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Photosynthesis Research

, Volume 117, Issue 1–3, pp 121–131 | Cite as

Photorespiration and carbon concentrating mechanisms: two adaptations to high O2, low CO2 conditions

  • James V. MoroneyEmail author
  • Nadine Jungnick
  • Robert J. DiMario
  • David J. Longstreth
Review

Abstract

This review presents an overview of the two ways that cyanobacteria, algae, and plants have adapted to high O2 and low CO2 concentrations in the environment. First, the process of photorespiration enables photosynthetic organisms to recycle phosphoglycolate formed by the oxygenase reaction catalyzed by ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco). Second, there are a number of carbon concentrating mechanisms that increase the CO2 concentration around Rubisco which increases the carboxylase reaction enhancing CO2 fixation. This review also presents possibilities for the beneficial modification of these processes with the goal of improving future crop yields.

Keywords

Calvin–Benson–Bassham cycle Carbon concentrating mechanism Carbonic anhydrase Cyanobacteria Photorespiration Rubisco 

Abbreviations

CA

Carbonic anhydrase

CBB cycle

Calvin–Benson–Bassham cycle

CCM

Carbon (dioxide) concentrating mechanism

PEP

Phosphoenolpyruvate

Rubisco

Ribulose-1,5-bisphosphate carboxylase/oxygenase

RuBP

Ribulose-1,5-bisphosphate

References

  1. Andrews TJ, Lorimer GH, Tolbert NE (1973) Ribulose diphosphate oxygenase. 1. Synthesis of phosphoglycolate by fraction-1 protein of leaves. Biochem-Us 12(1):11–18. doi: 10.1021/Bi00725a003 CrossRefGoogle Scholar
  2. Badger M, Kaplan A, Berry J (1980) Internal inorganic carbon pool of Chlamydomonas reinhardtii: evidence for a carbon dioxide-concentrating mechanism. Plant Physiol 66(3):407PubMedCrossRefGoogle Scholar
  3. Bainbridge G, Madgwick P, Parmar S, Mitchell R, Paul M, Pitts J, Keys AJ, Parry MAJ (1995) Engineering Rubisco to change its catalytic properties. J Exp Bot 46:1269–1276CrossRefGoogle Scholar
  4. Bauwe H, Hagemann M, Fernie AR (2010) Photorespiration: players, partners and origin. Trends Plant Sci 15(6):330–336. doi: 10.1016/j.tplants.2010.03.006 PubMedCrossRefGoogle Scholar
  5. Bauwe H, Hagemann M, Kern R, Timm S (2012) Photorespiration has a dual origin and manifold links to central metabolism. Curr Opin Plant Biol 15(3):269–275. doi: 10.1016/j.pbi.2012.01.008 PubMedCrossRefGoogle Scholar
  6. Benson AA, Bassham JA, Calvin M, Goodale TC, Haas VA, Stepka W (1950) The path of carbon in photosynthesis. 5. Paper chromatography and radioautography of the products. J Am Chem Soc 72(4):1710–1718. doi: 10.1021/Ja01160a080 CrossRefGoogle Scholar
  7. Blackwell RD, Murray AJS, Lea PJ, Kendall AC, Hall NP, Turner JC, Wallsgrove RM (1988) The value of mutants unable to carry out photorespiration. Photosynth Res 16(1–2):155–176. doi: 10.1007/Bf00039491 CrossRefGoogle Scholar
  8. Bowes G, Ogren WL, Hageman RH (1971) Phosphoglycolate production catalyzed by ribulose diphosphate carboxylase. Biochem Biophys Res Commun 45(3):716–722. doi: 10.1016/0006-291X(71)90475-X PubMedCrossRefGoogle Scholar
