Alteration of the interconversion of pyruvate and malate in the plastid or cytosol of ripening tomato fruit invokes diverse consequences on sugar but similar effects on cellular organic acid, metabolism, and transitory starch accumulation

Plant Physiology

Volumn 161, Issue 2, 2013, Pages 628-643

  Osorio, Sonia ^a,b   Vallarino, José G ^b   Szecowka, Marek ^a   Ufaz, Shai ^c   Tzin, Vered ^c   Angelovici, Ruthie ^c   Galili, Gad ^c   Fernie, Alisdair R ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^b UNIVERSITY OF MÁLAGA   (Spain)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84873248632     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.211094     Document Type: Article

References (84)

1. Araújo WL, Nunes-Nesi A, Osorio S, Usadel B, Fuentes D, Nagy R, Balbo I, Lehmann M, Studart-Witkowski C, Tohge T, et al (2011) Antisense inhibition of the iron-sulphur subunit of succinate dehydrogenase enhances photosynthesis and growth in tomato via an organic acidmediated effect on stomatal aperture. Plant Cell 23: 600-627
2. Bahrami AR, Chen ZH, Walker RP, Leegood RC, Gray JE (2001) Ripeningrelated occurrence of phosphoenolpyruvate carboxykinase in tomato fruit. Plant Mol Biol 47: 499-506
3. Borsani J, Budde CO, Porrini L, Lauxmann MA, Lombardo VA, Murray R, Andreo CS, Drincovich MF, Lara MV (2009) Carbon metabolism of peach fruit after harvest: changes in enzymes involved in organic acid and sugar level modifications. J Exp Bot 60: 1823-1837
4. Bugos RC, Chiang VL, Zhang XH, Campbell ER, Podila GK, Campbell WH (1995) RNA isolation from plant tissues recalcitrant to extraction in guanidine. Biotechniques 19: 734-737
5. Carrari F, Baxter C, Usadel B, Urbanczyk-Wochniak E, Zanor MI, Nunes-Nesi A, Nikiforova V, Centero D, Ratzka A, Pauly M, et al (2006) Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant Physiol 142: 1380-1396
6. Carrari F, Fernie AR (2006) Metabolic regulation underlying tomato fruit development. J Exp Bot 57: 1883-1897
7. Centeno DC, Osorio S, Nunes-Nesi A, Bertolo AL, Carneiro RT, Araújo WL, Steinhauser MC, Michalska J, Rohrmann J, Geigenberger P, et al (2011) Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening. Plant Cell 23: 162-184
8. Chollet R, Vidal J, O'Leary MH (1996) Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 273-298
9. 4NADP-malic enzyme: expression in Escherichia coli and characterization of site-directed mutants at the putative nucleosidebinding sites. J Biol Chem 278: 13757-13764
10. Drincovich MF, Casati P, Andreo CS (2001) NADP-malic enzyme from plants: a ubiquitous enzyme involved in different metabolic pathways. FEBS Lett 490: 1-6
11. Edwards GE, Andreo CS (1992) NADP-malic enzyme from plants. Phytochemistry 31: 1845-1857
12. Famiani F, Baldicchi A, Battistelli A, Moscatello S, Walker RP (2009) Soluble sugar and organic acid contents and the occurrence and potential role of phosphoenolpyruvate carboxykinase (PEPCK) in gooseberry (Ribes grossularia L.). J Hortic Sci Biotechnol 84: 249-254
13. Famiani F, Cultrera NG, Battistelli A, Casulli V, Proietti P, Standardi A, Chen ZH, Leegood RC, Walker RP (2005) Phosphoenolpyruvate carboxykinase and its potential role in the catabolism of organic acids in the flesh of soft fruit during ripening. J Exp Bot 56: 2959-2969
14. Farineau J (1977) Light versus dark carbon metabolism in cherry tomato fruits. II. Relationship between malate metabolism and photosynthetic activity. Plant Physiol 60: 877-880
