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Review Article

A critical review on the improvement of photosynthetic carbon assimilation in C3 plants using genetic engineering

, &
Pages 1-21 | Received 04 Jun 2010, Accepted 14 Oct 2010, Published online: 24 Jun 2011

References

  • Agarie S, Miura A, Sumikura R, Tsukamoto S, Nose A, Arima S, Matsuoka M, Miyao-Tokutomi M. (2002). Overexpression of C4 PEPC caused O2-insensitive photosynthesis in transgenic rice plants. Plant Sci, 162, 257–265.
  • Andersson I, Taylor TC. (2003). Structural framework for catalysis and regulation in ribulose-1,5-bisphosphate carboxylase/oxygenase. Arch Biochem Biophys, 414, 130–140.
  • Austin RB. (1989). Genetic variation in photosynthesis. J Agric Sci, 112, 287–294.
  • Bandyopadhyay A, Datta K, Zhang J, Yang W, Raychaudhuri S, Miyao M, Datta SK. (2007). Enhanced photosynthesis rate in genetically engineered indica rice expressing pepc gene cloned from maize. Plant Sci, 172, 1204–1209.
  • Bauwe H, Kolukisaoglu U. (2003). Genetic manipulation of glycine decarboxylation. J Exp Bot, 54, 1523–1535.
  • Black CC Jr. (1973). Photosynthetic carbon fixation in relation to net CO2 uptake. Ann Rev Plant Physiol, 24, 253–286.
  • Boldt R, Edner C, Kolukisaoglu U, Hagemann M, Weckwerth W, Wienkoop S, Morgenthal K, Bauwe H. (2005). D-Glycerate 3-kinase, the last unknown enzyme in the photorespiratory cycle in Arabidopsis, belongs to a novel kinase family. Plant Cell, 17, 2413–2420.
  • Brooks A, Farquhar GD. (1985). Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase oxygenase and the rate of respiration in the light – estimates from gas-exchange measurements on spinach. Planta, 165, 397–406.
  • Brown RH, Bouton JH. (1993). Physiology and genetics of interspecific hybrids between photosynthetic types. Ann Rev Plant Physiol Plant Mol Biol, 44, 435–456.
  • Casati P, Lara MV, Andreo CS. (2000). Induction of a C4-like mechanism of CO2 fixation in Egeria densa, a submerged aquatic species. Plant Physiol, 123, 1611–1621.
  • Chandler VL, Vaucheret H. (2001). Gene activation and gene silencing. Plant Physiol, 125, 145–148.
  • Chen S, Hajirezaei M, Peisker M, Tschiersch H, Sonnewald U, Börnke F. (2005). Decreased sucrose-6-phosphate phosphatase level in transgenic tobacco inhibits photosynthesis, alters carbohydrate partitioning, and reduces growth. Planta, 221, 479–492.
  • Chen Y, Xu DQ. (2007). Changes in leaf photosynthesis of transgenic rice with silenced OsBP-73 gene. Photosynthetica, 45, 419–425.
  • Chida H, Nakazawa A, Akazaki H, Hirano T, Suruga K, Ogawa M, Satoh T, Kadokura K, Yamada S, Hakamata W, Isobe K, Ito T, Ishii R, Nishio T, Sonoike K, Oku T. (2007). Expression of the algal cytochrome c6 gene in Arabidopsis enhances photosynthesis and growth. Plant Cell Physiol, 48, 948–957.
  • Cooper TG, Wood HG (1971). The carboxylation of phosphoenolpyruvate and pyruvate. II. The active species of ‘CO2’ utilized by phosphoenolpyruvate carboxylase and pyruvate carboxylase. J Biol Chem, 246, 5488–5490.
  • Crosbie TM, Pearce RB. (1982). Effects of recurrent phenotypic selection for high and low photosynthesis on agronomic traits in two maize populations. Crop Sci, 22, 809–813.
  • Crosbie TM, Pearce RB, Mock JJ. (1981). Recurrent phenotypic selection for high and low photosynthesis in two maize populations. Crop Sci 21, 736–740.
  • Daie J. (1993). Cytosolic fructose-1,6-bisphosphatase: A key enzyme in the sucrose biosynthetic pathway. Photosynth Res, 38, 5–14.
  • de Groote D, Kennedy RA. (1977). Photosynthesis in Elodea canadensis Michx. Plant Physiol, 59, 1133–1135.