  9. Cannon GC, Heinhorst S, Kerfeld CA (2010) Carboxysomal carbonic anhydrases: Structure and role in microbial CO2 fixation. Biochim Biophys Acta (BBA)—Proteins & Proteomics 1804(2):382–392. doi: 10.1016/j.bbapap.2009.09.026 CrossRefGoogle Scholar
  10. Chollet R, Ogren WL (1975) Regulation of photorespiration in C3 and C4 species. Bot Rev 41(2):137–179. doi: 10.1007/Bf02860828 CrossRefGoogle Scholar
  11. Christin P-A, Osborne C (2013) The recurrent assembly of C4 photosynthesis, an evolutionary tale. Photosynthesis research (in press)Google Scholar
  12. Cleland WW, Andrews TJ, Gutteridge S, Hartman FC, Lorimer GH (1998) Mechanism of Rubisco: the carbamate as general base. Chem Rev 98(2):549–561. doi: 10.1021/Cr970010r PubMedCrossRefGoogle Scholar
  13. Dai ZY, Ku MSB, Edwards GE (1993) C4 photosynthesis—the CO2-concentrating mechanism and photorespiration. Plant Physiol 103(1):83–90PubMedGoogle Scholar
  14. Duanmu D, Miller AR, Horken KM, Weeks DP, Spalding MH (2009) Knockdown of limiting-CO2-induced gene HLA3 decreases HCO3 transport and photosynthetic Ci affinity in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 106(14):5990–5995. doi: 10.1073/pnas.0812885106 PubMedCrossRefGoogle Scholar
  15. Edwards GE, Furbank RT, Hatch MD, Osmond CB (2001) What does it take to be C-4? Lessons from the evolution of C-4 photosynthesis. Plant Physiol 125(1):46–49. doi: 10.1104/Pp.125.1.46 PubMedCrossRefGoogle Scholar
  16. Eisenhut M, Ruth W, Haimovich M, Bauwe H, Kaplan A, Hagemann M (2008) The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants. Proc Natl Acad Sci USA 105(44):17199–17204. doi: 10.1073/pnas.0807043105 PubMedCrossRefGoogle Scholar
  17. Espie G, Kandasamy R (1994) Monensin inhibition of Na+-dependent HCO3 transport distinguishes it from Na+-independent HCO3 transport and provides evidence for Na+/HCO3 symport in the cyanobacterium Synechococcus UTEX 625. Plant Physiol 104(4):1419–1428PubMedGoogle Scholar
  18. Fukuzawa H, Suzuki E, Komukai Y, Miyachi S (1992) A gene homologous to chloroplast carbonic anhydrase (icfA) is essential to photosynthetic carbon dioxide fixation by Synechococcus PCC7942. Proc Natl Acad Sci USA 89(10):4437–4441PubMedCrossRefGoogle Scholar
  19. Funke RP, Kovar JL, Weeks DP (1997) Intracellular carbonic anhydrase is essential to photosynthesis in Chlamydomonas reinhardtii at atmospheric levels of CO2. Demonstration via genomic complementation of the high-CO2-requiring mutant ca-1. Plant physiol 114(1):237–244PubMedCrossRefGoogle Scholar
  20. Furbank RT, von Caemmerer S, Sheehy J, Edwards G (2009) C-4 rice: a challenge for plant phenomics. Funct Plant Biol 36(10–11):845–856. doi: 10.1071/Fp09185 CrossRefGoogle Scholar
  21. Genkov T, Meyer M, Griffiths H, Spreitzer RJ (2010) Functional hybrid Rubisco enzymes with plant small subunits and algal large subunits. J Biol Chem 285(26):19833–19841. doi: 10.1074/jbc.M110.124230 PubMedCrossRefGoogle Scholar
  22. Govindjee, Shevela D (2011) Adventures with cyanobacteria: a personal perspective. Front Plant Sci 2:28. doi: 10.3389/fpls.2011.00028 PubMedCrossRefGoogle Scholar
  23. Hagemann M, Eisenhut M, Hackenberg C, Bauwe H (2010) Pathway and importance of photorespiratory 2-phosphoglycolate metabolism in cyanobacteria. Adv Exp Med Biol 675:91–108. doi: 10.1007/978-1-4419-1528-3_6 PubMedCrossRefGoogle Scholar
