Elements required for an efficient NADP-malic enzyme type C4 photosynthesis

Plant Physiology

Volumn 164, Issue 4, 2014, Pages 2231-2246

  Wang, Yu ^a   Long, Stephen P ^b   Zhu, Xin Guang ^a  

^a Chinese Academy of Sciences   (China)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; CARBON DIOXIDE; MALATE DEHYDROGENASE; MALATE DEHYDROGENASE (OXALOACETATE-DECARBOXYLATING) (NADP+); NITROGEN;

BIOLOGICAL MODEL; LIGHT; METABOLISM; PHOTOSYNTHESIS; PLASMODESMA; RADIATION RESPONSE; REPRODUCIBILITY; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CARBON; CARBON DIOXIDE; CARBON ISOTOPES; LIGHT; MALATE DEHYDROGENASE; MODELS, BIOLOGICAL; NITROGEN; PHOTOSYNTHESIS; PLASMODESMATA; REPRODUCIBILITY OF RESULTS;

EID: 84898717194     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.230284     Document Type: Article

References (95)

1. Arisz WH (1969) Intercellular polar transport and the role of the plasmodesmatain coleoptiles and Vallisneria leaves. Acta Bot Neerl 18: 14-38
2. Aubry S, Brown NJ, Hibberd JM (2011) The role of proteins in C(3) plants prior to their recruitment into the C(4) pathway. J Exp Bot 62: 3049-3059
3. 2 assimilation in Amaranthus edulis L. J Exp Bot 51 (Spec No): 339-346
4. Berry J, Farquhar G (1978) The CO2 concentrating function of C4 photosynthesis. A biochemical model. In Hall D, Coombs J, Goodwin T, eds, Proceedings of the Fourth International Congress on Photosynthesis, Reading, England, 1977. The Biochemical Society, London, pp 119-131
5. Botha CEJ (1992) Plasmodesmatal distribution, structure and frequency in relation to assimilation in C3 and C4 grasses in southern Africa. Planta 187: 348-358
6. Bräutigam A, Hoffmann-Benning S, Weber APM (2008) Comparative proteomics of chloroplast envelopes from C3 and C4 plants reveals specific adaptations of the plastid envelope to C4 photosynthesis and candidate proteins required for maintaining C4 metabolite fluxes. Plant Physiol 148: 568-579
7. Chastain CJ, Failing CJ, Manandhar L, Zimmerman MA, Lakner MM, Nguyen THT (2011) Functional evolution of C(4) pyruvate, orthophosphate dikinase. J Exp Bot 62: 3083-3091
8. Cheng WH, Im KH, Chourey PS (1996) Sucrose phosphate synthase expression at the cell and tissue level is coordinated with sucrose sink-tosource transitions in maize leaf. Plant Physiol 111: 1021-1029
9. Christensen NM, Faulkner C, Oparka K (2009) Evidence for unidirectional flow through plasmodesmata. Plant Physiol 150: 96-104
10. Cleland WW (1963) The kinetics of enzyme-catalyzed reactions with two or more substrates or products. I. Nomenclature and rate equations. Biochim Biophys Acta 67: 104-137
11. Collatz GJ, Ribas-Carbo M, Berry JA (1992) Coupled photosynthesisstomatal conductance model for leaves of C4 plants. Aust J Plant Physiol 19: 519-538
12. Cousins AB, Badger MR, von Caemmerer S (2006) Carbonic anhydrase and its influence on carbon isotope discrimination during C4 photosynthesis: insights from antisense RNA in Flaveria bidentis. Plant Physiol 141: 232-242
13. Cousins AB, Ghannoum O, Von Caemmerer S, Badger MR (2010) Simultaneous determination of Rubisco carboxylase and oxygenase kinetic parameters in Triticum aestivum and Zea mays using membrane inlet mass spectrometry. Plant Cell Environ 33: 444-452
14. Craig H (1957) Isotopic standards for carbon and oxygen and correction factors for mass-spectrometric analysis of carbon dioxide. Geochim Cosmochim Acta 12: 133-149
15. Dai Z, Ku M, Edwards GE (1993) C4 photosynthesis (the CO2-concentrating mechanism and photorespiration). Plant Physiol 103: 83-90
