photosynthetic microorganisms to changing ambient CO2 concentration. — Proc. Natl. Acad. Sci. 98: 4817–4818, 2001.PubMedCrossRefGoogle Scholar
  59. Keeley, J.E.: Isoettis howellii: a submerged aquatic CAM plant. — Am. J. Bot. 68: 420–424, 1981.CrossRefGoogle Scholar
  60. Keeley, J.E.: C4 photosynthetic modifications in the evolutionary transition from land to water in aquatic grasses. — Oecologia 116: 85–97, 1998.CrossRefGoogle Scholar
  61. Keeley, J.E.: Photosynthetic pathway diversity in a seasonal pool community. — Funct. Ecol. 13:106–118, 1999.CrossRefGoogle Scholar
  62. Keys, A.J., Major, I., Parry, M.A.J.: Is there another player in the game of Rubisco regulation? — J. Exp. Bot. 46: 1245–1251, 1995.Google Scholar
  63. Khan, S., Andralojc, P.J., Lea, P.J., Parry, M.A.J.: Carboxy-Darabitinol 1-phosphate protects ribulose 1,5-bisphosphate carboxylase/oxygenase against proteolytic breakdown. — Eur. J. Biochem. 266: 840–847, 1999.PubMedCrossRefGoogle Scholar
  64. Koch, K., Kennedy, R.A.: Characteristics of Crassulacean acid metabolism in the succulent C4 dicot, Portulaca oleracea L. — Plant Physiol. 65: 193–197, 1980.PubMedCrossRefGoogle Scholar
  65. Körner, C., Diemer, M.: In situ photosynthesis responses to light, temperature and carbon dioxide in herbaceous plants from low and high altitude. — Funct. Ecol. 1: 179–194, 1987.CrossRefGoogle Scholar
  66. Körner, C., Diemer, M.: Evidence that plants from high altitude retains their greater photosynthetic efficiency under elevated CO2. — Funct. Ecol. 8: 58–68, 1994.CrossRefGoogle Scholar
  67. Kostov, R.V., Small, C.L., McFadden, B.A.: Mutations in a sequence near the N-terminus of the small subunit alters the CO2/O2 specificity factor for ribulose bisphosphate carboxylase/oxygenase. — Photosynth. Res. 54: 127–134, 1997.CrossRefGoogle Scholar
  68. Ku, M.S.B., Agarie, S., Nomura, M., Fukayama, H., Tsuchida, H., Ono, K., Hirose, S., Toki, S., Miyao, M., Matsuoka, M.: High level expression of maize phosphoenolpyruvate carboxylase in transgenic rice plants. — Nat. Biotechnol. 17: 76–80, 1999.PubMedCrossRefGoogle Scholar
  69. Kumar, N., Kumar, S., Ahuja, P.S.: Photosynthetic characteristics of Hordeum, Triticum, Rumex, and Trifolium species at contrasting altitudes. — Photosynthetica 43: 195–201, 2005.CrossRefGoogle Scholar
  70. Kumar, N., Kumar, S., Vats, S.K., Ahuja, P.S.: Effect of altitude on the primary products of photosynthesis and the associated enzymes in barley and wheat. — Photosynth. Res. 88: 63–71, 2006.PubMedCrossRefGoogle Scholar
  71. Kumar, N., Vats, S.K., Kumar, S., Ahuja, P.S.: Altitude-related changes in activities of carbon metabolism enzymes in Rumex nepalensis. — Photosynthetica 46: 611–614, 2008.CrossRefGoogle Scholar
  72. Latzko, E., Kelly, G.J.: The many-faceted function of phosphoenolpyruvate carboxylase in C3 plants. — Physiol. Vég. 21: 805–815, 1983.Google Scholar
  73. Leegood, R.C.: C4 photosynthesis: principles of CO2 concentration and prospects for its introduction into C3 plants. — J. Exp. Bot. 53: 581–590, 2002.PubMedCrossRefGoogle Scholar
  74. Long, S.P., Ainsworth, E.A., Rogers, A., Ort, D.R.: Rising atmospheric carbon dioxide: plants face their future. — Ann. Rev. Plant Biol. 55: 591–628, 2004.CrossRefGoogle Scholar