15. Fernandez AI, Viron N, Alhagdow M, Karimi M, Jones M, Amsellem Z, Sicard A, Czerednik A, Angenent G, Grierson D, et al (2009) Flexible tools for gene expression and silencing in tomato. Plant Physiol 151: 1729-1740
16. Fernie AR, Martinoia E (2009) Malate: jack of all trades or master of a few? Phytochemistry 70: 828-832
17. Fernie AR, Roscher A, Ratcliffe RG, Kruger NJ (2001) Fructose 2,6-bisphosphate activates pyrophosphate:fructose-6-phosphate 1-phosphotransferase and increases triose phosphate to hexose phosphate cycling in heterotrophic cells. Planta 212: 250-263
18. Franke KE, Adams DO (1995) Cloning of a full-length cDNA for malic enzyme (EC 1.1.1.40) from grape berries. Plant Physiol 107: 1009-1010
19. Fraser P, Bickmore W (2007) Nuclear organization of the genome and the potential for gene regulation. Nature 447: 413-417
20. Fraser PD, Enfissi EM, Halket JM, Truesdale MR, Yu D, Gerrish C, Bramley PM (2007) Manipulation of phytoene levels in tomato fruit: effects on isoprenoids, plastids, and intermediary metabolism. Plant Cell 19: 3194-3211
21. Geigenberger P (2011) Regulation of starch biosynthesis in response to a fluctuating environment. Plant Physiol 155: 1566-1577
22. Geigenberger P, Fernie AR, Gibon Y, Christ M, Stitt M (2000) Metabolic activity decreases as an adaptive response to low internal oxygen in growing potato tubers. Biol Chem 381: 723-740
23. Geigenberger P, Muller-Rober B, Stitt M (1999) Contribution of adenosine 59-diphosphoglucose pyrophosphorylase to the control of starch synthesis is decreased by water stress in growing potato tubers. Planta 209: 338-345
24. Geigenberger P, Regierer B, Nunes-Nesi A, Leisse A, Urbanczyk-Wochniak E, Springer F, van Dongen JT, Kossmann J, Fernie AR (2005) Inhibition of de novo pyrimidine synthesis in growing potato tubers leads to a compensatory stimulation of the pyrimidine salvage pathway and a subsequent increase in biosynthetic performance. Plant Cell 17: 2077-2088
25. Geigenberger P, Reimholz R, Geiger M, Merlo L, Canale V, Stitt M (1997) Regulation of sucrose and starch metabolism in potato tubers in response to short-term water deficit. Planta 201: 502-518 Gerrard
26. Gerrard Wheeler M, Arias CL, Maurino VG, Andreo CS, Drincovich MF (2009) Identification of domains involved in the allosteric regulation of cytosolic Arabidopsis thaliana NADP-malic enzyme. FEBS Lett 276: 5665-5677 Gerrard
27. Gerrard Wheeler MC, Tronconi MA, DrincovichMF, Andreo CS, Flügge UI, Maurino VG (2005) A comprehensive analysis of the NADP-malic enzyme gene family of Arabidopsis. Plant Physiol 139: 39-51
28. Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell (Suppl) 16: S170-S180
29. Halinska A, Frenkel C (1991) Acetaldehyde stimulation of net gluconeogenic carbon movement from applied malic acid in tomato fruit pericarp tissue. Plant Physiol 95: 954-960
30. Jenner HL, Winning BM, Millar AH, Tomlinson KL, Leaver CJ, Hill SA (2001) NAD malic enzyme and the control of carbohydrate metabolism in potato tubers. Plant Physiol 126: 1139-1149
31. Karlova R, Rosin FM, Busscher-Lange J, Parapunova V, Do PT, Fernie AR, Fraser PD, Baxter C, Angenent GC, de Maagd RA (2011) Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell 23: 923-941
32. Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45: 41-59
33. +malic enzyme and organic acid levels in developing tomato fruits. J Am Soc Hortic Sci 117: 799-801
34. Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, Geigenberger P (2005) Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci USA 102: 11118-11123