  24. Hatch MD (2002) C-4 photosynthesis: discovery and resolution. Photosynth Res 73(1–3):251–256. doi: 10.1023/A:1020471718805 PubMedCrossRefGoogle Scholar
  25. Hesketh J (1967) Enhancement of photosynthetic CO2 assimilation in absence of oxygen as dependent upon species and temperature. Planta 76(4):371–374. doi: 10.1007/Bf00387543 CrossRefGoogle Scholar
  26. Husic DW, Husic HD, Tolbert NE (1987) The oxidative photosynthetic carbon-cycle or C2 cycle. Crit Rev Plant Sci 5(1):45–100. doi: 10.1080/07352688709382234 CrossRefGoogle Scholar
  27. Jordan DB, Ogren WL (1981a) A sensitive assay procedure for simultaneous determination of ribulose-1,5-bisphosphate carboxylase and oxygenase activities. Plant Physiol 67(2):237–245. doi: 10.1104/Pp.67.2.237 PubMedCrossRefGoogle Scholar
  28. Jordan DB, Ogren WL (1981b) Species variation in the specificity of ribulose-biphosphate carboxylase-oxygenase. Nature 291(5815):513–515. doi: 10.1038/291513a0 CrossRefGoogle Scholar
  29. Karlsson J, Clarke AK, Chen Z-Y, Hugghins SY, Park Y-I, Husic HD, Moroney JV, Samuelsson G (1998) A novel [alpha]-type carbonic anhydrase associated with the thylakoid membrane in Chlamydomonas reinhardtii is required for growth at ambient CO2. EMBO J 17(5):1208–1216PubMedCrossRefGoogle Scholar
  30. Kasting JF (1987) Theoretical constraints on oxygen and carbon-dioxide concentrations in the precambrian atmosphere. Precambrian Res 34(3–4):205–229. doi: 10.1016/0301-9268(87)90001-5 PubMedCrossRefGoogle Scholar
  31. Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch HJ, Rosenkranz R, Stabler N, Schonfeld B, Kreuzaler F, Peterhansel C (2007) Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nat Biotechnol 25(5):593–599. doi: 10.1038/Nbt1299 PubMedCrossRefGoogle Scholar
  32. Kern R, Bauwe H, Hagemann M (2011) Evolution of enzymes involved in the photorespiratory 2-phosphoglycolate cycle from cyanobacteria via algae toward plants. Photosynth Res 109(1–3):103–114. doi: 10.1007/s11120-010-9615-z PubMedCrossRefGoogle Scholar
  33. Klein MG, Zwart P, Bagby SC, Cai F, Chisholm SW, Heinhorst S, Cannon GC, Kerfeld CA (2009) Identification and structural analysis of a novel carboxysome shell protein with implications for metabolite transport. J Mol Biol 392(2):319–333. doi: 10.1016/j.jmb.2009.03.056 PubMedCrossRefGoogle Scholar
  34. Kozaki A, Takeba G (1996) Photorespiration protects C3 plants from photooxidation. Nature 384(6609):557–560. doi: 10.1038/384557a0 CrossRefGoogle Scholar
  35. 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(1):43–50. doi: 10.1046/j.1467-7652.2003.00003.x PubMedCrossRefGoogle Scholar
  36. Long BM, Badger MR, Whitney SM, Price GD (2007) Analysis of carboxysomes from Synechococcus PCC7942 reveals multiple Rubisco complexes with carboxysomal proteins CcmM and CcaA. J Biol Chem 282(40):29323–29335. doi: 10.1074/jbc.M703896200 PubMedCrossRefGoogle Scholar
  37. Lorimer GH, Andrews TJ, Tolbert NE (1973) Ribulose Diphosphate Oxygenase. 2. Further Proof of Reaction-Products and Mechanism of Action. Biochem-Us 12(1):18–23. doi: 10.1021/Bi00725a004 CrossRefGoogle Scholar
  38. Ludwig M (2013) Evolution of the C4 photosynthetic pathway: events at the cell and molecular levels. Photosynthesis research (in press)Google Scholar