  75. Long, S.P., Ainsworth, E.A., Leakey, A.D.B., Morgan, P.B.: Global food insecurity. Treatment of major food crops with elevated carbon dioxide or ozone under large-scale fully open-air conditions suggests recent models may have overestimated future yields Phil. Trans. Royal Soc. B: — Biol. Sci. 360: 2011–2020, 2005.CrossRefGoogle Scholar
  76. Long, S.P., Zhu, X.G., Naidu, S.L., Ort, D.R.: Can improvement in photosynthesis increase crop yields? — Plant Cell Environ. 29: 315–330, 2006.PubMedCrossRefGoogle Scholar
  77. Lu, Z.M., Percy, R.G., Qualset, C.O., Zeiger, E.: Stomatal conductance predicts yields in irrigated Pima cotton and bread wheat grown at high temperatures. — J. Exp. Bot. 49: 453–460, 1998.CrossRefGoogle Scholar
  78. Lüttge, U.: Ecophysiology of Crassulacean acid metabolism (CAM). — Ann. Bot. 93: 629–652, 2004.PubMedCrossRefGoogle Scholar
  79. Maberly, S.C.: Diel, episodic and seasonal changes in pH and concentrations of inorganic carbon in a productive English Lake, Esthwaite Water, Cumbria. — Freshwater Biol. 35: 579–598, 1996.CrossRefGoogle Scholar
  80. Maberly, S.C., Madsen, T.V.: Freshwater angiosperm carbon concentrating mechanisms: processes and patterns. — Funct. Plant Biol. 29: 393–405, 2002.CrossRefGoogle Scholar
  81. Madsen, T.V.: Interactions between internal and external CO2 pools in the photosynthesis of the aquatic CAM plants Littorella uniflora (L.) Aschers and Isoetes lacustris L. — New Phytol. 106: 35–50, 1987.CrossRefGoogle Scholar
  82. Madsen, T.V., Sand-Jensen, K.: Photosynthetic carbon assimilation in aquatic macrophytes. — Aquatic Bot. 41: 5–40, 1991.CrossRefGoogle Scholar
  83. Magnin, N.C., Cooley, B.A., Reiskind, J.B., Bowes, G.: Regulation and localization of key enzymes during the induction of Kranz-less, C4-type photosynthesis in Hydrilla verticillata. — Plant Physiol. 115: 1681–1689, 1997.PubMedGoogle Scholar
  84. Matsuoka, M., Furbank, R.T., Fukayama, H., Miyao, M.: Molecular engineering of C4 photosynthesis. — Ann. Rev. Plant Physiol. Plant Mol. Biol. 52: 297–314, 2001.CrossRefGoogle Scholar
  85. Medrano, H., Parry, M.A.J., Socias, X., Lawlor, D.W.: Longterm water stress inactivates Rubisco in subterranean clover. — Ann. Appl. Biol. 131: 491–501, 1997.CrossRefGoogle Scholar
  86. Melzer, E., O’Leary, M.H.: Anapleurotic CO2 fixation by phosphoenolpyruvate carboxylase in C3 plants. — Plant Physiol. 84: 58–60, 1987.PubMedCrossRefGoogle Scholar
  87. Mercado, J.M., Andría, J.R., Pérez-Llorens, J.L., Vergara, J.J., Axelsson, L.: Evidence for a plasmalemma-based CO2 concentrating mechanism in Laminaria saccharina. — Photosynth. Res. 88: 259–268, 2006.PubMedCrossRefGoogle Scholar
  88. Miller, A.G., Espie, G.S., Canvin, D.T.: Physiological aspects of CO2 and HCO3 transport by cyanobacteria: a review. — Can. J. Bot. 68: 1291–1302, 1990.CrossRefGoogle Scholar
  89. Miyagawa, Y., Tamoi, M., Shigeoka, S.: Overexpression of a cyanobacterial fructose-1,6-/sedoheptulose-1,7-bisphosphatase in tobacco enhances photosynthesis and growth. — Nature Biotechnol. 19: 965–969, 2001.CrossRefGoogle Scholar
  90. Miyao, M.: Molecular evolution and genetic engineering of C4 photosynthetic enzymes. — J. Exp. Bot. 54: 179–189, 2003.PubMedCrossRefGoogle Scholar
