Skip to main content

Advertisement

Log in

CO2 sequestration in plants: lesson from divergent strategies

  • Review
  • Published:
Photosynthetica

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

CA:

carbonic anhydrase

CAM:

crassulacean acid metabolism

CCM:

CO2-concentrating mechanism

HCO3 :

bicarbonate

PEPCase:

phosphoenolpyruvate carboxylase

PEPCK:

phosphoenolpyruvate carboxykinase

PPDK:

pyruvate orthophosphate dikinase

RA:

Rubisco activase

Rubisco:

ribulose-1,5-bisphosphate carboxylase/oxygenase

References

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Badger, M.R.: The role of carbonic anhydrases in photosynthetic CO2 concentrating mechanisms. — Photosynth. Res. 73: 83–94, 2003.

    Article  Google Scholar 

  • Badger, M.R., Hanson, D., Price, G.D.: Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria. — Funct. Plant Biol. 29: 161–173, 2002.

    Article  CAS  Google Scholar 

  • Badger, M.R., Price, G.D.: The role of carbonic anhydrase in photosynthesis. — Ann. Rev. Plant Physiol. Plant Mol. Biol. 45: 369–392, 1994.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Beardall, J., Giordano, M.: Ecological implications of microalgal and cyanobacterial CO2 concentrating mechanisms, and their regulation. — Funct. Plant Biol. 29: 335–347, 2002.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Blankenship, R.E.: Origin and early evolution of photosynthesis. — Photosynth. Res. 33: 91–111, 1992.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Bowes, G., Ogren, W.L., Hageman, R.H.: Phospohglycolate production catalyzed by ribulose diphosphate carboxylase. — Biochem. Biophys. Res. Commun. 45: 716–722, 1971.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Bowes, G., Salvucci, M.E.: Plasticity in the photosynthetic carbon metabolism of submersed aquatic macrophytes. — Aquat. Bot. 34: 233–266, 1989.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • Datta, S.K.: Rice biotechnology: A need for developing countries. — AgBioForum 7: 31–35, 2004.

    Google Scholar 

  • Decker, J.P.: Some effects of temperature and carbon dioxide concentration on photosynthesis of mimules. — Plant Physiol. 34: 103–106, 1959.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Dencic, S.: Designing a wheat ideotype with increased sink capacity. — Plant Breed. 112: 311–317, 1994.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ellis, R.J.: The most abundant protein in the world. — Trends Biochem. Sci. 4: 241–244, 1979.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Evans, J.R.: Photosynthetic acclimation and nitrogen partitioning within a lucerne canopy. I. Canopy Characteristics. — Aust. J. Plant Physiol. 20: 55–67, 1993.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Herring, R.J.: Opposition to transgenic technologies: ideology, interests and collective action frames. — Nat. Rev. Genet. 9: 458–463, 2008.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Holtum, J.A.M.: Crassulacean acid metabolism: plastic in expression, complexity of control — J. Exp. Bot. 53: 657–661, 2002.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Huertas, I.E., Colman, B., Espie, G.S.: Inorganic carbon acquisition and its energization in eustigmatophyte algae. — Funct. Plant Biol. 29: 271–277, 2002.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Kaplan, A., Reinhold, L.: CO2 concentrating mechanisms in photosynthetic microorganisms. — Ann. Rev. Plant Physiol. Plant Mol. Biol. 50: 539–570, 1999.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Keeley, J.E.: Isoettis howellii: a submerged aquatic CAM plant. — Am. J. Bot. 68: 420–424, 1981.

    Article  CAS  Google Scholar 

  • Keeley, J.E.: C4 photosynthetic modifications in the evolutionary transition from land to water in aquatic grasses. — Oecologia 116: 85–97, 1998.

