Integrated bioinformatics to decipher the ascorbic acid metabolic network in tomato

Plant Molecular Biology

Volumn 91, Issue 4-5, 2016, Pages 397-412

  Ruggieri, Valentino ^a   Bostan, Hamed ^a   Barone, Amalia ^a   Frusciante, Luigi ^a   Chiusano, Maria Luisa ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Co expression analysis; Expression atlas; Metabolic pathway; RNA Seq; Solanum lycopersicum; Vitamin C

Indexed keywords

ASCORBIC ACID;

BIOLOGY; CHROMOSOMAL MAPPING; GENE EXPRESSION REGULATION; GENETICS; INTERNET; METABOLISM; PLANT GENE; PROCEDURES; SEQUENCE ANALYSIS; TOMATO;

ASCORBIC ACID; CHROMOSOME MAPPING; COMPUTATIONAL BIOLOGY; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; INTERNET; LYCOPERSICON ESCULENTUM; METABOLIC NETWORKS AND PATHWAYS; SEQUENCE ANALYSIS, RNA;

EID: 84961828058     PISSN: 01674412     EISSN: 15735028     Source Type: Journal    
DOI: 10.1007/s11103-016-0469-4     Document Type: Article

References (97)

1. Agius F, Gonzalez-Lamothe R, Caballero JL, Munoz-Blanco J, Botella MA, Valpuesta V (2003) Engineering increased vitamin C levels in plants by overexpression of a d-galacturonic acid reductase. Nat Biotechnol 21:177–181
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
3. Amaya I et al (2015) Increased antioxidant capacity in tomato by ectopic expression of the strawberry d-galacturonate reductase gene. Biotechnol J 10:490–500
4. Aoki K, Ogata Y, Shibata D (2007) Approaches for extracting practical information from gene co-expression networks in plant biology. Plant Cell Physiol 48:381–390
5. Argyrou E, Sophianopoulou V, Schultes N, Diallinas G (2001) Functional characterization of a maize purine transporter by expression in Aspergillus nidulans. Plant Cell 13:953–964
6. Atmodjo MA et al (2011) Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan:galacturonosyltransferase complex. Proc Natl Acad Sci USA 108:20225–20230
7. Badejo AA, Wada K, Gao Y, Maruta T, Sawa Y, Shigeoka S, Ishikawa T (2012) Translocation and the alternative d-galacturonate pathway contribute to increasing the ascorbate level in ripening tomato fruits together with the d-mannose/l-galactose pathway. J Exp Bot 63:229–239
8. Baich A, Wolfe RG, Reithel FJ (1960) The enzymes of mammary gland. I. Isolation of phosphoglucose isomerase. J Biol Chem 235:3130–3133
9. Bird CR et al (1988) The tomato polygalacturonase gene and ripening-specific expression in transgenic plants. Plant Mol Biol 11:651–662
10. Bolger A et al (2014) The genome of the stress-tolerant wild tomato species Solanum pennellii. Nat Genet 46:1034–1038
11. Bostan H, Chiusano ML (2015) NexGenEx-Tom: a gene expression platform to investigate the functionalities of the tomato genome. BMC Plant Biol 15:48
12. Cai X, Ye J, Hu T, Zhang Y, Ye Z, Li H (2014) Genome-wide classification and expression analysis of nucleobase–ascorbate transporter (NAT) gene family in tomato. Plant Growth Regul 73:19–30
13. Causse M et al (2004) A genetic map of candidate genes and QTLs involved in tomato fruit size and composition. J Exp Bot 55:1671–1685
14. Chen Z, Gallie DR (2004) The ascorbic acid redox state controls guard cell signaling and stomatal movement. Plant Cell 16:1143–1162
15. Chen Z, Young TE, Ling J, Chang SC, Gallie DR (2003) Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc Natl Acad Sci USA 100:3525–3530
16. Chiusano ML et al (2008) ISOL@: an Italian SOLAnaceae genomics resource. BMC Bioinform 9(Suppl 2):S7