  91. Miyao, M., Fukayama, H.: Metabolic consequences of overproduction of phosphoenolpyruvate carboxylase in C3 plants. — Arch. Biochem. Biophys. 414: 197–203, 2003.PubMedGoogle Scholar
  92. Mooney, H.A., Strain, B.R., West, M.: Photosynthetic efficiency at reduced carbon dioxide tensions. — Ecology 47: 490–491, 1966.CrossRefGoogle Scholar
  93. Moore, P.D.: Mixed metabolism in plant pools. — Nature 399: 109–110, 1999.CrossRefGoogle Scholar
  94. Moroney, J.V., Bartlett, S.G., Samuelsson, G.: Carbonic anhydrase in plants and algae. — Plant Cell Environ. 24: 141–153, 2001.CrossRefGoogle Scholar
  95. Moroney, J.V., Somanchi, A.: How do microalgae concentrate CO2 to increase the efficiency of photosynthetic carbon fixation? — Plant Physiol. 119: 9–16, 1999.PubMedCrossRefGoogle Scholar
  96. Moroney, J.V., Ynalvez, R.A.: A proposed carbon dioxide concentration mechanism in Chlamydomonas reinhardtii. — Eukaryotic Cell 6: 1251–1259, 2007.PubMedCrossRefGoogle Scholar
  97. Nelson, T., Langdale, J.A.: Developmental genetics of C4 photosynthesis. — Ann. Rev. Plant Physiol. Plant Mol. Biol. 43: 25–47, 1992.CrossRefGoogle Scholar
  98. Nievola, C., Kraus, J., Freschi, L., Souza, B., Mercier, H.: Temperature determines the occurrence of CAM or C3 photosynthesis in pineapple plantlets grown in vitro. — In Vitro Cellular Develop. Biol. Plant. 41: 832–837, 2005.CrossRefGoogle Scholar
  99. Nishio, J.N., Ting, I.P.: Photosynthetic characteristics of the palisade mesophyll and spongy mesophyll in the CAM/C4 intermediate plant Peperomia camptotricha. — Bot. Acta 106: 120–125, 1993.Google Scholar
  100. Nobel, P.S., Hartsock, T.L.: Drought-induced shifts in daily CO2 uptake patterns for leafy cacti. — Physiol. Plant. 70: 114–118, 1987.CrossRefGoogle Scholar
  101. Ogren, W.L., Bowes, G.: Ribulose diphosphate carboxylase regulates soybean photorespiration. — Nature-New Biol. 230: 159–160, 1971.PubMedGoogle Scholar
  102. Ort, D.R., Long, S.P.: Converting solar energy into crop production. — In: Chrispeels, M.J., Sadava, D.E. (ed.): Converting Solar Energy into Crop Production. Pp. 240–269. Amer. Soc. Plant Biol., Boston 2003.Google Scholar
  103. Palmqvist, K., Sültemeyer, D., Baldet, P., Andrews, T.J., Badger, M.R.: Characterization of inorganic carbon fluxes, carbonic anhydrase(s) and ribulose-1,5-bisphosphate carboxylase-oxygenase in the green unicellular alga Coccomyxa: comparison with low-CO2 cells of Chlamydomonas reinhardtii. — Planta 197: 352–361, 1995.CrossRefGoogle Scholar
  104. Pandey, O.P., Bhadula, S.K., Purohit, A.N.: Changes in the activity of some photosynthetic and photorespiratory enzymes in Selinum vaginatum Clarke, grown at two altitudes. — Photosynthetica 18: 153–155, 1984.Google Scholar
  105. Parry, M.A.J., Andralojc, P.J., Mitchell, R.A.C., Madgwick, P.J., Keys, A.J.: Manipulation of Rubisco: the amount, the activity, function and regulation. — J. Exp. Bot. 54: 1321–1333, 2003.PubMedCrossRefGoogle Scholar
  106. Parry, M.A.J., Keys, A.J., Madgwick, P.J., Carmo-Silca, A.E., Andralojc, P.J.: Rubisco regulation: a role for inhibitors. — J. Exp. Bot. 59: 1569–1580, 2008.PubMedCrossRefGoogle Scholar