    Article  Google Scholar 

  • Keeley, J.E.: Photosynthetic pathway diversity in a seasonal pool community. — Funct. Ecol. 13:106–118, 1999.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Koch, K., Kennedy, R.A.: Characteristics of Crassulacean acid metabolism in the succulent C4 dicot, Portulaca oleracea L. — Plant Physiol. 65: 193–197, 1980.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Körner, C., Diemer, M.: Evidence that plants from high altitude retains their greater photosynthetic efficiency under elevated CO2. — Funct. Ecol. 8: 58–68, 1994.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kumar, N., Kumar, S., Ahuja, P.S.: Photosynthetic characteristics of Hordeum, Triticum, Rumex, and Trifolium species at contrasting altitudes. — Photosynthetica 43: 195–201, 2005.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Latzko, E., Kelly, G.J.: The many-faceted function of phosphoenolpyruvate carboxylase in C3 plants. — Physiol. Vég. 21: 805–815, 1983.

    CAS  Google Scholar 

  • Leegood, R.C.: C4 photosynthesis: principles of CO2 concentration and prospects for its introduction into C3 plants. — J. Exp. Bot. 53: 581–590, 2002.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Lüttge, U.: Ecophysiology of Crassulacean acid metabolism (CAM). — Ann. Bot. 93: 629–652, 2004.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Maberly, S.C., Madsen, T.V.: Freshwater angiosperm carbon concentrating mechanisms: processes and patterns. — Funct. Plant Biol. 29: 393–405, 2002.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Madsen, T.V., Sand-Jensen, K.: Photosynthetic carbon assimilation in aquatic macrophytes. — Aquatic Bot. 41: 5–40, 1991.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Melzer, E., O’Leary, M.H.: Anapleurotic CO2 fixation by phosphoenolpyruvate carboxylase in C3 plants. — Plant Physiol. 84: 58–60, 1987.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Miyao, M.: Molecular evolution and genetic engineering of C4 photosynthetic enzymes. — J. Exp. Bot. 54: 179–189, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Miyao, M., Fukayama, H.: Metabolic consequences of overproduction of phosphoenolpyruvate carboxylase in C3 plants. — Arch. Biochem. Biophys. 414: 197–203, 2003.

    PubMed  CAS  Google Scholar 

  • Mooney, H.A., Strain, B.R., West, M.: Photosynthetic efficiency at reduced carbon dioxide tensions. — Ecology 47: 490–491, 1966.

    Article  Google Scholar 

  • Moore, P.D.: Mixed metabolism in plant pools. — Nature 399: 109–110, 1999.

    Article  CAS  Google Scholar 

  • Moroney, J.V., Bartlett, S.G., Samuelsson, G.: Carbonic anhydrase in plants and algae. — Plant Cell Environ. 24: 141–153, 2001.

    Article  CAS  Google Scholar 

  • Moroney, J.V., Somanchi, A.: How do microalgae concentrate CO2 to increase the efficiency of photosynthetic carbon fixation? — Plant Physiol. 119: 9–16, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Moroney, J.V., Ynalvez, R.A.: A proposed carbon dioxide concentration mechanism in Chlamydomonas reinhardtii. — Eukaryotic Cell 6: 1251–1259, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Nelson, T., Langdale, J.A.: Developmental genetics of C4 photosynthesis. — Ann. Rev. Plant Physiol. Plant Mol. Biol. 43: 25–47, 1992.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Nobel, P.S., Hartsock, T.L.: Drought-induced shifts in daily CO2 uptake patterns for leafy cacti. — Physiol. Plant. 70: 114–118, 1987.

    Article  Google Scholar 

  • Ogren, W.L., Bowes, G.: Ribulose diphosphate carboxylase regulates soybean photorespiration. — Nature-New Biol. 230: 159–160, 1971.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Paul, M.J., Cockburn, W.: The stimulation of CAM activity in Mesembryanthemum crystallinum in nitrate- and phosphatedeficient conditions. — New Phytol. 114: 391–398, 1990.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Raines, C.A.: Transgenic approaches to manipulate the environmental responses of the C3 carbon fixation cycle. — Plant Cell Environ. 29: 331–339, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Raven, J.A.: Exogenous inorganic carbon sources in plant photosynthesis — Biol. Rev. 45: 167–221, 1970.

