Photosynthetica 2011, 49(4):481-496 | DOI: 10.1007/s11099-011-0078-z

CO2 sequestration in plants: lesson from divergent strategies

S. K. Vats1,*, S. Kumar2, P. S. Ahuja1
1 Biodiversity Divisions, Institute of Himalayan Bioresource Technology, Palampur, India
2 Biotechnology Divisions, Institute of Himalayan Bioresource Technology, Palampur, India

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.

Keywords: aquatic; carbon-concentrating mechanisms; crassulacean acid metabolism; C4 photosynthesis; Rubisco

Received: February 22, 2011; Accepted: September 4, 2011; Published: December 1, 2011Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Vats, S.K., Kumar, S., & Ahuja, P.S. (2011). CO2 sequestration in plants: lesson from divergent strategies. Photosynthetica49(4), 481-496. doi: 10.1007/s11099-011-0078-z.
Download citation

References

  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. Go to original source...
  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. Go to original source...
  3. Badger, M.R.: The role of carbonic anhydrases in photosynthetic CO2 concentrating mechanisms. - Photosynth. Res. 73: 83-94, 2003. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  9. Beardall, J., Giordano, M.: Ecological implications of microalgal and cyanobacterial CO2 concentrating mechanisms, and their regulation. - Funct. Plant Biol. 29: 335-347, 2002. Go to original source...
  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.
  11. Blankenship, R.E.: Origin and early evolution of photosynthesis. - Photosynth. Res. 33: 91-111, 1992. Go to original source...
  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. Go to original source...
  13. Bowes, G., Ogren, W.L., Hageman, R.H.: Phospohglycolate production catalyzed by ribulose diphosphate carboxylase. - Biochem. Biophys. Res. Commun. 45: 716-722, 1971. Go to original source...
  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. Go to original source...
  15. Bowes, G., Salvucci, M.E.: Plasticity in the photosynthetic carbon metabolism of submersed aquatic macrophytes. - Aquat. Bot. 34: 233-266, 1989. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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.
  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. Go to original source...
  22. Datta, S.K.: Rice biotechnology: A need for developing countries. - AgBioForum 7: 31-35, 2004.
  23. Decker, J.P.: Some effects of temperature and carbon dioxide concentration on photosynthesis of mimules. - Plant Physiol. 34: 103-106, 1959. Go to original source...
  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. Go to original source...
  25. Dencic, S.: Designing a wheat ideotype with increased sink capacity. - Plant Breed. 112: 311-317, 1994. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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.
  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. Go to original source...
  31. Ellis, R.J.: The most abundant protein in the world. - Trends Biochem. Sci. 4: 241-244, 1979. Go to original source...
  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. Go to original source...
  33. Evans, J.R.: Photosynthetic acclimation and nitrogen partitioning within a lucerne canopy. I. Canopy Characteristics. - Aust. J. Plant Physiol. 20: 55-67, 1993. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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.
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  49. Herring, R.J.: Opposition to transgenic technologies: ideology, interests and collective action frames. - Nat. Rev. Genet. 9: 458-463, 2008. Go to original source...
  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. Go to original source...
  51. Holtum, J.A.M.: Crassulacean acid metabolism: plastic in expression, complexity of control - J. Exp. Bot. 53: 657-661, 2002. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  57. Kaplan, A., Reinhold, L.: CO2 concentrating mechanisms in photosynthetic microorganisms. - Ann. Rev. Plant Physiol. Plant Mol. Biol. 50: 539-570, 1999. Go to original source...
  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. Go to original source...
  59. Keeley, J.E.: Isoettis howellii: a submerged aquatic CAM plant. - Am. J. Bot. 68: 420-424, 1981. Go to original source...
  60. Keeley, J.E.: C4 photosynthetic modifications in the evolutionary transition from land to water in aquatic grasses. - Oecologia 116: 85-97, 1998. Go to original source...
  61. Keeley, J.E.: Photosynthetic pathway diversity in a seasonal pool community. - Funct. Ecol. 13:106-118, 1999. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  72. Latzko, E., Kelly, G.J.: The many-faceted function of phosphoenolpyruvate carboxylase in C3 plants. - Physiol. Vég. 21: 805-815, 1983.
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  78. Lüttge, U.: Ecophysiology of Crassulacean acid metabolism (CAM). - Ann. Bot. 93: 629-652, 2004. Go to original source...
  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.
  80. Maberly, S.C., Madsen, T.V.: Freshwater angiosperm carbon concentrating mechanisms: processes and patterns. - Funct. Plant Biol. 29: 393-405, 2002. Go to original source...
  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. Go to original source...
  82. Madsen, T.V., Sand-Jensen, K.: Photosynthetic carbon assimilation in aquatic macrophytes. - Aquatic Bot. 41: 5-40, 1991. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  86. Melzer, E., O'Leary, M.H.: Anapleurotic CO2 fixation by phosphoenolpyruvate carboxylase in C3 plants. - Plant Physiol. 84: 58-60, 1987. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  90. Miyao, M.: Molecular evolution and genetic engineering of C4 photosynthetic enzymes. - J. Exp. Bot. 54: 179-189, 2003. Go to original source...
  91. Miyao, M., Fukayama, H.: Metabolic consequences of overproduction of phosphoenolpyruvate carboxylase in C3 plants. - Arch. Biochem. Biophys. 414: 197-203, 2003. Go to original source...
  92. Mooney, H.A., Strain, B.R., West, M.: Photosynthetic efficiency at reduced carbon dioxide tensions. - Ecology 47: 490-491, 1966. Go to original source...
  93. Moore, P.D.: Mixed metabolism in plant pools. - Nature 399: 109-110, 1999. Go to original source...
  94. Moroney, J.V., Bartlett, S.G., Samuelsson, G.: Carbonic anhydrase in plants and algae. - Plant Cell Environ. 24: 141-153, 2001. Go to original source...