  39. Ma Y, Pollock SV, Xiao Y, Cunnusamy K, Moroney JV (2011) Identification of a novel gene, CIA6, required for normal pyrenoid formation in Chlamydomonas reinhardtii. Plant Physiol 156(2):884–896. doi: 10.1104/pp.111.173922 PubMedCrossRefGoogle Scholar
  40. Moroney JV, Tolbert NE (1985) Inorganic carbon uptake by Chlamydomonas reinhardtii. Plant Physiol 77(2):253–258PubMedCrossRefGoogle Scholar
  41. Moroney JV, Wilson BJ, Tolbert NE (1986) Glycolate metabolism and excretion by Chlamydomonas Reinhardtii. Plant Physiol 82(3):821–826. doi: 10.1104/Pp.82.3.821 PubMedCrossRefGoogle Scholar
  42. Moroney JV, Husic HD, Tolbert NE, Kitayama M, Manuel LJ, Togasaki RK (1989) Isolation and characterization of a mutant of Chlamydomonas reinhardtii deficient in the CO2 concentrating mechanism. Plant Physiol 89(3):897–903PubMedCrossRefGoogle Scholar
  43. Moroney JV, Ma Y, Frey WD, Fusilier KA, Pham TT, Simms TA, DiMario RJ, Yang J, Mukherjee B (2011) The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles. Photosynth Res 109(1–3):133–149. doi: 10.1007/s11120-011-9635-3 PubMedCrossRefGoogle Scholar
  44. Nobel P (2009) Physicochemical and environmental plant physiology, 4th edn. Elsevier, OxfordGoogle Scholar
  45. Ogawa T, Katoh A, Sonoda M (1998) Molecular mechanisms of CO2 concentration and proton extrusion in cyanobacteria. Paper presented at the Stress Responses of Photosynthetic Organisms, AmsterdamGoogle Scholar
  46. Ohkawa H, Sonoda M, Katoh H, Ogawa T (1998) The use of mutants in the analysis of the CO2-concentrating mechanism in cyanobacteria. Botany 76(6):1035–1042CrossRefGoogle Scholar
  47. Omata T, Price GD, Badger MR, Okamura M, Gohta S, Ogawa T (1999) Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC 7942. Proc Natl Acad Sci USA 96(23):13571–13576PubMedCrossRefGoogle Scholar
  48. Omata T, Yamaguchi O, Takahashi Y, Nishimura T (2002) Structure, function and regulation of the cyanobacterial high-affinity bicarbonate transporter, BCT1. Funct Plant Biol 29(3):151–159CrossRefGoogle Scholar
  49. Orús M, Rodriguez M, Martinez F, Marco E (1995) Biogenesis and ultrastructure of carboxysomes from wild type and mutants of Synechococcus sp. strain PCC 7942. Plant Physiol 107(4):1159–1166PubMedGoogle Scholar
  50. Pena KL, Castel SE, de Araujo C, Espie GS, Kimber MS (2010) Structural basis of the oxidative activation of the carboxysomal gamma-carbonic anhydrase, CcmM. Proc Natl Acad Sci USA 107(6):2455–2460. doi: 10.1073/pnas.0910866107 PubMedCrossRefGoogle Scholar
  51. Peterhansel C, Maurino VG (2011) Photorespiration redesigned. Plant Physiol 155(1):49–55. doi: 10.1104/pp.110.165019 PubMedCrossRefGoogle Scholar
  52. Pierce J, Carlson TJ, Williams JG (1989) A cyanobacterial mutant requiring the expression of ribulose bisphosphate carboxylase from a photosynthetic anaerobe. Proc Natl Acad Sci USA 86(15):5753–5757PubMedCrossRefGoogle Scholar
  53. Pollock SV, Prout DL, Godfrey AC, Lemaire SD, Moroney JV (2004) The Chlamydomonas reinhardtii proteins CCP1 and CCP2 are required for long-term growth, but are not necessary for efficient photosynthesis, in a low-CO2 environment. Plant Mol Biol 56(1):125–132. doi: 10.1007/s11103-004-2650-4 PubMedCrossRefGoogle Scholar