17. Conklin PL, Norris SR, Wheeler GL, Williams EH, Smirnoff N, Last RL (1999) Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) biosynthesis. Proc Natl Acad Sci USA 96:4198–4203
18. Cronje C, George GM, Fernie AR, Bekker J, Kossmann J, Bauer R (2012) Manipulation of l-ascorbic acid biosynthesis pathways in Solanum lycopersicum: elevated GDP-mannose pyrophosphorylase activity enhances l-ascorbate levels in red fruit. Planta 235:553–564
19. Cruz-Rus E, Amaya I, Sanchez-Sevilla JF, Botella MA, Valpuesta V (2011) Regulation of l-ascorbic acid content in strawberry fruits. J Exp Bot 62:4191–4201
20. Davey MW et al (2000) Plant l-ascorbic acid: chemistry, function, metabolism, bioavailability and effects of processing. J Sci Food Agric 80:825–860
21. De Tullio MC, Guether M, Balestrini R (2013) Ascorbate oxidase is the potential conductor of a symphony of signaling pathways. Plant Signal Behav 8:e23213
22. Deponte M (2013) Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim Biophys Acta 1830:3217–3266
23. Di Matteo A et al (2010) The ascorbic acid content of tomato fruits is associated with the expression of genes involved in pectin degradation. BMC Plant Biol 10:163
24. Dorokhov YL et al (2006) A novel function for a ubiquitous plant enzyme pectin methylesterase: the enhancer of RNA silencing. FEBS Lett 580:3872–3878
25. Druzhinina TN, Kusov YY, Shibaev VN, Kochetkov NK, Biely P, Kucar S, Bauer S (1975) Uridine diphosphate 2-deoxyglucose. Chemical synthesis, enzymic oxidation and epimerization. Biochim Biophys Acta 381:301–307
26. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868
27. Ficklin SP, Feltus FA (2011) Gene coexpression network alignment and conservation of gene modules between two grass species: maize and rice. Plant Physiol 156:1244–1256
28. Frei B, Birlouez-Aragon I, Lykkesfeldt J (2012) Authors’ perspective: what is the optimum intake of vitamin C in humans? Crit Rev Food Sci Nutr 52:815–829
29. Fries M, Ihrig J, Brocklehurst K, Shevchik VE, Pickersgill RW (2007) Molecular basis of the activity of the phytopathogen pectin methylesterase. EMBO J 26:3879–3887
30. Fukushima A, Nishizawa T, Hayakumo M, Hikosaka S, Saito K, Goto E, Kusano M (2012) Exploring tomato gene functions based on coexpression modules using graph clustering and differential coexpression approaches. Plant Physiol 158:1487–1502
31. Gallie DR (2013) l-Ascorbic acid: a multifunctional molecule supporting plant growth and development. Scientifica 2013:795964
32. Gatzek S, Wheeler GL, Smirnoff N (2002) Antisense suppression of l-galactose dehydrogenase in Arabidopsis thaliana provides evidence for its role in ascorbate synthesis and reveals light modulated l-galactose synthesis. Plant J Cell Mol Biol 30:541–553
33. Gest N, Garchery C, Gautier H, Jimenez A, Stevens R (2013) Light-dependent regulation of ascorbate in tomato by a monodehydroascorbate reductase localized in peroxisomes and the cytosol. Plant Biotechnol J 11:344–354
34. Ghosh Dastidar K, Maitra S, Goswami L, Roy D, Das KP, Majumder AL (2006) An insight into the molecular basis of salt tolerance of l-myo-inositol 1-P synthase (PcINO1) from Porteresia coarctata (Roxb.) Tateoka, a halophytic wild rice. Plant Physiol 140:1279–1296
35. Goulao LF, Oliveira CM (2008) Cell wall modifications during fruit ripening: when a fruit is not the fruit. Trends Food Sci Technol 19:4–25
36. Green MD, Falany CN, Kirkpatrick RB, Tephly TR (1985) Strain differences in purified rat hepatic 3 alpha-hydroxysteroid UDP-glucuronosyltransferase. Biochem J 230:403–409
