What can enzymes of C4 photosynthesis do for C3 plants under stress?

Plant Science

Volumn 180, Issue 4, 2011, Pages 575-583

  Doubnerová, Veronika ^a   Ryšlavá, Helena ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

Author keywords

NADP malic enzyme; Phosphoenolpyruvate carboxylase; Plant stress; Pyruvate, phosphate dikinase

Indexed keywords

CARBON DIOXIDE; MALATE DEHYDROGENASE; MALATE DEHYDROGENASE (OXALOACETATE DECARBOXYLATING) (NADP+); MALATE DEHYDROGENASE (OXALOACETATE-DECARBOXYLATING) (NADP+); PHOSPHOENOLPYRUVATE CARBOXYLASE; PYRUVATE PHOSPHATE DIKINASE; VEGETABLE PROTEIN;

CITRIC ACID CYCLE; ENZYMOLOGY; METABOLISM; PH; PHOTOSYNTHESIS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT; REVIEW;

CARBON DIOXIDE; CITRIC ACID CYCLE; HYDROGEN-ION CONCENTRATION; MALATE DEHYDROGENASE; PHOSPHOENOLPYRUVATE CARBOXYLASE; PHOTOSYNTHESIS; PLANT PROTEINS; PLANTS; PYRUVATE, ORTHOPHOSPHATE DIKINASE; STRESS, PHYSIOLOGICAL;

EID: 79952037320     PISSN: 01689452     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plantsci.2010.12.005     Document Type: Review

References (94)