35. Lara MV, Drincovich MF, Andreo CS (2004) Induction of a Crassulacean acid-like metabolism in the C(4) succulent plant, Portulaca oleracea L: study of enzymes involved in carbon fixation and carbohydrate metabolism. Plant Cell Physiol 45: 618-626
36. 2. Nat Cell Biol 10: 1217-1223
37. Leegood RC, Walker RP (2003) Regulation and roles of phosphoenolpyruvate carboxykinase in plants. Arch Biochem Biophys 414: 204-210
38. Lombardo VA, Osorio S, Borsani J, Lauxmann MA, Bustamante CA, Budde CO, Andreo CS, Lara MV, Fernie AR, Drincovich MF (2011) Metabolic profiling during peach fruit development and ripening reveals the metabolic networks that underpin each developmental stage. Plant Physiol 157: 1696-1710
39. Luedemann A, Strassburg K, Erban A, Kopka J (2008) TagFinder for the quantitative analysis of gas chromatography-mass spectrometry (GCMS)-based metabolite profiling experiments. Bioinformatics 24: 732-737
40. Matas AJ, Gapper NE, Chung MY, Giovannoni JJ, Rose JK (2009) Biology and genetic engineering of fruit maturation for enhanced quality and shelf-life. Curr Opin Biotechnol 20: 197-203
41. Meyer S, De Angeli A, Fernie AR, Martinoia E (2010) Intra-and extracellular excretion of carboxylates. Trends Plant Sci 15: 40-47
42. Michalska J, Zauber H, Buchanan BB, Cejudo FJ, Geigenberger P (2009) NTRC links built-in thioredoxin to light and sucrose in regulating starch synthesis in chloroplasts and amyloplasts. Proc Natl Acad Sci USA 106: 9908-9913
43. Moco S, Capanoglu E, Tikunov Y, Bino RJ, Boyacioglu D, Hall RD, Vervoort J, De Vos RC (2007) Tissue specialization at the metabolite level is perceived during the development of tomato fruit. J Exp Bot 58: 4131-4146
44. Moing A, Aharoni A, Biais B, Rogachev I, Meir S, Brodsky L, Allwood JW, Erban A, Dunn WB, Kay L, et al (2011) Extensive metabolic crosstalk in melon fruit revealed by spatial and developmental combinatorial metabolomics. New Phytol 190: 683-696
45. Müller-Röber BT, Kossmann J, Hannah LC, Willmitzer L, Sonnewald U (1990) One of two different ADP-glucose pyrophosphorylase genes from potato responds strongly to elevated levels of sucrose. Mol Gen Genet 224: 136-146
46. Nashilevitz S, Melamed-Bessudo C, Izkovich Y, Rogachev I, Osorio S, Itkin M, Adato A, Pankratov I, Hirschberg J, Fernie AR, et al (2010) An orange ripening mutant links plastid NAD(P)H dehydrogenase complex activity to central and specialized metabolism during tomato fruit maturation. Plant Cell 22: 1977-1997
47. Nielsen TH, Krapp A, Roper-Schwarz U, Stitt M (1998) The sugarmediated regulation of genes encoding the small subunit of Rubisco and the regulatory subunit of ADP glucose pyrophosphorylase is modified by phosphate and nitrogen. Plant Cell Environ 21: 443-454
48. Nunes-Nesi A, Araújo WL, Fernie AR (2011) Targeting mitochondrial metabolism and machinery as a means to enhance photosynthesis. Plant Physiol 155: 101-107
49. Nunes-Nesi A, Carrari F, Gibon Y, Sulpice R, Lytovchenko A, Fisahn J, Graham J, Ratcliffe RG, Sweetlove LJ, Fernie AR (2007) Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. Plant J 50: 1093-1106
50. Nunes-Nesi A, Carrari F, Lytovchenko A, Smith AM, Loureiro ME, Ratcliffe RG, Sweetlove LJ, Fernie AR (2005) Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiol 137: 611-622
51. Oliver SN, Tiessen A, Fernie AR, Geigenberger P (2008) Decreased expression of plastidial adenylate kinase in potato tubers results in an enhanced rate of respiration and a stimulation of starch synthesis that is attributable to post-translational redox-activation of ADP-glucose pyrophosphorylase. J Exp Bot 59: 315-325