  54. Price GD, Badger MR (1989a) Expression of human carbonic anhydrase in the cyanobacterium Synechococcus PCC7942 creates a high CO2-requiring phenotype : evidence for a central role for carboxysomes in the CO2 concentrating mechanism. Plant Physiol 91(2):505–513PubMedCrossRefGoogle Scholar
  55. Price GD, Badger MR (1989b) Isolation and characterization of high CO2-requiring-mutants of the cyanobacterium Synechococcus PCC7942: two phenotypes that accumulate inorganic carbon but are apparently unable to generate CO2 within the carboxysome. Plant Physiol 91(2):514–525. doi: 10.1104/pp.91.2.514 PubMedCrossRefGoogle Scholar
  56. Price G, Badger M (2002) Advances in understanding how aquatic photosynthetic organisms utilize sources of dissolved inorganic carbon for CO2 fixation. Funct Plant Biol 29(3):117–121CrossRefGoogle Scholar
  57. Price GD, Coleman JR, Badger MR (1992) Association of carbonic anhydrase activity with carboxysomes isolated from the cyanobacterium Synechococcus PCC7942. Plant Physiol 100(2):784–793PubMedCrossRefGoogle Scholar
  58. Price G, Maeda S-I, Omata T, Badger M (2002) Modes of active inorganic carbon uptake in the cyanobacterium, Synechococcus sp. PCC7942. Funct Plant Biol 29:131–149CrossRefGoogle Scholar
  59. Price GD, Woodger FJ, Badger MR, Howitt SM, Tucker L (2004) Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc Natl Acad Sci USA 101(52):18228–18233. doi: 10.1073/pnas.0405211101 PubMedCrossRefGoogle Scholar
  60. Price GD, Badger MR, Woodger FJ, Long BM (2008) Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59(7):1441–1461. doi: 10.1093/Jxb/Erm112 PubMedCrossRefGoogle Scholar
  61. Price GD, Badger MR, von Caemmerer S (2011) The prospect of using cyanobacterial bicarbonate transporters to improve leaf photosynthesis in C-3 crop plants. Plant Physiol 155(1):20–26. doi: 10.1104/pp.110.164681 PubMedCrossRefGoogle Scholar
  62. Rawat M, Henk MC, Lavigne LL, Moroney JV (1996) Chlamydomonas reinhardtii mutants without Ribulose-1,5-bisphosphate carboxylase-oxygenase lack a detectable pyrenoid. Planta 198(2):263–270CrossRefGoogle Scholar
  63. Sage RF (2004) The evolution of C4 photosynthesis. New Phytol 161(2):341–370. doi: 10.1111/j.1469-8137.2004.00974.x CrossRefGoogle Scholar
  64. Sage RF, Christin PA, Edwards EJ (2011) The C-4 plant lineages of planet earth. J Exp Bot 62(9):3155–3169. doi: 10.1093/Jxb/Err048 PubMedCrossRefGoogle Scholar
  65. Sage RF, Sage TL, Kocacinar F (2012) Photorespiration and the evolution of C-4 photosynthesis. Annu Rev Plant Biol 63(63):19–47PubMedCrossRefGoogle Scholar
  66. Schou L, Benson AA, Bassham JA, Calvin M (1950) The path of carbon in photosynthesis. 11. The role of glycolic acid. Physiol Plantarum 3(4):487–495. doi: 10.1111/j.1399-3054.1950.tb07676.x CrossRefGoogle Scholar
  67. Schwarz R, Reinhold L, Kaplan A (1995) Low activation state of ribulose-1,5-bisphosphate carboxylase/oxygenase in carboxysome-defective Synechococcus mutants. Plant Physiol 108(1):183–190. doi: 10.1104/pp.108.1.183 PubMedGoogle Scholar
  68. Sharkey TD (1988) Estimating the rate of photorespiration in leaves. Physiol Plantarum 73(1):147–152. doi: 10.1111/j.1399-3054.1988.tb09205.x CrossRefGoogle Scholar