37. Hanson PM, Yang R-y, Wu J, J-t Chen, Ledesma D, Tsou SCS, Lee T-C (2004) Variation for antioxidant activity and antioxidants in tomato. J Am Soc Hortic Sci 129:704–711
38. Hemavathi et al (2009) Over-expression of strawberry d-galacturonic acid reductase in potato leads to accumulation of vitamin C with enhanced abiotic stress tolerance. Plant Sci 177:659–667
39. Hemavathi et al (2011) Biochemical analysis of enhanced tolerance in transgenic potato plants overexpressing d-galacturonic acid reductase gene in response to various abiotic stresses. Mol Breeding 28:105–115
40. Ioannidi E et al (2009) Expression profiling of ascorbic acid-related genes during tomato fruit development and ripening and in response to stress conditions. J Exp Bot 60:663–678
41. Ishikawa T et al (2006) Functional characterization of d-galacturonic acid reductase, a key enzyme of the ascorbate biosynthesis pathway, from Euglena gracilis. Biosci Biotechnol Biochem 70:2720–2726
42. Ishikawa T et al (2008) The pathway via d-galacturonate/l-galactonate is significant for ascorbate biosynthesis in Euglena gracilis: identification and functional characterization of aldonolactonase. J Biol Chem 283:31133–31141
43. Jain A, Nessler C (2000) Metabolic engineering of an alternative pathway for ascorbic acid biosynthesis in plants. Mol Breeding 6:73–78
44. Johansson K, El-Ahmad M, Friemann R, Jornvall H, Markovic O, Eklund H (2002) Crystal structure of plant pectin methylesterase. FEBS Lett 514:243–249
45. Joshi JG, Handler P (1964) Phosphoglucomutase. I. purification and properties of phosphoglucomutase from escherichia coli. J Biol Chem 239:2741–2751
46. Kotake T, Yamaguchi D, Ohzono H, Hojo S, Kaneko S, Ishida HK, Tsumuraya Y (2004) UDP-sugar pyrophosphorylase with broad substrate specificity toward various monosaccharide 1-phosphates from pea sprouts. J Biol Chem 279:45728–45736
47. Kotchoni SO, Larrimore KE, Mukherjee M, Kempinski CF, Barth C (2009) Alterations in the endogenous ascorbic acid content affect flowering time in Arabidopsis. Plant Physiol 149:803–815
48. Kusano M, Fukushima A (2013) Current challenges and future potential of tomato breeding using omics approaches. Breed Sci 63:31–41
49. Laing WA, Bulley S, Wright M, Cooney J, Jensen D, Barraclough D, MacRae E (2004) A highly specific l-galactose-1-phosphate phosphatase on the path to ascorbate biosynthesis. Proc Natl Acad Sci USA 101(48):16976–16981
50. Laing WA, Wright MA, Cooney J, Bulley SM (2007) The missing step of the l-galactose pathway of ascorbate biosynthesis in plants, an l-galactose guanyltransferase, increases leaf ascorbate content. Proc Natl Acad Sci USA 104:9534–9539
51. Linster CL, Clarke SG (2008) l-Ascorbate biosynthesis in higher plants: the role of VTC2. Trends Plant Sci 13:567–573
52. Linster CL, Van Schaftingen E (2007) Vitamin C. Biosynthesis, recycling and degradation in mammals. FEBS J 274:1–22
53. Lobelle-Rich PA, Reeves RE (1983) Separation and characterization of two UTP-utilizing hexose phosphate uridylyltransferases from Entamoeba histolytica. Mol Biochem Parasitol 7:173–182
54. Locato V, de Pinto MC, De Gara L (2009) Different involvement of the mitochondrial, plastidial and cytosolic ascorbate–glutathione redox enzymes in heat shock responses. Physiol Plant 135:296–306
55. Locato V, Cimini S, Gara LD (2013) Strategies to increase vitamin C in plants: from plant defense perspective to food biofortification. Front Plant Sci 4:152
56. Lorence A, Chevone BI, Mendes P, Nessler CL (2004) myo-inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis. Plant Physiol 134:1200–1205