16. 18O-labeling. Plant Physiol 90: 500-511
17. Dengler NG, Nelson T (1999) Leaf structure and development in C4 plants. In Sage RF, Monson RK, eds, C4 Plant Biology. Academic Press, San Diego, pp 133-172
18. 2) concentration. Plant Physiol 59: 86-90
19. 4 plants. Plant Physiol 73: 555-559
20. Engelmann S, Bläsing OE, Gowik U, Svensson P, Westhoff P (2003) Molecular evolution of C4 phosphoenolpyruvate carboxylase in the genus Flaveria: a gradual increase from C3 to C4 characteristics. Planta 217: 717-725
21. Evans JR (1987) The dependence of quantum yield on wavelength and growth irradiance. Aust J Plant Physiol 14: 69-79
22. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78: 9-19
23. 2 diffusion pathway inside leaves. J Exp Bot 60: 2235-2248
24. Evert RF, Eschrich W, Heyser W (1977) Distribution and structure of the plasmodesmata in mesophyll and bundle-sheath cells of Zea mays L. Planta 136: 77-89
25. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40: 503-537
26. Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust J Plant Physiol 11: 539-552
27. 2 assimilation in leaves of C3 species. Planta 149: 78-90
28. Fell DA (1997) Understanding the control of metabolism. In Snell K, ed, Frontiers in Metabolism, Portland Press, London
29. Fernie AR, Geigenberger P, Stitt M (2005) Flux an important, but neglected, component of functional genomics. Curr Opin Plant Biol 8: 174-182
30. Fiehn O (2002) Metabolomics: the link between genotypes and phenotypes. Plant Mol Biol 48: 155-171
31. Fliege R, Flügge UI, Werdan K, Heldt HW (1978) Specific transport of inorganic phosphate, 3-phosphoglycerate and triosephosphates across the inner membrane of the envelope in spinach chloroplasts. Biochim Biophys Acta 502: 232-247
32. Furbank RT, Chitty JA, Jenkins CLD, Taylor WC, Trevanion SJ, von Caemmerer S, Ashton AR (1997) Genetic manipulation of key photosynthetic enzymes in the C4 plant Flaveria bidentis. Aust J Plant Physiol 24: 477-485
33. Furbank RT, Stitt M, Foyer CH (1985) Intercellular compartmentation of sucrose synthesis in leaves of Zea mays L. Planta 164: 172-178
34. 4 acid decarboxylation types? J Exp Bot 62: 3103-3108
35. Hatch MD (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochim Biophys Acta 895: 81-106
36. Hatch MD, Agostino A, Jenkins CLD (1995) Measurement of the leakage of CO2 from bundle-sheath cells of leaves during C4 photosynthesis. Plant Physiol 108: 173-181
37. Hatch MD, Osmond CB (1976) Compartmentation and transport in C, photosynthesis. In Stocking CR, Heber U, eds, Transport in Plants 111: Intracellular Interactions and Transport Processes. Encyclopedia of Plant Physiology, New Series, Vol 3. Springer-Verlag, Berlin, pp 144-184
38. Henderson SA, von Caemmerer S, Farquhar GD (1992) Short-term measurements of carbon isotope discrimination in several C4 species. Aust J Plant Physiol 19: 263-285
39. Hibberd JM, Sheehy JE, Langdale JA (2008) Using C4 photosynthesis to increase the yield of rice-rationale and feasibility. Curr Opin Plant Biol 11: 228-231
40. Kajala K, Covshoff S, Karki S, Woodfield H, Tolley BJ, Dionora MJA, Mogul RT, Mabilangan AE, Danila FR, Hibberd JM, et al (2011) Strategies for engineering a two-celled C-4 photosynthetic pathway into rice. J Exp Bot 62: 3001-3010.
41. Kanai R, Edwards GE (1999) The biochemistry of C4 photosynthesis. In Sage RF, Monson RK, eds, C4 Plant Biology. Academic Press, Toronto, pp 173-211.