52. Osorio S, Alba R, Damasceno CM, Lopez-Casado G, Lohse M, Zanor MI, Tohge T, Usadel B, Rose JK, Fei Z, et al (2011) Systems biology of tomato fruit development: combined transcript, protein, and metabolite analysis of tomato transcription factor (nor, rin) and ethylene receptor (Nr) mutants reveals novel regulatory interactions. Plant Physiol 157: 405-425
53. Osorio S, Alba R, Nikoloski Z, Kochevenko A, Fernie AR, Giovannoni JJ (2012) Integrative comparative analyses of transcript and metabolite profiles from pepper and tomato ripening and development stages uncovers species-specific patterns of network regulatory behavior. Plant Physiol 159: 1713-1729
54. Penfield S, Clements S, Bailey KJ, Gilday AD, Leegood RC, Gray JE, Graham IA (2012) Expression and manipulation of phosphoenolpyruvate carboxykinase 1 identifies a role for malate metabolism in stomatal closure. Plant J 69: 679-688
55. Rademacher T, Häusler RE, Hirsch HJ, Zhang L, Lipka V, Weier D, Kreuzaler F, Peterhänsel C (2002) An engineered phosphoenolpyruvate carboxylase redirects carbon and nitrogen flow in transgenic potato plants. Plant J 32: 25-39
56. Regierer B, Fernie AR, Springer F, Perez-Melis A, Leisse A, Koehl K, Willmitzer L, Geigenberger P, Kossmann J (2002) Starch content and yield increase as a result of altering adenylate pools in transgenic plants. Nat Biotechnol 20: 1256-1260
57. Roessner-Tunali U, Liu J, Leisse A, Balbo I, Perez-Melis A, Willmitzer L, Fernie AR (2004) Kinetics of labelling of organic and amino acids in potato tubers by gas chromatography-mass spectrometry following incubation in (13)C labelled isotopes. Plant J 39: 668-679
58. Rose JK, Bennett AB (1999) Cooperative disassembly of the cellulosexyloglucan network of plant cell walls: parallels between cell expansion and fruit ripening. Trends Plant Sci 4: 176-183
59. Ruffner HP (1982) Metabolism of tartaric and malic acids in Vitis: a review. Part A. Vitis 21: 346-358
60. Ruffner HP, Possner D, Brem S, Rast DM (1984) The physiological role of malic enzyme in grape ripening. Planta 160: 444-448
61. Runquist M, Kruger NJ (1999) Control of gluconeogenesis by isocitrate lyase in endosperm of germinating castor bean seedlings. Plant J 19: 423-431
62. Schauer N, Semel Y, Roessner U, Gur A, Balbo I, Carrari F, Pleban T, Perez-Melis A, Bruedigam C, Kopka J, et al (2006) Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat Biotechnol 24: 447-454
63. 2evolution in spinach leaves. Plant Physiol Biochem 26: 473-481
64. Schippers JH, Nunes-Nesi A, Apetrei R, Hille J, Fernie AR, Dijkwel PP (2008) The Arabidopsis onset of leaf death5 mutation of quinolinate synthase affects nicotinamide adenine dinucleotide biosynthesis and causes early ageing. Plant Cell 20: 2909-2925
65. Seymour G, Poole M, Manning K, King GJ (2008) Genetics and epigenetics of fruit development and ripening. Curr Opin Plant Biol 11: 58-63
66. Sowokinos JR (1981) Pyrophosphorylases in Solanum tuberosum. II. Catalytic properties and regulation of ADP-glucose and UDP-glucose pyrophosphorylase activities in potatoes. Plant Physiol 68: 924-929
67. Sowokinos JR, Preiss J (1982) Pyrophosphorylases in Solanum tuberosum. III. Purification, physical, and catalytic properties of ADPglucose pyrophosphorylase in potatoes. Plant Physiol 69: 1459-1466
68. Stitt M, Rees T (1979) Capacities of pea chloroplasts to catalyse the oxidative pentose phosphate pathway and glycolysis. Phytochemistry 18: 1905-1911
69. Sweetlove LJ, Beard KFM, Nunes-Nesi A, Fernie AR, Ratcliffe RG (2010) Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci 15: 462-470