1. Bray E.A., Bailey-Serres J., Weretilnyk E. Responses to abiotic stresses. Biochemistry & Molecular Biology of Plants 2000, 1158-1203. American Society of Plant Physiologists, Rockville, Maryland. B.B. Buchanan, W. Gruissem, R.L. Jones (Eds.).
2. Sage R.F. The evolution of C4 photosynthesis. New Phytol. 2004, 161:341-370.
3. Edwards G.E., Franceschi V.R., Voznesenskaya E.V. Single-cell C4 photosynthesis versus the dual-cell (Kranz) paradigm. Annu. Rev. Plant Biol. 2004, 55:173-196.
4. Lara M.V., Chuong S.D.X., Akhani H., Andreo C.S., Edwards G.E. Species having C4 single-cell-type photosynthesis in the Chenopodiaceae family evolved a photosynthetic phosphoenolpyruvate carboxylase like that of Kranz-type C4 species. Plant Physiol. 2006, 142:673-684.
5. Izui K., Matsumura H., Furumoto T., Kai Y. Phosphoenolpyruvate carboxylase: a new era of structural biology. Annu. Rev. Plant Biol. 2004, 55:69-84.
6. Chollet R., Vidal J., O' Leary M.H. Phosphoenolpyruvate carboxylase: a ubiquitous highly regulated enzyme in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1996, 47:273-298.
7. Nimmo H.G. Control of the phosphorylation of phosphoenolpyruvate carboxylase in higher plants. Arch. Biochem. Biophys. 2003, 414:189-196.
8. Jeanneau M., Vidal J., Gousset-Dupont A., Lebouteiller B., Hodges M., Gerentes D., Perez P. Manipulating PEPC levels in plants. J. Exp. Bot. 2002, 53:1837-1845.
9. Cerny M., Doubnerova V., Muller K., Ryslava H. Characterization of phosphoenolpyruvate carboxylase from mature maize seeds: Properties of phosphorylated and dephosphorylated forms. Biochimie 2010, 92:1362-1370.
10. Sanchez R., Cejudo F.J., Identification expression analysis of a gene encoding a bacterial-type phosphoenolpyruvate carboxylase from Arabidopsis and rice. Plant Physiol. 2003, 132:949-957.
11. Latzko E., Kelly G.J. The many-faceted function of phosphoenolpyruvate carboxylase in C3 plants. Physiol. Vég. 1983, 21:805-815.
12. Seki M., Umezawa T., Urano K., Shinozaki K. Regulatory metabolic networks in drought stress responses. Curr. Opin. Plant Biol. 2007, 10:296-302.
13. Shinozaki K., Yamaguchi-Shinozaki K. Gene networks involved in drought stress response and tolerance. J. Exp. Bot. 2007, 58:221-227.
14. Soussi M., Ocana A., Lluch C. Effects of salt stress on growth, photosynthesis and nitrogen fixation in chick-pea (Cicer arietinum L.). J. Exp. Bot. 1998, 49:1329-1337.
15. Crecelius F., Streb P., Feierabend J. Malate metabolism and reactions of oxidoreduction in cold-hardened winter rye (Secale cereale L.) leaves. J. Exp. Bot. 2003, 54:1075-1083.
16. Cushman J.C., Bohnert H.J. Salt stress induction of crassulacean acid metabolism in a facultative CAM plant. Photosynth. Res. 1992, 34:103-1103.
17. Daniel P.P., Bryant J.A., Woodward F.I. Phosphoenolpyruvate carboxylase from pennywort (Umbilicus rupestris). Changes in properties after exposure to water stress. Biochem. J. 1984, 218:387-393.
18. Gonzalez M.C., Sanchez R., Cejudo F.J. Abiotic stresses affecting water balance induce phosphoenolpyruvate carboxylase expression in roots of wheat seedlings. Planta 2003, 216:985-992.
19. Sanchez R., Flores A., Cejudo F.J. Arabidopsis phosphoenolpyruvate carboxylase genes encode immunologically unrelated polypeptides and are differentially expressed in response to drought and salt stress. Planta 2006, 223:901-909.
20. Rangel A.F., Rao I.M., Braun H.P., Horst W.J. Aluminum resistance in common bean (Phaseolus vulgaris) involves induction and maintenance of citrate exudation from root apices. Physiol. Plant 2010, 138:176-190.
21. Lopez-Millan A.F., Morales F., Andaluz S., Gogorcena Y., Abadia A., De Las Rivas J., Abadia J. Responses of sugar beet roots to iron deficiency. Changes in carbon assimilation and oxygen use. Plant Physiol. 2000, 124:885-898.