  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. Go to original source...
  96. Moroney, J.V., Ynalvez, R.A.: A proposed carbon dioxide concentration mechanism in Chlamydomonas reinhardtii. - Eukaryotic Cell 6: 1251-1259, 2007. Go to original source...
  97. Nelson, T., Langdale, J.A.: Developmental genetics of C4 photosynthesis. - Ann. Rev. Plant Physiol. Plant Mol. Biol. 43: 25-47, 1992. Go to original source...
  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. Go to original source...
  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. Go to original source...
  100. Nobel, P.S., Hartsock, T.L.: Drought-induced shifts in daily CO2 uptake patterns for leafy cacti. - Physiol. Plant. 70: 114-118, 1987. Go to original source...
  101. Ogren, W.L., Bowes, G.: Ribulose diphosphate carboxylase regulates soybean photorespiration. - Nature-New Biol. 230: 159-160, 1971. Go to original source...
  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.
  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. Go to original source...
  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.
  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. Go to original source...
  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.
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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.
  112. Raines, C.A.: Transgenic approaches to manipulate the environmental responses of the C3 carbon fixation cycle. - Plant Cell Environ. 29: 331-339, 2006. Go to original source...
  113. Raven, J.A.: Exogenous inorganic carbon sources in plant photosynthesis - Biol. Rev. 45: 167-221, 1970. Go to original source...
  114. Raven, J.A.: Inorganic carbon concentrating mechanisms in relation to the biology of algae. - Photosynth. Res. 77: 155-171, 2003. Go to original source...
  115. Reddy, A.R., Sundar, D., Gnanam A.: Photosynthetic flexibility in Pedilanthus tithymaloides Poit, a CAM plant. - J. Plant Physiol. 160: 75-80, 2003. Go to original source...
  116. Reinfelder, J.R., Kraepiel, A.M., Morel, F.M.M.: Unicellular C4 photosynthesis in a marine diatom. - Nature 407: 996-999, 2000. Go to original source...
  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. Go to original source...
  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.
  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. Go to original source...
  120. Richards, R.A.: Selectable traits to increase crop photosynthesis and yield of grain crops. - J. Exp. Bot. 51: 447-458, 2000. Go to original source...
  121. Riebesell, U.: Carbon fix for a diatom. - Nature 407: 959-960, 2000. Go to original source...
  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. Go to original source...
  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. Go to original source...
  124. Rokka, A., Zhang, L., Aro, E.: Rubisco activase: an enzyme with a temperature-dependent dual function? - Plant J. 25: 463-471, 2001. Go to original source...
  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. Go to original source...
  126. Sage, R.F.: Are crassulacean acid metabolism and C4 photosynthesis incompatible? - Funct. Plant Biol. 29: 775-785, 2002a. Go to original source...
  127. Sage, R.F.: C4 photosynthesis in terrestrial plants does not require Kranz anatomy. - Trends Plant Sci. 7: 283-285, 2002b. Go to original source...
  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. Go to original source...
  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.
  130. Salvucci, M.E., Bowes, G.: Induction of reduced photorespiratory activity in submersed and amphibious aquatic macrophytes. - Plant Physiol. 67: 335-340, 1981. Go to original source...
  131. Salvucci, M.E., Bowes, G.: Two photosynthetic mechanisms mediating the low photorespiratory state in submersed aquatic angiosperms. - Plant Physiol. 73: 488-496, 1983. Go to original source...
  132. Somerville, C.R.: An early Arabidopsis demonstration. Resolving a few issues concerning photorespiration. - Plant Physiol. 125: 20-24, 2001. Go to original source...
  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. Go to original source...
  134. Spreitzer, R.J.: Role of the small subunit in ribulose-1,5-bisphosphate carboxylase/oxygenase. - Arch. Biochem. Biophys. 414: 141-149, 2003. Go to original source...
  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. Go to original source...
  136. Streb, P., Shang, W., Feierabend, J., Bligny, R.: Divergent strategies of photoprotection in high-mountain plants. - Planta 207: 313-324, 1998. Go to original source...
  137. Surridge, C.: Agricultural biotech: the rice squad. - Nature 416: 576-578, 2002. Go to original source...
  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. Go to original source...
  139. Swaminathan, M.S.: An evergreen revolution. - Crop Sci. 46: 2293-2303, 2006. Go to original source...
  140. Tabita, F.R.: Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: A different perspective - Photosynth. Res. 60: 1-28, 1999. Go to original source...
  141. Takeda, S., Matsuoka, M.: Genetic approaches to crop improvement: responding to environmental and population changes. - Nat. Rev. Genet. 9: 444-457, 2008. Go to original source...
  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. Go to original source...
  143. Thomas, H., Howarth, C.J.: Five ways to stay green. - J. Exp. Bot. 51: 329-337, 2000. Go to original source...
  144. Tiwari, A., Kumar, P., Singh, S., Ansari, S.A.: Carbonic anhydrase in relation to higher plants. - Photosynthetica 43: 1-11, 2005. Go to original source...
  145. Tollenaar, M., Wu, J.: Yield improvement in temperate maize is attributable to greater stress tolerance. - Crop Sci. 39: 1597-1604, 1999. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  152. Vats, S.K., Kumar, S.: Photosynthetic response of Podophyllum hexandrum Royle from different altitudes in Himalayan ranges. - Photosynthetica 44: 136-139, 2006. Go to original source...
  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. Go to original source...
  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.
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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.
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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.
  167. Zhu, G., Long, S.P., Ort, D.R.: Improving photosynthetic efficiency for greater yield. - Annu. Rev. Plant Biol. 61: 235-261, 2010. Go to original source...