  107. Paul, M.J., Cockburn, W.: The stimulation of CAM activity in Mesembryanthemum crystallinum in nitrate- and phosphatedeficient conditions. — New Phytol. 114: 391–398, 1990.CrossRefGoogle Scholar
  108. Price, G.D., Badger, M.R.: Advances in understanding how aquatic photosynthetic organisms utilize sources of dissolved inorganic carbon for CO2 fixation. — Funct. Plant Biol. 29: 117–121, 2002.CrossRefGoogle Scholar
  109. Price, G.D., von Caemmerer, S., Evans, J.R., Yu, J.-W., Lloyd, J., Oja, V., Kell, P., Harrison, K., Gallagher, A., Badger, M.R.: Specific reduction of chloroplast carbonic anhydrase activity by antisense RNA in transgenic tobacco plants has a minor effect on photosynthetic CO2 assimilation. — Planta 193: 331–340, 1994.CrossRefGoogle Scholar
  110. Prins, H.B.A., Snel, J.F.H., Zanstra, P.E., Helder, R.J.: The mechanism of bicarbonate assimilation by the polar leaves of Potamogeton and Elodea. CO2 concentrations at the leaf surface. — Plant Cell Environ. 5: 207–214, 1982.Google Scholar
  111. Pyke, K.A., Leech, R.M.: Cellular levels of ribulose 1,5bisphosphate carboxylase and chloroplast compartment size in wheat mesophyll cells. — J. Exp. Bot. 38: 1949–1956, 1987.CrossRefGoogle Scholar
  112. Raines, C.A.: Transgenic approaches to manipulate the environmental responses of the C3 carbon fixation cycle. — Plant Cell Environ. 29: 331–339, 2006.PubMedCrossRefGoogle Scholar
  113. Raven, J.A.: Exogenous inorganic carbon sources in plant photosynthesis — Biol. Rev. 45: 167–221, 1970.CrossRefGoogle Scholar
  114. Raven, J.A.: Inorganic carbon concentrating mechanisms in relation to the biology of algae. — Photosynth. Res. 77: 155–171, 2003.PubMedCrossRefGoogle Scholar
  115. Reddy, A.R., Sundar, D., Gnanam A.: Photosynthetic flexibility in Pedilanthus tithymaloides Poit, a CAM plant. — J. Plant Physiol. 160: 75–80, 2003.PubMedCrossRefGoogle Scholar
  116. Reinfelder, J.R., Kraepiel, A.M., Morel, F.M.M.: Unicellular C4 photosynthesis in a marine diatom. — Nature 407: 996–999, 2000.PubMedCrossRefGoogle Scholar
  117. Reiskind, J.B., Madsen, T.V., van Ginkel, L.C., Bowes, G.: Evidence that inducible C4-type photosynthesis is a chloroplastic CO2-concentrating mechanism in Hydrilla, a submersed monocot. — Plant Cell Environ. 20: 211–220, 1997.CrossRefGoogle Scholar
  118. Reynolds, M., Foulkes, M.J., Slafer, G.A., Berry, P., Parry, M.A.J., Snape, J.W., Angus, W.J.: Raising yield potential in wheat. — J. Exp. Bot. 60: 1899–1918, 2009.PubMedCrossRefGoogle Scholar
  119. Reynolds, M.P., van Ginkel, M., Ribaut, J.M.: Avenues for genetic modification of radiation use efficiency in wheat. — J. Exp. Bot. 51: 459–473, 2000.PubMedCrossRefGoogle Scholar
  120. Richards, R.A.: Selectable traits to increase crop photosynthesis and yield of grain crops. — J. Exp. Bot. 51: 447–458, 2000.PubMedCrossRefGoogle Scholar
  121. Riebesell, U.: Carbon fix for a diatom. — Nature 407: 959–960, 2000.PubMedCrossRefGoogle Scholar
  122. Rivero, R.M., Kojima, M., Gepstein, A., Sakakibara, H., Mittler, R., Gepstein, S., Blumwald, E.: Delayed leaf senescence induces extreme drought tolerance in a flowering plant. — Proc. Natl. Acad. Sci., USA. B: 19631–19636, 2007.Google Scholar
  123. Robinson, S.P., Portis, A.R.: Release of the nocturnal inhibitor, carboxyarabinitol-1-phosphate, from ribulose bisphosphate carboxylase oxygenase by Rubisco activase. — FEBS Letters 233: 413–416, 1988.CrossRefGoogle Scholar