  • Dodd AN, Borland AM, Haslam RP, Griffiths H, Maxwell K. (2002). Crassulacean acid metabolism: plastic, fantastic. J Exp Bot, 53, 569–580.
  • Dodd AN, Griffiths H, Taybi T, Cushman JC, Borland AM. (2003). Integrating diel starch metabolism with the circadian and environmental regulation of crassulacean acid metabolism in Mesembryanthemum crystallinum. Planta, 216, 789–797.
  • Dong LY, Masuda T, Kawamura T, Hata S, Izui K. (1998). Cloning, expression, and characterization of a root-form phosphoenolpyruvate carboxylase from Zea mays: comparison with the C4-form enzyme. Plant Cell Physiol, 39, 865–873.
  • Edwards G. (1999). Tuning up crop photosynthesis. Nat Biotechnol, 17, 22–23.
  • Edwards GE, Furbank RT, Hatch MD, Osmond CB. (2001). What does it take to be C4? Lessons from the evolution of C4 photosynthesis. Plant Physiol, 125, 46–49.
  • Ehleringer JR, Monson RK. (1993). Evolutionary and ecological aspects of photosynthetic pathway variation. Ann Rev Ecol Syst, 24, 411–439.
  • Fahnenstich H, Saigo M, Niessen M, Zanor MI, Andreo CS, Fernie AR, Drincovich MF, Flügge UI, Maurino VG. (2007). Alteration of organic acid metabolism in Arabidopsis overexpressing the maize C4 NADP-malic enzyme causes accelerated senescence during extended darkness. Plant Physiol, 145, 640–652.
  • Feng LL, Han YJ, Liu G, An BG, Yang J, Yang GH, Li YS, Zhu YG. (2007). Overexpression of sedoheptulose-1,7-bisphosphatase enhances photosynthesis and growth under salt stress in transgenic rice plants. Funct Plant Biol, 34, 822–834.
  • Feng LL, Li H, Jiao JM, Li D, Zhou L, Wan J, Li YS. (2009). Reduction in SBPase activity by antisense RNA in transgenic rice plants: effect on photosynthesis, growth, and biomass allocation at different nitrogen levels. J Plant Biol, 52, 382–393.
  • Finnegan PM, Suzuki S, Ludwig M, Burnell JN. (1999). Phosphoenolpyruvate carboxykinase in the C4 monocot Urochloa panicoides is encoded by four differentially expressed genes. Plant Physiol, 120, 1033–1041.
  • Firooznia F. (2007). The story of the Calvin cycle: bringing carbon fixation to life. Am Biol Teach, 69: 364–367.
  • Ford DM, Shibles R, Green DE. (1983). Growth and yield of soybean lines selected for divergent leaf photosynthetic ability. Crop Sci, 23, 517–520.
  • Freitag H, Stichler W. (2000). A remarkable new leaf type with unusual photosynthetic tissue in a central Asiatic genus of Chenopodiacea. Plant Biol, 2, 154–160.
  • Fukayama H, Hatch MD, Tamai T, Tsuchida H, Sudoh S, Furbank RT, Miyao M. (2003). Activity regulation and physiological impacts of maize C4-specific phosphoenolpyruvate carboxylase overproduced in transgenic rice plants. Photosyn Res, 77, 227–239.
  • Fukayama H, Tsuchida H, Agarie S, Nomura M, Onodera H, Ono K, Lee B-H Hirose, S, Toki S, Ku MSB, Makino A, Matsuoka M, Miyao M. (2001). Significant accumulation of C4-specific pyruvate, orthophosphate dikinase in a C3 plant, rice. Plant Physiol, 127, 1136–1146.
  • Furbank RT, Jenkins, CLD, Hatch, MD. (2000). Regulation of C4 photosynthesis. In: Leegood RC, Sharkey TD, von Caemmerer S, eds. Photosynthesis: Physiology and Metabolism (Advances in Photosynthesis). Dordrecht, The Netherlands: Kluwer Academic Publishers, 435–457.
  • Gelvin SB. (1998). The introduction and expression of transgenes in plants. Curr Opin Biotechnol, 9, 227–232.
  • Goodall GJ, Filipowicz W. (1991). Different effects of intron nucleotide composition and secondary structure on pre-mRNA splicing in monocot and dicot plants. EMBO Journal, 10, 2625–2644.