57. Lunn D, Phan TD, Tucker GA, Lycett GW (2013) Cell wall composition of tomato fruit changes during development and inhibition of vesicle trafficking is associated with reduced pectin levels and reduced softening. Plant Physiol Biochem 66:91–97
58. Maruta T et al (2010) The contribution of Arabidopsis homologs of l-gulono-1,4-lactone oxidase to the biosynthesis of ascorbic acid. Biosci Biotechnol Biochem 74:1494–1497
59. Massot C, Stevens R, Genard M, Longuenesse JJ, Gautier H (2012) Light affects ascorbate content and ascorbate-related gene expression in tomato leaves more than in fruits. Planta 235:153–163
60. Melino VJ, Soole KL, Ford CM (2009) Ascorbate metabolism and the developmental demand for tartaric and oxalic acids in ripening grape berries. BMC Plant Biol 9:145
61. Mellidou I, Keulemans J, Kanellis AK, Davey MW (2012) Regulation of fruit ascorbic acid concentrations during ripening in high and low vitamin C tomato cultivars. BMC Plant Biol 12:239
62. Micheli F (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci 6:414–419
63. Movahedi S, Van de Peer Y, Vandepoele K (2011) Comparative network analysis reveals that tissue specificity and gene function are important factors influencing the mode of expression evolution in Arabidopsis and rice. Plant Physiol 156:1316–1330
64. Ostergaard J, Persiau G, Davey MW, Bauw G, Van Montagu M (1997) Isolation of a cDNA coding for l-galactono-gamma-lactone dehydrogenase, an enzyme involved in the biosynthesis of ascorbic acid in plants. Purification, characterization, cDNA cloning, and expression in yeast. J Biol Chem 272:30009–30016
65. Ozaki S et al (2010) Coexpression analysis of tomato genes and experimental verification of coordinated expression of genes found in a functionally enriched coexpression module. DNA Res Int J Rapid Publ Rep Genes Genomes 17:105–116
66. Pang C-H, Wang B-S (2010) Role of ascorbate peroxidase and glutathione reductase in ascorbate–glutathione cycle and stress tolerance in plants. In: Anjum NA, Chan M-T, Umar S (eds) Ascorbate–glutathione pathway and stress tolerance in plants. Springer, Netherlands, pp 91–113
67. Pieslinger AM, Hoepflinger MC, Tenhaken R (2010) Cloning of Glucuronokinase from Arabidopsis thaliana, the last missing enzyme of the myo-inositol oxygenase pathway to nucleotide sugars. J Biol Chem 285:2902–2910
68. Pilling J, Willmitzer L, Bucking H, Fisahn J (2004) Inhibition of a ubiquitously expressed pectin methyl esterase in Solanum tuberosum L. affects plant growth, leaf growth polarity, and ion partitioning. Planta 219:32–40
69. Qian W, Yu C, Qin H, Liu X, Zhang A, Johansen IE, Wang D (2007) Molecular and functional analysis of phosphomannomutase (PMM) from higher plants and genetic evidence for the involvement of PMM in ascorbic acid biosynthesis in Arabidopsis and Nicotiana benthamiana. Plant J Cell Mol Biol 49:399–413
70. Qin A, Shi Q, Yu X (2011) Ascorbic acid contents in transgenic potato plants overexpressing two dehydroascorbate reductase genes. Mol Biol Rep 38:1557–1566
71. Quackenbush J (2003) Genomics. Microarrays–guilt by association. Science 302:240–241
72. Ruggieri V, Sacco A, Calafiore R, Frusciante L, Barone A (2015) Dissecting a QTL into Candidate Genes Highlighted the Key Role of Pectinesterases in Regulating the Ascorbic Acid Content in Tomato Fruit. The Plant Genome 8. doi:10.3835/plantgenome2014.08.0038
73. Schauer N et al (2006) Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat Biotechnol 24:447–454