  124. Rokka, A., Zhang, L., Aro, E.: Rubisco activase: an enzyme with a temperature-dependent dual function? — Plant J. 25: 463–471, 2001.PubMedCrossRefGoogle Scholar
  125. Rotatore, C., Lew, R.R., Colman, B.: Active uptake of CO2 during photosynthesis in the green alga Eremosphaera viridis is mediated by a CO2-ATPase. — Planta 188: 539–545, 1992.CrossRefGoogle Scholar
  126. Sage, R.F.: Are crassulacean acid metabolism and C4 photosynthesis incompatible? — Funct. Plant Biol. 29: 775–785, 2002a.CrossRefGoogle Scholar
  127. Sage, R.F.: C4 photosynthesis in terrestrial plants does not require Kranz anatomy. — Trends Plant Sci. 7: 283–285, 2002b.PubMedCrossRefGoogle Scholar
  128. Sage, R.F., Coleman, J.R.: Effects of low atmospheric CO2 on plants: more than a thing of the past. — Trends Plant Sci. 6: 18–24, 2001.PubMedCrossRefGoogle Scholar
  129. Salisbury, F.B., Ross, C.W.: CO2 fixation in succulent species (Crassulacean Acid Metabolism). — In: Salisbury, F.B., Ross, C.W. (ed.): Plant Physiology. Pp. 207–209. CBS Publishers and Distributors, Delhi 1986.Google Scholar
  130. Salvucci, M.E., Bowes, G.: Induction of reduced photorespiratory activity in submersed and amphibious aquatic macrophytes. — Plant Physiol. 67: 335–340, 1981.PubMedCrossRefGoogle Scholar
  131. Salvucci, M.E., Bowes, G.: Two photosynthetic mechanisms mediating the low photorespiratory state in submersed aquatic angiosperms. — Plant Physiol. 73: 488–496, 1983.PubMedCrossRefGoogle Scholar
  132. Somerville, C.R.: An early Arabidopsis demonstration. Resolving a few issues concerning photorespiration. — Plant Physiol. 125: 20–24, 2001.PubMedCrossRefGoogle Scholar
  133. Spencer, W.E., Wetzel, R.G., Teeri, J.: Photosynthetic phenotype plasticity and the role of phosphoenolpyruvate carboxylase in Hydrilla verticillata. — Plant Sci. 118: 1–9, 1996.CrossRefGoogle Scholar
  134. Spreitzer, R.J.: Role of the small subunit in ribulose-1,5-bisphosphate carboxylase/oxygenase. — Arch. Biochem. Biophys. 414: 141–149, 2003.PubMedCrossRefGoogle Scholar
  135. Spreitzer, R.J., Salvucci, M.E.: Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. — Ann. Rev. Plant. Biol. 53: 449–475, 2002.CrossRefGoogle Scholar
  136. Streb, P., Shang, W., Feierabend, J., Bligny, R.: Divergent strategies of photoprotection in high-mountain plants. — Planta 207: 313–324, 1998.CrossRefGoogle Scholar
  137. Surridge, C.: Agricultural biotech: the rice squad. — Nature 416: 576–578, 2002.PubMedCrossRefGoogle Scholar
  138. Suzuki, S., Murai, N., Burnell, J., Arai, M.: Changes in photosynthetic carbon flow in transgenic rice plants that expess C4-type phosphoenolpyruvate carboxykinase from Urochloa panicoides. — Plant Physiol. 124: 163–172, 2000.PubMedCrossRefGoogle Scholar
  139. Swaminathan, M.S.: An evergreen revolution. — Crop Sci. 46: 2293–2303, 2006.CrossRefGoogle Scholar
  140. Tabita, F.R.: Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: A different perspective — Photosynth. Res. 60: 1–28, 1999.CrossRefGoogle Scholar
  141. Takeda, S., Matsuoka, M.: Genetic approaches to crop improvement: responding to environmental and population changes. — Nat. Rev. Genet. 9: 444–457, 2008.PubMedCrossRefGoogle Scholar