  • Greene CH, Pershing AJ. (2007). Climate drives sea change. Science, 315, 1084–1085.
  • Haake V, Geiger M, Walch-Liu P, Engels C, Zrenner R, Stitt M. (1999). Changes in aldolase activity in wild-type potato plants are important for acclimation to growth irradiance and carbon dioxide concentration, because plastid aldolase exerts control over the ambient rate of photosynthesis across a range of growth conditions. Plant J, 17, 479–489.
  • Harrison EP, Willingham NM, Lloyd JC, Raines CA. (1998). Reduced sedoheptulose-1,7-bisphosphatase levels in transgenic tobacco lead to decreased photosynthetic capacity and altered carbohydrate accumulation. Planta, 204, 27–36.
  • Hatch MD, Kagawa T, Craig S. (1975). Subdivision of C4-pathway species based on differing C4 acid decarboxylating systems and ultrastructural features. Aust J Plant Physiol, 2, 111–128.
  • Hatch MD. (1987). C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochim Biophy Acta, 895, 81–106.
  • Häusler RE, Hirsch HJ, Kreuzaler F, Peterhänsel C. (2002). Overexpression of C4-cycle enzymes in transgenic C3 plants: a biotechnological approach to improve C3-photosynthesis. J Exp Bot, 53, 591–607.
  • Häusler RE, Kleines M, Uhrig H, Hirsch HJ, Smets H. (1999). Overexpression of phosphoenolpyruvate carboxylase from Corynebacterium glutamicum lowers the CO2 compensation point (Γ*) and enhances dark and light respiration in transgenic potato. J Exp Bot, 50, 1231–1242.
  • Häusler RE, Rademacher T, Li J, Lipka V, Fischer KL, Schubert S, Kreuzaler F, Hirsch HJ. (2001). Single and double overexpression of C4-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.
  • Heineke D, Bykova N, Gardestrom P, Bauwe H. (2001). Metabolic response of potato plants to an antisense reduction of the P-protein of glycine decarboxylase. Planta, 212, 880–887.
  • Heldt HW. (2005). Plant Biochemistry (3rd ed). San. Diego, CA: Elsevier Academic Press.
  • Henkes S, Sonnewald U, Badur R, Flachmann R, Stitt M. (2001). A small decrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism. Plant Cell, 13, 535–551.
  • Hiei Y, Ohta S, Komari T, Kumashiro T. (1994). Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J, 6, 271–282.
  • Hill PW, Marshall C, Williams GG, Blum H, Harmens H, Jones DL, Farrar JF. (2007). The fate of photosynthetically-fixed carbon in Lolium perenne grassland as modified by elevated CO2 and sward management. New Phytol 173, 766–777.
  • Hobbs SLA. (1986). Relationships between carbon dioxide exchange rate, photosynthetic area and biomass in pea. Can J Plant Sci, 66, 465–472.
  • Holaday AS, Bowes G. (1980). C4 acid metabolism and dark CO2 fixation in a submerged aquatic macrophyte (Hydrilla verticillata). Plant Physiol, 65, 331–335.
  • Hudspeth RL, Grula JW, Dai Z, Edwards GE, Ku MSB. (1992). Expression of maize phosphoenolpyruvate carboxylase in transgenic tobacco. Effects on biochemistry and physiology. Plant Physiol, 98, 458–464.
  • IPCC. (2001). Climate change 2001: the scientific basis. Intergovernment panel on climate change. Cambridge, UK: Cambridge University Press.
  • IPCC. (2007). Climate change 2007: climate change impacts, adaptation and vulnerability. Working Group II. Geneva, Switzerland: IPCC.
  • Isebrands JG, Ceulemans R, Wiard B. (1988). Genetic variation in photosynthetic traits among Populus clones in relation to yield. Plant Physiol Biochem, 26, 427–437.
  • Ishimaru K, Ohkawa Y, Ishige T, Tobias DJ, Ohsugi R. (1998). Elevated pyruvate, orthophosphate dikinase (PPDK) activity alters carbon metabolism in C3 transgenic potato with a C4 maize PPDK gene. Physiol Plantarum, 103, 340–346.
  • Izui K, Ishijima S, Yamagushi Y, Katagiri F, Murata T, Shigesada K, Sugiyama T, Katsuki H. (1986). Cloning and sequence analysis of cDNA encoding active phosphoenolpyruvate carboxylase of the C4-pathway of maize. Nucl Acids Res, 14, 1615–1628.