    Article  CAS  Google Scholar 

  • Raven, J.A.: Inorganic carbon concentrating mechanisms in relation to the biology of algae. — Photosynth. Res. 77: 155–171, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Reddy, A.R., Sundar, D., Gnanam A.: Photosynthetic flexibility in Pedilanthus tithymaloides Poit, a CAM plant. — J. Plant Physiol. 160: 75–80, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Reinfelder, J.R., Kraepiel, A.M., Morel, F.M.M.: Unicellular C4 photosynthesis in a marine diatom. — Nature 407: 996–999, 2000.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Richards, R.A.: Selectable traits to increase crop photosynthesis and yield of grain crops. — J. Exp. Bot. 51: 447–458, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Riebesell, U.: Carbon fix for a diatom. — Nature 407: 959–960, 2000.

    Article  PubMed  CAS  Google Scholar 

  • 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.

  • 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.

    Article  CAS  Google Scholar 

  • Rokka, A., Zhang, L., Aro, E.: Rubisco activase: an enzyme with a temperature-dependent dual function? — Plant J. 25: 463–471, 2001.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Sage, R.F.: Are crassulacean acid metabolism and C4 photosynthesis incompatible? — Funct. Plant Biol. 29: 775–785, 2002a.

    Article  CAS  Google Scholar 

  • Sage, R.F.: C4 photosynthesis in terrestrial plants does not require Kranz anatomy. — Trends Plant Sci. 7: 283–285, 2002b.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Salvucci, M.E., Bowes, G.: Induction of reduced photorespiratory activity in submersed and amphibious aquatic macrophytes. — Plant Physiol. 67: 335–340, 1981.

    Article  PubMed  CAS  Google Scholar 

  • Salvucci, M.E., Bowes, G.: Two photosynthetic mechanisms mediating the low photorespiratory state in submersed aquatic angiosperms. — Plant Physiol. 73: 488–496, 1983.

    Article  PubMed  CAS  Google Scholar 

  • Somerville, C.R.: An early Arabidopsis demonstration. Resolving a few issues concerning photorespiration. — Plant Physiol. 125: 20–24, 2001.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Spreitzer, R.J.: Role of the small subunit in ribulose-1,5-bisphosphate carboxylase/oxygenase. — Arch. Biochem. Biophys. 414: 141–149, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Spreitzer, R.J., Salvucci, M.E.: Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. — Ann. Rev. Plant. Biol. 53: 449–475, 2002.

    Article  CAS  Google Scholar 

  • Streb, P., Shang, W., Feierabend, J., Bligny, R.: Divergent strategies of photoprotection in high-mountain plants. — Planta 207: 313–324, 1998.

    Article  CAS  Google Scholar 

  • Surridge, C.: Agricultural biotech: the rice squad. — Nature 416: 576–578, 2002.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Swaminathan, M.S.: An evergreen revolution. — Crop Sci. 46: 2293–2303, 2006.

    Article  Google Scholar 

  • Tabita, F.R.: Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: A different perspective — Photosynth. Res. 60: 1–28, 1999.

    Article  CAS  Google Scholar 

  • Takeda, S., Matsuoka, M.: Genetic approaches to crop improvement: responding to environmental and population changes. — Nat. Rev. Genet. 9: 444–457, 2008.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Thomas, H., Howarth, C.J.: Five ways to stay green. — J. Exp. Bot. 51: 329–337, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Tiwari, A., Kumar, P., Singh, S., Ansari, S.A.: Carbonic anhydrase in relation to higher plants. — Photosynthetica 43: 1–11, 2005.

    Article  CAS  Google Scholar 

  • Tollenaar, M., Wu, J.: Yield improvement in temperate maize is attributable to greater stress tolerance. — Crop Sci. 39: 1597–1604, 1999.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Vats, S.K., Kumar, S.: Photosynthetic response of Podophyllum hexandrum Royle from different altitudes in Himalayan ranges. — Photosynthetica 44: 136–139, 2006.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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 

  • Zhu, G., Long, S.P., Ort, D.R.: Improving photosynthetic efficiency for greater yield. — Annu. Rev. Plant Biol. 61: 235–261, 2010.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. K. Vats.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vats, S.K., Kumar, S. & Ahuja, P.S. CO2 sequestration in plants: lesson from divergent strategies. Photosynthetica 49, 481–496 (2011). https://doi.org/10.1007/s11099-011-0078-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-011-0078-z

Additional key words

Navigation