  142. Takeuchi, Y., Akagi, H., Kamasawa, N., Osumi, M., Honda, H.: Aberrant chloroplasts in transgenic rice plants expressing a high level of maize NADP-dependent malic enzyme. — Planta 211: 265–274, 2000.PubMedCrossRefGoogle Scholar
  143. Thomas, H., Howarth, C.J.: Five ways to stay green. — J. Exp. Bot. 51: 329–337, 2000.PubMedCrossRefGoogle Scholar
  144. Tiwari, A., Kumar, P., Singh, S., Ansari, S.A.: Carbonic anhydrase in relation to higher plants. — Photosynthetica 43: 1–11, 2005.CrossRefGoogle Scholar
  145. Tollenaar, M., Wu, J.: Yield improvement in temperate maize is attributable to greater stress tolerance. — Crop Sci. 39: 1597–1604, 1999.CrossRefGoogle Scholar
  146. Tregunna, E.B., Smith, B.N., Berry, J.A., Downton, W.J.S.: Some methods for studying the photosynthetic taxonomy of the angiosperms. — Can J. Bot. 48: 1209–1214, 1970.CrossRefGoogle Scholar
  147. Uchino, A., Samejima, M., Ishii, R., Ueno, O.: Photosynthetic carbon metabolism in an amphibious sedge, Eleocharis baldwinii (Torr.) Chaman: modified expression of C4 characteristics under submerged aquatic conditions. — Plant Cell Physiol. 36: 229–238, 1995.Google Scholar
  148. Uemura, K., Suzuki, Y., Shikanai, T., Wadano, A., Jensen, R.G., Chmara, W., Yokota, A.: A rapid and sensitive method for determination of relative specificity of Rubisco from various species by anion exchange chromatography. — Plant Cell Physiol. 37: 325–331, 1996.Google Scholar
  149. Uemura, K., Miyachi, A.S., Yokota, A.: Ribulose-1,5-bisphosphate carboxylase/oxygenase from thermophilic red algae with a strong specificity for CO2 fixation. — Biochem. Biophys. Res. Comm. 233: 568–571, 1997.PubMedCrossRefGoogle Scholar
  150. Ueno, O., Samejima, M., Muto, S., Miyachi, S.: Photosynthetic characteristics of an amphibious plant Eleocharis vivipara: expression of C4 and C3 modes in contrasting environments. — Proc. Natl. Acad. Sci. USA 85: 6733–6737, 1988.PubMedCrossRefGoogle Scholar
  151. Ueno, O.: Induction of Kranz anatomy and C4-like biochemical characteristics in a submerged amphibious plant by abscisic acid. — Plant Cell 10: 571–583, 1998.PubMedCrossRefGoogle Scholar
  152. Vats, S.K., Kumar, S.: Photosynthetic response of Podophyllum hexandrum Royle from different altitudes in Himalayan ranges. — Photosynthetica 44: 136–139, 2006.CrossRefGoogle Scholar
  153. von Caemmerer, S.: C4 photosynthesis in a single C3 cell is theoretically inefficient but may ameliorate internal CO2 diffusion limitations of C3 leaves. — Plant Cell Environ. 26: 1191–1197, 2003.CrossRefGoogle Scholar
  154. von Caemmerer, S., Quinn, V., Hancock, N.C., Price, G.D., Furbank, R.T., Ludwig, M.: Acclimation of photosynthetic microorganisms to changing ambient CO2 concentration. — Proc. Natl. Acad. Sci. 98: 4817–4818, 2001.CrossRefGoogle Scholar
  155. Voznesenskaya, E.V., Franceschi, V.R., Kiirats, O., Freitag, H., Edwards, G.E.: Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. — Nature 414: 543–546, 2001.PubMedCrossRefGoogle Scholar
  156. Voznesenskaya, E.V., Franceschi, V.R., Kiirats, O., Artyusheva, E.G., Freitag, H., Edwards, G.E.: Proof of C4 photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodiaceae). — Plant J. 31: 649–662, 2002.PubMedCrossRefGoogle Scholar