  • Jiao D, Li X, Huang X, Chi W, Kuang T, Ku MSB. (2001). The characteristics of CO2 assimilation of photosynthesis and chlorophyll fluorescence in transgenic PEPC rice. Chinese Sci Bull, 46, 1080–1084.
  • Jiao DM. (2008). Redesigning C4 rice from limited rice C4 photosynthesis. In: Sheehy JE, Mitchell PL, Hardy B, ed. Charting new pathways to C4 rice. Singapore: World Scientific Publishing Co. Pte. Ltd., 145–162.
  • Karami O. (2008). Factors affecting Agrobacterium-mediated transformation of plants. Transgenic Plant J, 3, 127–137.
  • Kerr RA. (2007). Scientists tell policy makers we’re all warming the world. Science, 315, 754–757.
  • Kershanskaya OI, Teixeira da Silva JA. (2010). Photosynthetic basis for wheat crop improvement: Genetic modification of photosynthesis. In: Yerlan T, Ed. Khazakistan Plant Science and Biotechnology. Asian Austral J Plant Sci Biotech, 4 (Special Issue 1), 27–34.
  • Kintisch E. (2007). New congress may be warming up to plans for capping emissions. Science, 315, 444.
  • Kluger J. (2007). Global warming: what now? Our feverish planet badly needs a cure. Time Mag, 9, 50–109.
  • Krapp A, Chaves MM, David MM, Rodriques ML, Pereira JS, Stitt M. (1994). Decreased ribulose-1,5-bisphosphate carboxylase/oxygenase in transgenic tobacco transformed with antisense rbcS. 8. Impact on photosynthesis and growth in tobacco growing under extreme high irradiance and high temperature. Plant Cell Environ, 17, 945–953.
  • Ku MSB, Agarie S, Nomura M, Fukayama H, Tsuchida H, Ono K, Hirose S, Toki S, Miyao M, Matsuoka M. (1999). High-level expression of maize phosphoenolpyruvate carboxylase in transgenic rice plants. Nat Biotechnol, 17, 76–80.
  • Ku MSB, Cho D, Ranade U, Hsu T-P Li, X, Jiao D-M Ehleringer, J, Miyao M, Matsuoka M. (2000). Photosynthetic performance of transgenic rice plants overexpressing maize C4 photosynthesis enzymes. In: Sheehy JE, Mitchell PL, Hardy B, eds. Redesigning rice photosynthesis to increase yield. Philippines, and Amsterdam: Elsevier, 193–204.
  • Ku MSB, Cho DH, Li X, Jiao DM, Pinto M, Miyao M, Matsuoka M. (2001). Introduction of genes encoding C4 photosynthesis enzymes into rice plants: physiological consequences. In: Goode JA, Chadwich DC, ed. Rice Biotechnology: Improving Yield, Stress Tolerance and Grain Quality. NY, USA: John Wiley & Sons, 100–116.
  • Ku MSB, Kano-Murakami Y, Matsuoka M. (1996). Evolution and expression of C4 photosynthesis genes. Plant Physiol, 111, 949–957.
  • Kumar A, Li C, Portis Jr AR. (2009). Arabidopsis thaliana expressing a thermostable chimeric Rubisco activase exhibits enhanced growth and higher rates of photosynthesis at moderately high temperatures. Photosynth Res, 100, 143–153.
  • Kurek I, Chang TK, Bertain SM, Madrigal A, Liu L, Lassner MW, Zhu G. (2007). Enhanced thermostability of Arabidopsis Rubisco activase improves photosynthesis and growth rates under moderate heat stress. Plant Cell, 19, 3230–3241.
  • Lal R. (2004) Soil carbon sequestration impacts on global climate change and food security. Science, 304, 1624–1627.
  • Lal R. (2008). Carbon sequestration. Phil Trans R Soc B, 363, 815–830.
  • Lal R. (2009). Challenges and opportunities in soil organic matter research. Eur J Soil Sci, 60, 158–160.
  • Lashof D, Hare B. (1999). The role of biotic carbon stocks in stabilizing greenhouse gas concentrations at safe levels. Environ Sci Policy, 2, 101–109.