22. Dizengremel P., Le Thiec D., Hasenfratz-Sauder M.P., Vaultier M.N., Bagard M., Jolivet Y. Metabolic-dependent changes in plant cell redox power after ozone exposure. Plant Biol. 2009, 11:35-42.
23. Tabuchi M., Abiko T., Yamaya T. Assimilation of ammonium ions and reutilization of nitrogen in rice (Oryza sativa L.). J. Exp. Bot. 2007, 58:2319-2327.
24. Tschoep H., Gibon Y., Carillo P., Armengaud P., Szecowka M., Nunes-Nesi A., Fernie A.R., Koehl K., Stitt M. Adjustment of growth and central metabolism to a mild but sustained nitrogen-limitation in Arabidopsis. Plant Cell Environ. 2009, 32:300-318.
25. Sugiharto B., Sugiyama T. Effects of nitrate and ammonium on gene expression of phosphoenolpyruvate carboxylase and nitrogen metabolism in maize leaf tissue during recovery from nitrogen stress. Plant Physiol. 1992, 98:1403-1408.
26. Lasa B., Frechilla S., Aparicio-Tejo P.M., Lamsfus C. Role of glutamate dehydrogenase and phosphoenolpyruvate carboxylase activity in ammonium nutrition tolerance in roots. Plant Physiol. Biochem. 2002, 40:969-976.
27. Masumoto C., Miyazawa S., Ohkawa H., Fukuda T., Taniguchi Y., Murayama S., Kusano M., Saito K., Fukayama H., Miyao M. Phosphoenolpyruvate carboxylase intrinsically located in the chloroplast of rice plays a crucial role in ammonium assimilation. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:5226-5231.
28. Schultze M., Kondorosi A. Regulation of symbiotic root nodule development. Annu. Rev. Genet. 1998, 32:33-57.
29. Gregory A.L., Hurley B.A., Tran H.T., Valentine A.J., She Y.M., Knowles V.L., Plaxton W.C. In vivo regulatory phosphorylation of the phosphoenolpyruvate carboxylase AtPPC1 in phosphate-starved Arabidopsis thaliana. Biochem. J. 2009, 420:57-65.
30. Toyota K., Koizumi N., Sato F. Transcriptional activation of phosphoenolpyruvate carboxylase by phosphorus deficiency in tobacco. J. Exp. Bot. 2003, 54:961-969.
31. Duff S.M.G., Moorhead G.B.G., Lefebvre D.D., Plaxton W.C. Phosphate starvation inducible bypasses of adenylate and phosphate dependent glycolytic-enzymes in Brassica nigra suspension cells. Plant Physiol. 1989, 90:1275-1278.
32. Moraes T.F., Plaxton W.C. Purification and characterization of phosphoenolpyruvate carboxylase from Brassica napus (rapeseed) suspension cell cultures: implications for phosphoenolpyruvate carboxylase regulation during phosphate starvation and the integration of glycolysis with nitrogen assimilation. Eur. J. Biochem. 2000, 267:4465-4476.
33. Le Roux M.R., Ward C.L., Botha F.C., Valentine A.J. Routes of pyruvate synthesis in phosphorus-deficient lupin roots and nodules. New Phytol. 2006, 169:399-408.
34. Penaloza E., Munoz G., Salvo-Garrido H., Silva H., Corcuera L.J. Phosphate deficiency regulates phosphoenolpyruvate carboxylase expression in proteoid root clusters of white lupin. J. Exp. Bot. 2005, 56:145-153.
35. Schulze J., Temple G., Temple S.J., Beschow H., Vance C.P. Nitrogen fixation by white lupin under phosphorus deficiency. Ann. Bot. 2006, 98:731-740.
36. Chen Z.H., Nimmo G.A., Jenkins G.I., Nimmo H.G. BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis. Biochem. J. 2007, 405:191-198.
37. De Nisi P., Zocchi G. Phosphoenolpyruvate carboxylase in cucumber (Cucumis sativus L.) roots under iron deficiency: activity and kinetic characterization. J. Exp. Bot. 2000, 51:1903-1909.
38. Lopez-Millan A.F., Morales F., Gogorcena Y., Abadia A., Abadia J. Metabolic responses in iron deficient tomato plants. J. Plant Physiol. 2009, 166:375-384.
39. Rabotti G., De Nisi P., Zocchi G. Metabolic implications in the biochemical responses to iron deficiency in cucumber (Cucumis sativus L.) roots. Plant Physiol. 1995, 107:1195-1199.