  157. Wanek, W., Huber, W., Arndt, S.K., Popp, M.: Mode of photosynthesis during different life stages of hemiepiphytic Clusia species. — Funct. Plant Biol. 29: 725–732, 2002.CrossRefGoogle Scholar
  158. Williams, T.G., Flanagan, L.B., Coleman, J.R.: Photosynthetic gas exchange and discrimination against 13CO2 and C18O16O in tobacco plants modified by an antisense construct to have low chloroplastic carbonic anhydrase. — Plant Physiol. 112: 319–326, 1996.PubMedGoogle Scholar
  159. Wingler, A., Lea, P.J., Quick, W.P., Leegood, R.C.: Photorespiration: metabolic pathways and their role in stress protection. — Phil Trans R Soc Lond B 355: 1517–1529, 2000.CrossRefGoogle Scholar
  160. Winter, K., Gademann, R.: Daily changes in CO2 and water vapour exchange, chlorophyll fluorescence, and leaf water relations in the halophyte Mesembryanthemum crystallinum during the induction of crassulacean acid metabolism in response to high NaCl salinity. — Plant Physiol. 95: 768–776, 1991.PubMedCrossRefGoogle Scholar
  161. Winter, K., Garcia, M., Holtum, J.A.M.: On the nature of facultative and constitutive CAM: environmental and developmental control of CAM expression during early growth of Clusia, Kalanchoë, and Opuntia. — J. Exp. Bot. 59: 1829–1840, 2008.PubMedCrossRefGoogle Scholar
  162. Winter, K., Smith, J.A.C.: Introduction to crassulacean acid metabolism: biochemical principles and ecological diversity. — In: Winter, K., Smith, J.A.C. (ed.): Crassulacean Acid Metabolism: Biochemistry, Ecophysiology and Evolution. Pp 1–13. Springer-Verlag, Berlin 1996.CrossRefGoogle Scholar
  163. Wu, D.X., Shu, Q.Y. Wang, Z.H., Cui, H.R., Xia, Y.W.: Quality variations in transgenic rice with a synthetic cry1Ab gene from Bacillus thuringiensis. — Plant Breed. 121: 198–202, 2002.CrossRefGoogle Scholar
  164. Zhang, B.J., Ling, L.L., Wang, R.F., Jiao, D.M.: Photosynthetic characteristics and effect of ATP in transgenic rice with phosphoenolpyruvate carboxylase and pyruvate orthophosphate dikinase genes — Photosynthetica 47: 133–136, 2009.CrossRefGoogle Scholar
  165. Zotz, G., Winter, K.: Diel patterns of CO2 exchange in rainforest canopy plants. — In: Mulkey, S.S., Chazdon, R.L., Smith, A.P. (ed.): Tropical Forest Plant Ecophysiology. Pp 89–113. Chapman & Hall, New York 1996.CrossRefGoogle Scholar
  166. Zhu, G., Kurek, I., True, T., Zhang, X., Majumdar, M., Liu, L., Lassner, M.: Enhancing photosynthesis by improving Rubisco carboxylase activity and specificity, and Rubisco activase thermostability through DNA shuffling. — In: Van der Est, A., Bruce, D. (ed.): Photosynthesis: Fundamental Aspects to Global Perspectives. Proc. 13th International Congress on Photosynthesis, Montreal 2004. Pp. 841–843. Int. Soc. Photosynthesis, Alliance Communications Group, Lawrence 2005.Google Scholar
  167. Zhu, G., Long, S.P., Ort, D.R.: Improving photosynthetic efficiency for greater yield. — Annu. Rev. Plant Biol. 61: 235–261, 2010.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Biodiversity DivisionsInstitute of Himalayan Bioresource TechnologyPalampurIndia
  2. 2.Biotechnology DivisionsInstitute of Himalayan Bioresource TechnologyPalampurIndia

Personalised recommendations