74. Schlueter AK, Johnston CS (2011) Vitamin C: overview and Update. J Evid Based Complement Altern Med 16:49–57
75. Shearer LA et al (2014) Fluorescence in situ hybridization and optical mapping to correct scaffold arrangement in the tomato genome. G3 (Bethesda, Md) 4:1395–1405
76. Slater GS, Birney E (2005) Automated generation of heuristics for biological sequence comparison. BMC Bioinform 6:31
77. Smirnoff N, Wheeler GL (2000) Ascorbic acid in plants: biosynthesis and function. Crit Rev Biochem Mol Biol 35:291–314
78. Smirnoff N, Conklin PL, Loewus FA (2001) Biosynthesis of ascorbic acid in plants: a renaissance. Ann Rev Plant Physiol Plant Mol Biol 52:437–467
79. Soukas A, Cohen P, Socci ND, Friedman JM (2000) Leptin-specific patterns of gene expression in white adipose tissue. Genes Dev 14:963–980
80. Stevens R, Buret M, Duffe P, Garchery C, Baldet P, Rothan C, Causse M (2007) Candidate genes and quantitative trait loci affecting fruit ascorbic acid content in three tomato populations. Plant Physiol 143:1943–1953
81. Stevens R, Page D, Gouble B, Garchery C, Zamir D, Causse M (2008) Tomato fruit ascorbic acid content is linked with monodehydroascorbate reductase activity and tolerance to chilling stress. Plant, Cell Environ 31:1086–1096
82. Tedone L, Hancock RD, Alberino S, Haupt S, Viola R (2004) Long-distance transport of l-ascorbic acid in potato. BMC Plant Biol 4:16
83. The UniProt Consortium (2015) UniProt: a hub for protein information. Nucleic Acids Res 43:D204–D212
84. Tian FX, Zang JL, Wang T, Xie YL, Zhang J, Hu JJ (2015) Aldehyde dehydrogenase gene superfamily in populus: organization and expression divergence between paralogous gene pairs. PLoS ONE 10:e0124669
85. Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641
86. Torabinejad J, Donahue JL, Gunesekera BN, Allen-Daniels MJ, Gillaspy GE (2009) VTC4 is a bifunctional enzyme that affects myoinositol and ascorbate biosynthesis in plants. Plant Physiol 150:951–961
87. Troesch B, Hoeft B, McBurney M, Eggersdorfer M, Weber P (2012) Dietary surveys indicate vitamin intakes below recommendations are common in representative Western countries. Br J Nutr 108:692–698
88. Usadel B et al (2004) Identification and characterization of a UDP-d-glucuronate 4-epimerase in Arabidopsis. FEBS Lett 569:327–331
89. Valpuesta V, Botella MA (2004) Biosynthesis of l-ascorbic acid in plants: new pathways for an old antioxidant. Trends Plant Sci 9:573–577
90. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
91. Wen F, Zhu Y, Hawes MC (1999) Effect of pectin methylesterase gene expression on pea root development. Plant Cell 11:1129–1140
92. Wheeler GL, Jones MA, Smirnoff N (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393:365–369
93. Wolucka BA, Van Montagu M (2003) GDP-mannose 3′,5′-epimerase forms GDP-l-gulose, a putative intermediate for the de novo biosynthesis of vitamin C in plants. J Biol Chem 278:47483–47490
94. Wolucka BA, Van Montagu M (2007) The VTC2 cycle and the de novo biosynthesis pathways for vitamin C in plants: an opinion. Phytochemistry 68:2602–2613
95. Yeung KY, Haynor DR, Ruzzo WL (2001) Validating clustering for gene expression data. Bioinformatics 17:309–318
96. Yin L et al (2010) Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminum stress in transgenic tobacco. Planta 231:609–621
97. Zhang C et al (2013) Reducing AsA leads to leaf lesion and defence response in knock-down of the AsA biosynthetic enzyme GDP-d-mannose pyrophosphorylase gene in tomato plant. PLoS ONE 8:e61987