  69. Shibata M, Ohkawa H, Katoh H, Shimoyama M, Ogawa T (2002) Two CO2 uptake systems in cyanobacteria: four systems for inorganic carbon acquisition in Synechocystis sp. strain PCC6803. Funct Plant Biol 29(2/3):123–129CrossRefGoogle Scholar
  70. S-i Maeda, Badger MR, Price GD (2002) Novel gene products associated with NdhD3/D4-containing NDH-1 complexes are involved in photosynthetic CO2 hydration in the cyanobacterium, Synechococcus sp. PCC7942. Mol Microbiol 43(2):425–435. doi: 10.1046/j.1365-2958.2002.02753.x CrossRefGoogle Scholar
  71. So AK, John-McKay M, Espie GS (2002a) Characterization of a mutant lacking carboxysomal carbonic anhydrase from the cyanobacterium Synechocystis PCC6803. Planta 214(3):456–467PubMedCrossRefGoogle Scholar
  72. So AKC, Cot SSW, Espie GS (2002b) Characterization of the C-terminal extension of carboxysomal carbonic anhydrase from Synechocystis sp. PCC6803. Funct Plant Biol 29(3):183–194CrossRefGoogle Scholar
  73. Somanchi A, Handley E, Moroney J (1998) Chlamydomonas reinhardtii cDNAs upregulated in low-CO2 conditions: expression and analyses. Botany 76(6):1003–1009CrossRefGoogle Scholar
  74. Somerville CR, Ogren WL (1982) Genetic-modification of photo-respiration. Trends Biochem Sci 7(5):171–174. doi: 10.1016/0968-0004(82)90130-X CrossRefGoogle Scholar
  75. Spalding MH, Spreitzer RJ, Ogren WL (1983a) Carbonic anhydrase-deficient mutant of Chlamydomonas reinhardii requires elevated carbon dioxide concentration for photoautotrophic growth. Plant Physiol 73(2):268–272PubMedCrossRefGoogle Scholar
  76. Spalding MH, Spreitzer RJ, Ogren WL (1983b) Reduced inorganic carbon transport in a CO2-requiring mutant of Chlamydomonas reinhardii. Plant Physiol 73(2):273–276PubMedCrossRefGoogle Scholar
  77. Spreitzer RJ (1993) Genetic dissection of Rubisco structure and function. Annu Rev Plant Physiol 44:411–434. doi: 10.1146/annurev.pp.44.060193.002211 CrossRefGoogle Scholar
  78. Spreitzer RJ, Salvucci ME (2002) Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Annu Rev Plant Biol 53:449–475. doi: 10.1146/annurev.arplant.53.100301.135233 PubMedCrossRefGoogle Scholar
  79. Tanaka S, Kerfeld CA, Sawaya MR, Cai F, Heinhorst S, Cannon GC, Yeates TO (2008) Atomic-level models of the bacterial carboxysome shell. Science 319(5866):1083–1086. doi: 10.1126/science.1151458 PubMedCrossRefGoogle Scholar
  80. Tcherkez GGB, Farquhar GD, Andrews TJ (2006) Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc Natl Acad Sci USA 103(19):7246–7251. doi: 10.1073/pnas.0600605103 PubMedCrossRefGoogle Scholar
  81. Tholen D, Zhu XG (2011) The mechanistic basis of internal conductance: a theoretical analysis of mesophyll cell photosynthesis and CO2 diffusion. Plant Physiol 156(1):90–105. doi: 10.1104/pp.111.172346 PubMedCrossRefGoogle Scholar
  82. Timm S, Mielewczik M, Florian A, Frankenbach S, Dreissen A, Hocken N, Fernie AR, Walter A, Bauwe H (2012) High-to-Low CO2 Acclimation Reveals Plasticity of the Photorespiratory Pathway and Indicates Regulatory Links to Cellular Metabolism of Arabidopsis. PLoS One 7(8):e42809. doi: 10.1371/journal.pone.0042809 PubMedCrossRefGoogle Scholar
  83. Tolbert NE (1973) Glycolate biosynthesis. Curr Top Cell Regul 7:21–50Google Scholar