40. Panda S.K., Baluska F., Matsumoto H. Aluminum stress signaling in plants. Plant Signal Behav. 2009, 4:592-597.
41. Ma J.F., Furukawa J. Recent progress in the research of external Al detoxification in higher plants: a minireview. J. Inorg. Biochem. 2003, 97:46-51.
42. Ermolayev V., Weschke W., Manteuffel R. Comparison of Al-induced gene expression in sensitive and tolerant soybean cultivars. J. Exp. Bot. 2003, 54:2745-2756.
43. Leitao L., Bethenod O., Biolley J.P. The impact of ozone on juvenile maize (Zea mays L.) plant photosynthesis: effects on vegetative biomass pigmentation, and carboxylases (PEPc and Rubisco). Plant Biol. (Stuttg) 2007, 9:478-488.
44. Leitao L., Maoret J.J., Biolley J.P. Changes in PEP carboxylase, rubisco and rubisco activase mRNA levels from maize (Zea mays) exposed to a chronic ozone stress. Biol. Res. 2007, 40:137-153.
45. Dizengremel P. Effects of ozone on the carbon metabolism of forest trees. Plant Physiol. Biochem. 2001, 39:729-742.
46. Fontaine V., Cabane M., Dizengremel P. Regulation of phosphoenolpyruvate carboxylase in Pinus halepensis needles submitted to ozone and water stress. Physiol. Plant 2003, 117:445-452.
47. Inclan R., Gimeno B.S., Dizengremel P., Sanchez M. Compensation processes of Aleppo pine (Pinus halepensis Mill.) to ozone exposure and drought stress. Environ. Pollut. 2005, 137:517-524.
48. Gaucher C., Costanzo N., Afif D., Mauffette Y., Chevrier N., Dizengremel P. The impact of elevated ozone and carbon dioxide on young Acer saccharum seedlings. Physiol. Plant 2003, 117:392-402.
49. Saurer M., Maurer S., Matyssek R., Landolt W., Gunthardtgoerg M.S., Siegenthaler U. The influence of ozone and nutrition on delta-C-13 in Betula pendula. Oecologia 1995, 103:397-406.
50. Dizengremel P., Le Thiec D., Bagard M., Jolivet Y. Ozone risk assessment for plants: central role of metabolism-dependent changes in reducing power. Environ. Pollut. 2008, 156:11-15.
51. Jones J.D., Dangl J.L. The plant immune system. Nature 2006, 444:323-329.
52. Poschenrieder C., Tolra R., Barcelo J. Can metals defend plants against biotic stress?. Trends Plant Sci. 2006, 11:288-295.
53. Dangl J.L., Jones J.D. Plant pathogens and integrated defence responses to infection. Nature 2001, 411:826-833.
54. Hammond-Kosack K., Jones J.D.G. Responses to Plant Pathogens. Biochemistry & Molecular Biology of Plants 2000, 1102-1155. American Society of Plant Physiologists, Rockville, Maryland. B.B. Buchanan, W. Gruissem, R.L. Jones (Eds.).
55. Muller K., Doubnerova V., Synkova H., Cerovska N., Ryslava H. Regulation of phosphoenolpyruvate carboxylase in PVYNTN-infected tobacco plants. Biol. Chem. 2009, 390:245-251.
56. Ryslava H., Muller K., Semoradova S., Synkova H., Cerovska N. Photosynthesis and activity of phosphoenolpyruvate carboxylase in Nicotiana tabacum L. leaves infected by Potato virus A and Potato virus Y. Photosynthetica 2003, 41:357-363.
57. Synkova H., Semoradova S., Schnablova R., Muller K., Pospisilova J., Ryslava H., Malbeck J., Cerovska N. Effects of biotic stress caused by Potato virus Y on photosynthesis in ipt transgenic and control Nicotiana tabacum L. Plant Sci. 2006, 171:607-616.
58. Drincovich M.F., Casati P., Andreo C.S. NADP-malic enzyme from plants: a ubiquitous enzyme involved in different metabolic pathways. FEBS Lett. 2001, 490:1-6.
59. Edwards G.E., Andreo C.S. NADP-malic enzyme from plants. Phytochemistry 1992, 31:1845-1857.
60. Ryslava H., Doubnerova V., Muller K., Batkova P., Schnablova R., Liberda J., Synkova H., Cerovska N. The enzyme kinetics of the NADP-malic enzyme from tobacco leaves. Collect. Czech Chem. Commun. 2007, 72:1420-1434.
61. Chi W., Yang J., Wu N., Zhang F. Four rice genes encoding NADP malic enzyme exhibit distinct expression profiles. Biosci. Biotechnol. Biochem. 2004, 68:1865-1874.