70. Sweetlove LJ, Muller-Rober B, Willmitzer L, Hill SA (1999) The contribution of adenosine 59-diphosphoglucose pyrophosphorylase to the control of starch synthesis in potato tubers. Planta 209: 330-337
71. Sweetman C, Deluc LG, Cramer GR, Ford CM, Soole KL (2009) Regulation of malate metabolism in grape berry and other developing fruits. Phytochemistry 70: 1329-1344
72. Szecowka M, Osorio S, Obata T, Araújo WL, Rohrmann J, Nunes-Nesi A, Fernie AR (2012) Decreasing the mitochondrial synthesis of malate in potato tubers does not affect plastidial starch synthesis, suggesting that the physiological regulation of ADPglucose pyrophosphorylase is context dependent. Plant Physiol 160: 2227-2238
73. Tauberger E, Fernie AR, Emmermann M, Renz A, Kossmann J, Willmitzer L, Trethewey RN (2000) Antisense inhibition of plastidial phosphoglucomutase provides compelling evidence that potato tuber amyloplasts import carbon from the cytosol in the form of glucose-6-phosphate. Plant J 23: 43-53
74. Tieman D, Taylor M, Schauer N, Fernie AR, Hanson AD, Klee HJ (2006) Tomato aromatic amino acid decarboxylases participate in synthesis of the flavor volatiles 2-phenylethanol and 2-phenylacetaldehyde. Proc Natl Acad Sci USA 103: 8287-8292
75. Tiessen A, Hendriks JH, Stitt M, Branscheid A, Gibon Y, Farré EM, Geigenberger P (2002) Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14: 2191-2213
76. Tiessen A, Prescha K, Branscheid A, Palacios N, McKibbin R, Halford NG, Geigenberger P (2003) Evidence that SNF1-related kinase and hexokinase are involved in separate sugar-signalling pathways modulating post-translational redox activation of ADP-glucose pyrophosphorylase in potato tubers. Plant J 35: 490-500
77. Timm S, Nunes-Nesi A, Pärnik T, Morgenthal K, Wienkoop S, Keerberg O, Weckwerth W, Kleczkowski LA, Fernie AR, Bauwe H (2008) A cytosolic pathway for the conversion of hydroxypyruvate to glycerate during photorespiration in Arabidopsis. Plant Cell 20: 2848-2859
78. Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635-641 van der
79. Van der Merwe MJ, Osorio S, Moritz T, Nunes-Nesi A, Fernie AR (2009) Decreased mitochondrial activities of malate dehydrogenase and fumarase in tomato lead to altered root growth and architecture via diverse mechanisms. Plant Physiol 149: 653-669
80. Voll LM, Zell MB, Engelsdorf T, Saur A, Wheeler MG, Drincovich MF, Weber AP, Maurino VG (2012) Loss of cytosolic NADP-malic enzyme 2 in Arabidopsis thaliana is associated with enhanced susceptibility to Colletotrichum higginsianum. New Phytol 195: 189-202
81. Walker RP, Chen ZH, Tecsi LI, Famiani F, Lea PJ, Leegood RC (1999) Phosphoenolpyruvate carboxykinase plays a role in interactions of carbon and nitrogen metabolism during grape seed development. Planta 210: 9-18
82. Zamboni A, Di Carli M, Guzzo F, Stocchero M, Zenoni S, Ferrarini A, Tononi P, Toffali K, Desiderio A, Lilley KS, et al (2010) Identification of putative stage-specific grapevine berry biomarkers and omics data integration into networks. Plant Physiol 154: 1439-1459
83. Zanor MI, Osorio S, Nunes-Nesi A, Carrari F, Lohse M, Usadel B, Kühn C, Bleiss W, Giavalisco P, Willmitzer L, et al (2009) RNA interference of LIN5 in tomato confirms its role in controlling Brix content, uncovers the influence of sugars on the levels of fruit hormones, and demonstrates the importance of sucrose cleavage for normal fruit development and fertility. Plant Physiol 150: 1204-1218
84. Zhang J, Wang X, Yu O, Tang J, Gu X, Wan X, Fang C (2011) Metabolic profiling of strawberry (Fragaria 3 ananassa Duch.) during fruit development and maturation. J Exp Bot 62: 1103-1118