42. Kopka J, Schauer N, Krueger S, Birkemeyer C, Usadel B, Bergmüller E, Dörmann P, Weckwerth W, Gibon Y, Stitt M, et al (2005) GMD@CSB. DB: the Golm Metabolome Database. Bioinformatics 21: 1635-1638
43. 2 uptake. Plant Physiol 148: 2144-2155
44. 2 in NADP-malic enzyme type species. Photosynth Res 66: 199-224
45. 2 uptake under free-air concentration enrichment (FACE). Glob Change Biol 10: 951-962
46. Leegood RC (1985) The intercellular compartmentation of metabolites in leaves of Zea mays L. Planta 164: 163-171
47. 3 plants. J Exp Bot 53: 581-590
48. Leegood RC, von Caemmerer S (1989) Some relationships between contents of photosynthetic intermediates and the rate of photosynthetic carbon assimilation in leaves of Zea mays L. Planta 178: 258-266
49. Lefebvre S, Lawson T, Fryer M, 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
50. Long SP (2012) Virtual special issue on food security: greater than anticipated impacts of near-term global atmospheric change on rice and wheat. Glob Change Biol 18: 1489-1490
51. Lunn JE, Furbank RT (1997) Localisation of sucrose-phosphate synthase and starch in leaves of C4 plants. Planta 202: 106-111
52. 3 photosynthesis. J Exp Bot 62: 3061-3069
53. Majeran W, Cai Y, Sun Q, vanWijk KJ (2005) Functional differentiation of bundle sheath and mesophyll maize chloroplasts determined by comparative proteomics. Plant Cell 17: 3111-3140
54. Majeran W, Friso G, Ponnala L, Connolly B, Huang MS, Reidel E, Zhang CK, Asakura Y, Bhuiyan NH, Sun Q, et al (2010) Structural and metabolic transitions of C4 leaf development and differentiation defined by microscopy and quantitative proteomics in maize. Plant Cell 22: 3509-3542
55. Majeran W, Zybailov B, Ytterberg AJ, Dunsmore J, Sun Q, van Wijk KJ (2008) Consequences of C4 differentiation for chloroplast membrane proteomes in maize mesophyll and bundle sheath cells. Mol Cell Proteomics 7: 1609-1638
56. Matsuoka M, Furbank RT, Fukayama H, Miyao M (2001) Molecular engineering of C-4 photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 52: 297-314
57. 2 concentration of maize leaves and its influence on stomatal movement. J Exp Bot 13: 284-293
58. 2 uptake in C 3 and C 4 grasses. Photosynth Res 3: 153-159
59. Moss DN (1962) The limiting carbon dioxide concentration for photosynthesis. Nature 193: 587
60. 2 partial-pressure and leaf inversion. Planta 189: 182-190
61. 4 species. Plant Physiol 84: 1096-1101
62. Oksman-Caldentey KM, Saito K (2005) Integrating genomics and metabolomics for engineering plant metabolic pathways. Curr Opin Biotechnol 16: 174-179
63. Paul MJ, Driscoll SP, Andralojc PJ, Knight JS, Gray JC, Lawlor DW (2000) Decrease of phosphoribulokinase activity by antisense RNA in transgenic tobacco: definition of the light environment under which phosphoribulokinase is not in large excess. Planta 211: 112-119
64. 2 through the C4 cycle. Plant Physiol 160: 1070-1080
65. Pettersson G, Ryde-Pettersson U (1988) A mathematical model of the Calvin photosynthesis cycle. Eur J Biochem 175: 661-672
66. Poolman MG, Fell DA, Thomas S (2000) Modelling photosynthesis and its control. J Exp Bot 51(Spec No): 319-328
67. 2 assimilation via a reduction in ribulose bisphosphate regeneration in transgenic tobacco plants. Planta 195: 369-378
68. 2 fumigation (FACE). BMC Plant Biol 11: 123
69. Saccardy K, Cornic G, Brulfert J, Reyss A (1996) Effect of drought stress on net CO2 uptake by Zea leaves. Planta 199: 589-595
70. Sage RF (2004) The evolution of C4 photosynthesis. New Phytol 161: 341-370