62. Wheeler M.C., Tronconi M.A., Drincovich M.F., Andreo C.S., Flugge U.I., Maurino V.G. A comprehensive analysis of the NADP-malic enzyme gene family of Arabidopsis. Plant Physiol. 2005, 139:39-51.
63. Doubnerova V., Muller K., Cerovska N., Synkova H., Spoustova P., Ryslava H. Effect of Potato virus Y on the NADP-malic enzyme from Nicotiana tabacum L.: mRNA expressed protein and activity. Int. J. Mol. Sci. 2009, 10:3583-3598.
64. Doubnerova V., Janoskova M., Synkova H., Subr Z., Cerovska N., Ryslava H. Effect of Potato virus Y on the activities of antioxidant and anaplerotic enzymes in Nicotiana tabacum L. transgenic plants transformed with the gene for P3 protein. Gen. Appl. Plant Physiol. 2007, 33:123-140.
65. Guo P.G., Baum M., Grando S., Ceccarelli S., Bai G.H., Li R.H., von Korff M., Varshney R.K., Graner A., Valkoun J. Differentially expressed genes between drought-tolerant and drought-sensitive barley genotypes in response to drought stress during the reproductive stage. J. Exp. Bot. 2009, 60:3531-3544.
66. Laporte M.M., Shen B., Tarczynski M.C. Engineering for drought avoidance: expression of maize NADP-malic enzyme in tobacco results in altered stomatal function. J. Exp. Bot. 2002, 53:699-705.
67. Liu S., Cheng Y., Zhang X., Guan Q., Nishiuchi S., Hase K., Takano T. Expression of an NADP-malic enzyme gene in rice (Oryza sativa L.) is induced by environmental stresses; over-expression of the gene in Arabidopsis confers salt and osmotic stress tolerance. Plant Mol. Biol. 2007, 64:49-58.
68. Maurino V.G., Saigo M., Andreo C.S., Drincovich M.F. Non-photosynthetic 'malic enzyme' from maize: a constituvely expressed enzyme that responds to plant defence inducers. Plant Mol. Biol. 2001, 45:409-420.
69. Muller G.L., Drincovich M.F., Andreo C.S., Lara M.V. Nicotiana tabacum NADP-malic enzyme: cloning characterization and analysis of biological role. Plant Cell Physiol. 2008, 49:469-480.
70. Saher S., Fernandez-Garcia N., Piqueras A., Hellin E., Olmos E. Reducing properties, energy efficiency and carbohydrate metabolism in hyperhydric and normal carnation shoots cultured in vitro: a hypoxia stress?. Plant Physiol. Biochem. 2005, 43:573-582.
71. Sun S.B., Shen Q.R., Wan J.M., Liu Z.P. Induced expression of the gene for NADP-malic enzyme in leaves of Aloe vera L. under salt stress. Acta Biochim. Biophys. Sin. 2003, 35:423-429.
72. Valderrama R., Corpas F.J., Carreras A., Gomez-Rodriguez M.V., Chaki M., Pedrajas J.R., Fernandez-Ocana A., Del Rio L.A., Barroso J.B. The dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants. Plant Cell Environ. 2006, 29:1449-1459.
73. Mateos R.M., Bonilla-Valverde D., del Rio L.A., Palma J.M., Corpas F.J. NADP-dehydrogenases from pepper fruits: effect of maturation. Physiol. Plant. 2009, 135:130-139.
74. Franck T., Gaspar T., Kevers C., Penel C., Dommes J., Hausman J.F. Are hyperhydric shoots of Prunus avium L. energy deficient?. Plant Sci. 2001, 160:1145-1151.
75. Krantev A., Yordanova R., Janda T., Szalai G., Popova L. Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J. Plant Physiol. 2008, 165:920-931.
76. Smeets K., Cuypers A., Lambrechts A., Semane B., Hoet P., Van Laere A., Vangronsveld J. Induction of oxidative stress and antioxidative mechanisms in Phaseolus vulgaris after Cd application. Plant Physiol. Biochem. 2005, 43:437-444.
77. Parsley K., Hibberd J.M. The Arabidopsis PPDK gene is transcribed from two promoters to produce differentially expressed transcripts responsible for cytosolic and plastidic proteins. Plant Mol. Biol. 2006, 62:339-349.
78. Burnell J.N., Chastain C.J. Cloning and expression of maize-leaf pyruvate, Pi dikinase regulatory protein gene. Biochem. Biophys. Res. Commun. 2006, 345:675-680.