  • Leegood RC, Lea PJ, Adcock MD, Haeusler RE. (1995). The regulation and control of photorespiration. J Exp Bot, 46, 1397–1414.
  • Leegood RC. (2002). C4 photosynthesis: principles of CO2 concentration and prospects for its introduction into C3 plants. J Exp Bot, 53, 581–590.
  • Lefebvre S, Lawson T, Zakhleniuk OV, Lloyd JC, Raines CA. (2005). Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiol, 138, 451–460.
  • Lieman-Hurwitz J, Asipov L, Rachmilevitch S, Marcus Y, Kaplan A. (2005). Expression of cyanobacterial ictB in higher plants enhanced photosynthesis and growth. In: Omasa K, Nouchi I, de Kok LJ, eds. Plant Responses to Air Pollution and Global Change. New York: Springer Verlag Tokyo Berlin Heidelberg, 133–139.
  • Lieman-Hurwitz J, Rachmilevitch S, Mittler R, Marcus Y, Kaplan A. (2003). Enhanced photosynthesis and growth of transgenic plants that express ictB, a gene involved in HCO3−accumulation in cyanobacteria. Plant Biotechnol, J 1, 43–50.
  • Lipka V, Häusler RE, Rademacher T, Li J, Hirsch H-J, Kreuzaler F. (1999). Solanum tuberosum double transgenic expressing phosphoenolpyruvate carboxylase and NADP-malic enzyme display reduced electron requirement for CO2 fixation. Plant Sci, 144, 93–105.
  • Long SP, Ainsworth EA, Rogers A, Ort DR. (2004). Rising atmospheric carbon dioxide: plants face the future. Ann Rev Plant Biol, 55, 591–628.
  • Luo HY. (2001). Comparison on C3, C4 and CAM plants. J Higher Correspondence Education (Nat Sci), 14, 35–38 (in Chinese).
  • Lutts S, Lefèvre I, Delpérée C, Kivits S, Dechamps C, Robledo A, Correal E. (2004). Heavy metal accumulation by the halophyte species Mediterranean saltbush. J Environ Qual, 33, 1271–1279.
  • Magnin NC, Cooley BA, Reiskind JB, Bowes G. (1997). Regulation and localization of key enzymes during the induction of Kranz-less, C4-type photosynthesis in Hydrilla verticillata. Plant Physiol, 115, 1681–1689.
  • Makino A, Nakano H, Mae T, Shimada T, Yamamoto N. (2000). Photosynthesis, plant growth and N allocation in transgenic rice plants with decreased Rubisco under CO2 enrichment. J Exp Bot, 51, 383–389.
  • Mann CC. (1999). Genetic engineers aim to soup up crop photosynthesis. Science, 283, 314–316.
  • Masle J, Hudson GS, Badger MR. (1993). Effects of ambient CO2 concentration on growth and nitrogen use in tobacco (Nicotiana tabacum) plants transformed with an antisense gene to the small-subunit of ribulose-1,5-bisphosphate carboxylase oxygenase. Plant Physiol, 103, 1075–1088.
  • Matsumura I., Patel M., Greene D. (2005). Directed evolution of Rubisco through genetic selections of metabolically engineered Escherichia coli. FASEB J, 19, A292–A292.
  • Matsuoka M, Fukayama H, Tsuchida H, Nomura M, Agarie S, Ku MSB, Miyao M. (2000). How to express some C4 photosynthesis genes at high levels in rice. Stud Plant Sci, 7, 167–175.
  • Matsuoka M, Furbank RT, Fukayama H, Miyao M. (2001). Molecular engineering of C4 photosynthesis. Ann Rev Plant Physiol Plant Mol Biol, 52: 297–314.
  • Meister M, Agostino A, Hatch MD. (1996). The roles of malate and aspartate in C4 photosynthetic metabolism in Flaveria bidentis (L.). Planta, 199, 262–269.
  • Mikkelsen M, Jorgensen M, Krebs FC. (2010). The teraton challenge. A review of fixation and transformation of carbon dioxide. Energy Environ Sci, 3, 43–81.
  • Miyagawa Y, Tamoi M, Shigeoka S. (2001). Overexpression of a cyanobacterial fructose-1,6-/sedoheptulose-1,7-bisphosphatase in tobacco enhances photosynthesis and growth. Nat Biotechnol, 19, 965–969.
  • Miyao M. (2003). Molecular evolution and genetic engineering of C4 photosynthetic enzymes. J Exp Bot 54, 179–189.