  84. Tsai Y, Sawaya MR, Cannon GC, Cai F, Williams EB, Heinhorst S, Kerfeld CA, Yeates TO (2007) Structural analysis of CsoS1A and the protein shell of the Halothiobacillus neapolitanus carboxysome. PLoS Biol 5(6):1345–1354. doi: 10.1371/journal.pbio.0050144 CrossRefGoogle Scholar
  85. Turner JS, Brittain EG (1962) Oxygen as a factor in photosynthesis. Biol Rev 37(1):130–170. doi: 10.1111/j.1469-185X.1962.tb01607.x PubMedCrossRefGoogle Scholar
  86. von Caemmerer S, Evans JR (2010) Enhancing C-3 photosynthesis. Plant Physiol 154(2):589–592. doi: 10.1104/pp.110.160952 CrossRefGoogle Scholar
  87. von Caemmerer S, Quick WP, Furbank RT (2012) The development of C-4 rice: current progress and future challenges. Science 336(6089):1671–1672. doi: 10.1126/science.1220177 CrossRefGoogle Scholar
  88. Wang Y, Spalding MH (2006) An inorganic carbon transport system responsible for acclimation specific to air levels of CO2 in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 103(26):10110–10115. doi: 10.1073/pnas.0603402103 PubMedCrossRefGoogle Scholar
  89. Warburg O (1920) Über die Geschwindigkeit der photochemischen Kohlensäurezersetzung in lebenden Zellen. II. Biochemische Zeitschrift 103:188–217Google Scholar
  90. Weber APM, von Caemmerer S (2010) Plastid transport and metabolism of C-3 and C-4 plants - comparative analysis and possible biotechnological exploitation. Curr Opin Plant Biol 13(3):257–265. doi: 10.1016/j.pbi.2010.01.007 PubMedCrossRefGoogle Scholar
  91. Whitney SM, Sharwood RE (2008) Construction of a tobacco master line to improve Rubisco engineering in chloroplasts. J Exp Bot 59(7):1909–1921. doi: 10.1093/Jxb/Erm311 PubMedCrossRefGoogle Scholar
  92. Whitney SM, Houtz RL, Alonso H (2011) Advancing our understanding and capacity to engineer nature’s CO2-sequestering enzyme Rubisco. Plant Physiol 155(1):27–35. doi: 10.1104/pp.110.164814 PubMedCrossRefGoogle Scholar
  93. Yeates TO, Kerfeld CA, Heinhorst S, Cannon GC, Shively JM (2008) Protein-based organelles in bacteria: carboxysomes and related microcompartments. Nat Rev Microbiol 6(9):681–691. doi: 10.1038/nrmicro1913 PubMedCrossRefGoogle Scholar
  94. Yu J-W, Price GD, Song L, Badger MR (1992) Isolation of a putative carboxysomal carbonic anhydrase gene from the cyanobacterium Synechococcus PCC7942. Plant Physiol 100(2):794–800. doi: 10.1104/pp.100.2.794 PubMedCrossRefGoogle Scholar
  95. Zelitch I, Ochoa S (1953) Oxidation and reduction of glycolic and glyoxylic acids in plants. 1. Glycolic acid oxidase. J Biol Chem 201(2):707–718PubMedGoogle Scholar
  96. Zelitch I, Schultes NP, Peterson RB, Brown P, Brutnell TP (2009) High glycolate oxidase activity is required for survival of maize in normal air. Plant Physiol 149(1):195–204. doi: 10.1104/pp.108.128439 PubMedCrossRefGoogle Scholar
  97. Zhu XG, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Ann Rev Plant Biol 61(61):235–261. doi: 10.1146/annurev-arplant-042809-112206 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • James V. Moroney
    • 1
    Email author
  • Nadine Jungnick
    • 1
  • Robert J. DiMario
    • 1
  • David J. Longstreth
    • 1
  1. 1.Department of Biological SciencesLouisiana State UniversityBaton RougeUSA

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