79. Chastain C.J., Heck J.W., Colquhoun T.A., Voge D.G., Gu X.Y. Posttranslational regulation of pyruvate, orthophosphate dikinase in developing rice (Oryza sativa) seeds. Planta 2006, 224:924-934.
80. Taylor L., Nunes-Nesi A., Parsley K., Leiss A., Leach G., Coates S., Wingler A., Fernie A.R., Hibberd J.M. Cytosolic pyruvate,orthophosphate dikinase functions in nitrogen remobilization during leaf senescence and limits individual seed growth and nitrogen content. Plant J. 2010, 62:641-652.
81. Ohta S., Ishida Y., Usami S. Expression of cold-tolerant pyruvate, orthophosphate dikinase cDNA, and heterotetramer formation in transgenic maize plants. Transgenic Res. 2004, 13:475-485.
82. Chastain C.J., Fries J.P., Vogel J.A., Randklev C.L., Vossen A.P., Dittmer S.K., Watkins E.E., Fiedler L.J., Wacker S.A., Meinhover K.C., Sarath G., Chollet R. Pyruvate,orthophosphate dikinase in leaves and chloroplasts of C3 plants undergoes light-/dark-induced reversible phosphorylation. Plant Physiol. 2002, 128:1368-1378.
83. Chastain C.J., Xu W., Parsley K., Sarath G., Hibberd J.M., Chollet R. The pyruvate, orthophosphate dikinase regulatory proteins of Arabidopsis possess a novel, unprecedented Ser/Thr protein kinase primary structure. Plant J. 2008, 53:854-863.
84. Wang D., Portis A.R., Moose S.P., Long S.P. Cool C4 photosynthesis: pyruvate Pi dikinase expression and activity corresponds to the exceptional cold tolerance of carbon assimilation in Miscanthus x giganteus. Plant Physiol. 2008, 148:557-567.
85. Casati P., Zhang X., Burlingame A.L., Walbot V. Analysis of leaf proteome after UV-B irradiation in maize lines differing in sensitivity. Mol. Cell Proteomics 2005, 4:1673-1685.
86. Huang S., Greenway H., Colmer T.D., Millar A.H. Protein synthesis by rice coleoptiles during prolonged anoxia: implications for glycolysis growth and energy utilization. Ann. Bot. 2005, 96:703-715.
87. Moons A., Valcke R., Van Montagu M. Low-oxygen stress and water deficit induce cytosolic pyruvate orthophosphate dikinase (PPDK) expression in roots of rice, a C3 plant. Plant J. 1998, 15:89-98.
88. Kai Y., Matsumura H., Izui K. Phosphoenolpyruvate carboxylase: three-dimensional structure and molecular mechanisms. Arch. Biochem. Biophys. 2003, 414:170-179.
89. Jeanneau M., Gerentes D., Foueillassar X., Zivy M., Vidal J., Toppan A., Perez P. Improvement of drought tolerance in maize: towards the functional validation of the Zm-Asr1 gene and increase of water use efficiency by over-expressing C4-PEPC. Biochimie 2002, 84:1127-1135.
90. Taniguchi Y., Ohkawa H., Masumoto C., Fukuda T., Tamai T., Lee K., Sudoh S., Tsuchida H., Sasaki H., Fukayama H., Miyao M. Overproduction of C4 photosynthetic enzymes in transgenic rice plants: an approach to introduce the C4-like photosynthetic pathway into rice. J. Exp. Bot. 2008, 59:1799-1809.
91. Miyao M., Fukayama H. Metabolic consequences of overproduction of phosphoenolpyruvate carboxylase in C3 plants. Arch. Biochem. Biophys. 2003, 414:197-203.
92. Casati P., Lara M.V., Andreo C.S. Induction of a C4-like mechanism of CO2 fixation in Egeria densa, a submersed aquatic species. Plant Physiol. 2000, 123:1611-1622.
93. Doubnerova V., Jiraskova A., Janoskova M., Muller K., Bat'kova P., Synkova H., Cerovska N., Ryslava H. The activity and isoforms of NADP-malic enzyme in Nicotiana benthamiana plants under biotic stress. Gen. Physiol. Biophys. 2007, 26:281-289.
94. Carmo-Silva A.E., Bernardes da Silva A., Keys A.J., Parry M.A., Arrabaca M.C. The activities of PEP carboxylase and the C4 acid decarboxylases are little changed by drought stress in three C4 grasses of different subtypes. Photosynth. Res. 2008, 97:223-233.