  • Monson RK, Rawsthorne S. (2000). CO2 assimilation in C3–C4 intermediate plants. In: Leegood RC, Sharkey TD, von Caemmerer S, eds. Photosynthesis: physiology and metabolism. Advances in photosynthesis, Vol. 9. Dordrecht: Kluwer Academic Publishers, 533–550.
  • Monson RK. (1999). The origins C4 genes and evolutionary pattern in the C4 metabolic phenotype. In: Sage RF, Monson RK, eds. C4 plant biology. San Diego: Academic Press, 377–410.
  • Nelson CJ. (1988). Genetic associations between photosynthetic characteristics and yield: review of the evidence. Plant Physiol Biochem, 26, 543–554.
  • Nobel PS. (1991). Achievable productivities of certain CAM plants: basis for high values compared with C3 and C4 plants. New Phytol, 119, 183–205.
  • Nowak R, Ellsworth DS, Smith SD. (2004). Functional responses of plants to elevated atmospheric CO2-do photosynthetic and productivity data from FACE experiments support early predictions? New Phytol, 162, 253–280.
  • O’Leary MH. (1982). Phosphoenolpyruvate carboxylase: an enzymologist’s view. Ann Rev Plant Physiol, 33, 297–315.
  • Ogren WL. (1984) Photorespiration – pathways, regulation and modification. Ann Rev Plant Physiol Mol Biol, 35, 415–442.
  • Osmond CB, Grace SC. (1995). Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? J Exp Bot, 46, 1351–1362.
  • Osmond CB. (1978). Crassulacean acid metabolism: curiosity in context. Ann Rev Plant Physiol Plant Mol Biol, 29, 379–414.
  • Pan RZ. (2008). Plant Physiology (6 rd). Beijing: Higher Education Press.
  • Parry MAJ, Andralojc PJ, Mitchell RAC, Madgwick PJ, Keys AJ. (2003). Manipulation of Rubisco: the amount, activity, function and regulation. J Exp Bot, 54, 1321–1333.
  • Parry MAJ, Madgwick PJ, Carvalho JFC, Andralojc PJ. (2007). Prospects for increasing photosynthesis by overcoming the limitations of Rubisco. J Agric Sci, 145, 31–43.
  • Peterhänsel C, Hirsch HJ, Kreazaaler F. (2008b). Overexpression of C4 pathway genes in the C3 dicots potato, tobacco, and Arabidopsis: experiences and future challenges. In: Sheehy JE, Mitchell PL, Hardy B, eds. Charting new pathways to C4 rice. Singapore: World Scientific Publishing Co. Pte. Ltd., 163–170.
  • Peterhänsel C, Niessen M, Kebeish RM. (2008a). Metabolic engineering towards the enhancement of photosynthesis. Photochem Photobiol, 84, 1317–323.
  • Poetsch W, Hermans J, Westhoff P. (1991). Multiple cDNAs of phosphoenolpyruvate carboxylase in the C4 dicot Flaveria trinervia. FEBS Lett, 292, 133–136.
  • Prendergast HDV, Hattersley PW, Stone NE. (1987). New structural/biochemical associations in leaf blades of C4 grasses (Poaceae). Aust J Plant Physiol, 14, 403–420.
  • Raines CA. (2003). The Calvin cycle revisited. Photosynth Res, 75, 1–10.
  • Raines CA. (2006). Transgenic approaches to manipulate the environmental responses of the C3 carbon fixation cycle. Plant Cell Environ, 29, 331–339.
  • Repo E, Hatch MD. (1976). Photosynthesis in Gomphrena celosioides and its classification among C4 pathway plants. Aust J Plant Physiol, 3, 863–876.
  • Rozema J, Flowers T. (2008). Crops for a salinized world. Science, 322, 1478–1480.
  • Ruan CJ, Li H, Guo YQ, Qin P, Gallagher JL, Seliskar DM, Lutts S, Mahy G. (2008). Kosteletzkya virginica, an agroecoengineering halophytic species for alternative agricultural production in China’s east coast: ecological adaptation and benefits, seed yield, oil content, fatty acid and biodiesel properties. Ecol Eng, 32, 320–328.
  • Running SM. (2006). Is global warming causing more large wildfires? Science, 313, 927–928.