71. 4 photosynthesis. J Exp Bot 62: 2989-3000
72. Sowiński P, Szczepanik J, Minchin PEH (2008) On the mechanism of C4 photosynthesis intermediate exchange between Kranz mesophyll and bundle sheath cells in grasses. J Exp Bot 59: 1137-1147
73. Stitt M, Heldt HW(1981) Simultaneous synthesis and degradation of starch in spinach-chloroplasts in the light. Biochim Biophys Acta 638: 1-11
74. Stitt M, Heldt HW (1985a) Control of photosynthetic sucrose synthesis by fructose-2,6-bisphosphate: intercellular metabolite distribution and properties of the cytosolic fructosebisphosphatase in leaves of Zea mays L. Planta 164: 179-188
75. Stitt M, Heldt HW (1985b) Generation and maintenance of concentration gradients between the mesophyll and bundle sheath in maize leaves. Biochim Biophys Acta 808: 400-414
76. Sumner LW, Mendes P, Dixon RA (2003) Plant metabolomics: large-scale phytochemistry in the functional genomics era. Phytochemistry 62: 817-836
77. Szecowka M, Heise R, Tohge T, Nunes-Nesi A, Vosloh D, Huege J, Feil R, Lunn J, Nikoloski Z, Stitt M, et al (2013) Metabolic fluxes in an illuminated Arabidopsis rosette. Plant Cell 25: 694-714
78. Tamoi M, Nagaoka M, Miyagawa Y, Shigeoka S (2006) Contribution of fructose-1,6-bisphosphatase and sedoheptulose-1,7-bisphosphatase to the photosynthetic rate and carbon flow in the Calvin cycle in transgenic plants. Plant Cell Physiol 47: 380-390
79. 2 leakiness in Amaranthus cruentus, a C4 dicot, grown in high or low light. Plant Cell Physiol 49: 19-29
80. Troughton JH, Card KA, Hendy CH (1974) Photosynthetic pathways and carbon isotope discrimination by plants. Carnegie Inst Wash Yearbook 73: 768-780
81. 2 permeability. Plant Cell 20: 648-657
82. 4 cycle and reductive pentose phosphate pathway under various light intensities in maize leaves. Plant Physiol 84: 549-554
83. 4 plants. Plant Physiol 65: 1017-1022
84. von Caemmerer S (2000) Biochemical Models of Leaf Photosynthesis. CSIRO Publishing, Collingwood, Australia
85. von Caemmerer S, Furbank RT (1999) Modelling C4 photosynthesis. In Sage RF, Monson RK, eds, C4 Plant Biology. Academic Press, Toronto, pp 173-211
86. 2 pump. Photosynth Res 77: 191-207
87. von Caemmerer S, Quick WP, Furbank RT (2012) The development of C rice: current progress and future challenges. Science 336: 1671-1672
88. Weber APM, von Caemmerer S (2010) Plastid transport and metabolism of C3 and C4 plants: comparative analysis and possible biotechnological exploitation. Curr Opin Plant Biol 13: 257-265
89. Weckwerth W (2003) Metabolomics in systems biology. Annu Rev Plant Biol 54: 669-689
90. Wiechert W, Schweissgut O, Takanaga H, Frommer WB (2007) Fluxomics: mass spectrometry versus quantitative imaging. Curr Opin Plant Biol 10: 323-330
91. Winter H, Robinson DG, Heldt HW (1993) Subcellular volumes and metabolite concentrations in barley leaves. Planta 191: 180-190
92. Zhu XG, de Sturler E, Long SP (2007) Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: a numerical simulation using an evolutionary algorithm. Plant Physiol 145: 513-526
93. Zhu XG, Long SP, Ort DR (2008) What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Curr Opin Biotechnol 19: 153-159
94. Zhu XG, Shan LL, Wang Y, Quick WP (2010) C4 rice: an ideal arena for systems biology research. J Integr Plant Biol 52: 762-770
95. Zhu XG, Wang Y, Ort DR, Long SP (2013) e-photosynthesis: A comprehensive dynamic mechanistic model of C3 photosynthesis: from light capture to sucrose synthesis. Plant Cell Environ 36: 1711-1727