  • Sage RF, Pearcy RW. (1987). The nitrogen use efficiency of C3 and C4 plants. I. leaf nitrogen, growth and biomass partitioning in Chenopodium album (L.) and Amaranthus retroflexus (L.). Plant Physiol, 84, 954–958.
  • Sage RF. (2004). The evolution of C4 photosynthesis. New Phytol, 161, 341–370.
  • Salvucci ME, Bowes G. (1981). Induction of reduced photorespiratory activity in submerged and amphibious aquatic macrophytes. Plant Physiol, 67, 335–340.
  • Salvucci ME, Bowes G. (1983). Two photosynthetic mechanisms mediating the low photorespiratory state in submerged aquatic angiosperm. Plant Physiol, 73, 488–496.
  • Secor J, McCarty DR, Shibles R, Green DE. (1982). Variability and selection for leaf photosynthesis in advanced generations of soybeans. Crop Sci, 22, 255–259.
  • Sharkey TD. (1988). Estimating the rate of photorespiration in leaves. Physiol Plantarum, 73, 147–152.
  • Sheehy JE, Mitchell PL, Hardy B. (2000). Redesigning rice photosynthesis to increase yield. Philippines: International Rice Research Institute, Amsterdam: Elsevier.
  • Sheriff A, Meyer H, Riedel E, Schmitt JM, Lapke C. (1998). The influence of plant pyruvate, orthophosphate dikinase on a C3 plant with respect to the intracellular location of the enzyme. Plant Sci, 136, 43–57.
  • Singh R, Malhotra SP. (2000). Carbon fixation, sucrose synthesis and its transport to storage tissues. Dev Crop Sci, 26, 1–34.
  • Smith AL. (1997). Oxford dictionary of biochemistry and molecular biology. Oxford: Oxford University Press.
  • Spencer WE, Wetzel RG, Teeri J. (1996). Photosynthetic phenotype plasticity and the role of phosphoenolpyruvate carboxylase in Hydrilla verticillata. Plant Sci, 118, 1–9.
  • Spreitzer RJ, Salvucci ME. (2002). Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Ann Rev Plant Biol, 53, 449–475.
  • Stemmer WPC. (1994). Rapid evolution of a protein in-vitro by DNA shuffling. Nature, 370, 389–391.
  • Stitt M, Schulze D. (1994). Does Rubisco control the rate of photosynthesis and plant growth – an exercise in molecular ecophysiology. Plant Cell Environ, 17, 465–487.
  • Streatfield SJ, Weber A, Kinsman EA, Häusler RE, Li J, Post-Beitenmiller D, Kaiser WM, Pyke KA, Flügge UI, Chory J. (1999). The phosphoenolpyruvate/phosphate translocator is required for phenolic metabolism, palisade cell development and plastid-dependent nuclear gene expression. Plant Cell, 11, 1609–1621.
  • Sun JD, Yang LX, Wang YL, Ort DR. (2009). Facing the global change: Opportunities for improvement in photosynthetic radiation use efficiency and crop yield. Plant Sci, 177, 511–522.
  • Surridge C. 2002. The rice squad. Nature, 416, 576–578.
  • Suzuki S, Murai N, Burnell JN, Arai M. (2000). Changes in photosynthetic carbon flow in transgenic rice plants that express C4-type phosphoenolpyruvate carboxykinase from Urochloa panicoides. Plant Physiol, 124, 163–172.
  • Suzuki S, Murai N, Kasaoka K, Hiyoshi T, Imaseki H, Burnell JN, Arai M. (2006). Carbon metabolism in transgenic rice plants that express phosphoenolpyruvate carboxylase and/or phosphoenolpyruvate carboxykinase. Plant Sci, 170, 1010–1019.
  • Suzuki Y, Miyamoto T, Yoshizawa R, Mae T, Makino A. (2009). Rubisco content and photosynthesis of leaves at different positions in transgenic rice with an overexpression of RBCS. Plant Cell Environ, 32, 417–427.
  • Svensson P, Bläsing O, Westhoff P. (1997). Evolution of the enzymatic characteristics of C4 phosphoenolpyruvate carboxylase. A comparison of the orthologous PPCA phosphoenolpyruvate carboxylases of Flaveria trinervia (C4) and Flaveria pringlei (C3). Eur J Biochem, 246, 452–460.
  • Taiz L, Zeiger E. (2006). Plant Physiology (4th ed.). Sunderland MA: Sinauer Associates Inc.
  • Takeuchi K, Akagi H, Kamasawa N, Osumi M, Honda H. (2000). Aberrant chloroplasts in transgenic rice plants expressing a high level of maize NADP-dependent malic enzyme. Planta 211, 265–274.
  • Tamoi M, Shigeoka S. (2005). Improvement of photosynthesis in higher plants. In: Omasa K, Nouchi I, DeKok LJ, ed. Plant Responses to Air Pollution and Global Change. New York: Springer-Verlag, 141–147.
  • Taniguchi Y, Ohkawa H, Masumoto C, Fukuda T, Tamai T, Lee K, Sudoh S, Tsuchida H, Sasaki H, Fukayama H, Miyao M. (2008). Overproduction of C4 photosynthetic enzymes in transgenic rice plants: an approach to introduce the C4-like photosynthetic pathway into rice. J Exp Bot, 59, 1799–1809.
  • Tsuchida H, Tamai T, Fukayama H, Agarie S, Nomura M, Onodera H, Ono K, Nishizawa Y, Lee BH, Hirose S, Toki S, Ku MSB, Matsuoka M, Miyao M. (2001). High level expression of C4-specific NADP–malic enzyme in leaves and impairment of photoautotrophic growth in a C3 plant, rice. Plant Cell Physiol, 42, 138–145.
  • von Caemmerer S, Furbank RT. (2003). The C4 pathway: an efficient CO2 pump. Photosynth Res, 77, 191–207.
  • Wang JM, Li RZ. (2008). Integration of C4-specific ppdk gene of Echinochloa to C3 upland rice and its photosynthesis characteristics analysis. Afr J Biotechnol, 7, 783–787.
  • Westerling AL, Hidalgo HG, Cayan DR, Swetnam TW. (2006). Warming and earlier spring increase western U.S. forest wildfire activity. Science, 313, 940–943.
  • Whitney SM, Baldet P, Hudson GS, Andrews TJ. (2001). Form 1 Rubiscos from non-green algae are expressed abundantly but not assembled in tobacco chloroplasts. Plant J, 26, 535–547.
  • Wild B, Wanek W, Postl W, Richter A. (2010). Contribution of carbon fixed by Rubisco and PEPC to phloem export in the Crassulacean acid metabolism plant Kalanchoe daigremontiana. J Exp Bot, 61, 1375–1383.
  • Wingler A, Walker RP, Chen ZH, Leegood RC. (1999). Phosphoenolpyruvate carboxykinase is involved in the decarboxylation of aspartate in the bundle sheath of maize. Plant Physiol, 120, 539–545.
  • Winter K, Smith JAC. (1996). An introduction to Crassulacean acid metabolism. Biochemical principles and ecological diversity. In: Winter K, Smith JAC, eds. Crassulacean Acid Metabolism: Biochemistry, Ecophysiology and Evolution. Berlin: Springer, 1–13.
  • Winzer T, Heineke D, Bauwe H. (2001). Growth and phenotype of potato plants expressing an antisense gene of P-protein of glycine decarboxylase under control of a promoter with preference for the mesophyll. Ann Appl Biol, 138, 9–15.
  • Yuan DY, Duan MJ, Tan YN, Yi ZL, Yuan LP, Sun SS. (2007). Generating marker-free transgenic homozygous rice restorer lines with PEPC and PPDK genes by Agrobacterium-mediated transformation using super binary vector. Hybrid Rice, 22, 57–63 (in Chinese with English abstract).
  • Zerai DB, Glenn EP, Chatervedi R, Lu Z Mamood, AN, Nelson SG, Ray DT. (2010). Potential for improvement of Salicornia bigelovii through selective breeding. Ecol Eng, 36, 730–739.
  • Zhang BJ, Hua C, Zhou F, Zhou QC, Chen QZ, Wang RF, Jiao DM. (2008). Photosynthetic characteristics of transgenic rice with PEPC+PPDK gene. Sci Agric Sin, 41, 3008–3014 (in Chinese with English abstract).
  • Zhang JF, Bandyopadhyay A, Sellappan K, Wang GY, Xie HA, Datta K, Datta SK. (2010). Characterization of a C4 maize pyruvate orthophosphate dikinase expressed in C3 transgenic rice plants. Afr J Biotechnol, 9, 234–242.

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