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Transcriptional regulation of tocopherol biosynthesis in tomato

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Abstract

Tocopherols, compounds with vitamin E (VTE) activity, are potent lipid-soluble antioxidants synthesized only by photosynthetic organisms. Their biosynthesis requires the condensation of phytyl-diphosphate and homogentisate, derived from the methylerythritol phosphate (MEP) and shikimate pathways (SK), respectively. These metabolic pathways are central in plant chloroplast metabolism and are involved in the biosynthesis of important molecules such as chlorophyll, carotenoids, aromatic amino-acids and prenylquinones. In the last decade, few studies have provided insights into the regulation of VTE biosynthesis and its accumulation. However, the pathway regulatory mechanism/s at mRNA level remains unclear. We have recently identified a collection of tomato genes involved in tocopherol biosynthesis. In this work, by a dedicated qPCR array platform, the transcript levels of 47 genes, including paralogs, were determined in leaves and across fruit development. Expression data were analyzed for correlation with tocopherol profiles by coregulation network and neural clustering approaches. The results showed that tocopherol biosynthesis is controlled both temporally and spatially however total tocopherol content remains constant. These analyses exposed 18 key genes from MEP, SK, phytol recycling and VTE-core pathways highly associated with VTE content in leaves and fruits. Moreover, genomic analyses of promoter regions suggested that the expression of the tocopherol-core pathway genes is trancriptionally coregulated with specific genes of the upstream pathways. Whilst the transcriptional profiles of the precursor pathway genes would suggest an increase in VTE content across fruit development, the data indicate that in the M82 cultivar phytyl diphosphate supply limits tocopherol biosynthesis in later fruit stages. This is in part due to the decreasing transcript levels of geranylgeranyl reductase (GGDR) which restricts the isoprenoid precursor availability. As a proof of concept, by analyzing a collection of Andean landrace tomato genotypes, the role of the pinpointed genes in determining fruit tocopherol content was confirmed. The results uncovered a finely tuned regulation able to shift the precursor pathways controlling substrate influx for VTE biosynthesis and overcoming endogenous competition for intermediates. The whole set of data allowed to propose that 1-deoxy-D-xylulose-5-phosphate synthase and GGDR encoding genes, which determine phytyl-diphosphate availability, together with enzyme encoding genes involved in chlorophyll-derived phytol metabolism appear as the most plausible targets to be engineered aiming to improve tomato fruit nutritional value.

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References

  • Abbasi AR, Hajirezaei M, Hofius D, Sonnewald U, Voll LM (2007) Specific roles of α- and γ-tocopherol in abiotic stress responses of transgenic tobacco plants. Plant Physiol 143:720–738

    Article  Google Scholar 

  • Abushita AA, Hebshi EA, Daood HG, Biacs PA (1997) Determination of antioxidant vitamins in tomatoes. Food Chem 60:207–212

    Article  Google Scholar 

  • Alba R, Payton P, Fei Z, McQuinn R, Debbie P, Martin GB, Tanksley SD, Giovannoni JJ (2005) Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development. Plant Cell 17:2954–2965

    Article  CAS  PubMed  Google Scholar 

  • Almeida J, Quadrana L, Asís R, Setta N, de Godoy F, Bermúdez L, Otaiza SN, Correa da Silva JV, Fernie AR, Carrari F, Rossi M (2011) Genetic dissection of vitamin E biosynthesis in tomato. J Exp Bot 62:3781–3798

    Article  CAS  PubMed  Google Scholar 

  • Andersen CL, Jensen JL, Ørntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64:5245–5250

    Article  CAS  PubMed  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2:28–36

    CAS  PubMed  Google Scholar 

  • Bailey TL, Bodén M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME suite: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208

    Article  CAS  PubMed  Google Scholar 

  • Barsan C, Sanchez-Bel P, Rombaldi C, Egea I, Rossignol M, Kuntz M, Zouine M, Latché A, Bouzayen M, Pech JC (2010) Characteristics of the tomato chromoplast revealed by proteomic analysis. J Exp Bot 61:2413–2431

    Article  CAS  PubMed  Google Scholar 

  • Bombarely A, Menda N, Tecle IY, Buels RM, Strickler S, Fischer-York T, Pujar A, Leto J, Gosselin J, Mueller LA (2011) The Sol Genomics Network (solgenomics.net): growing tomatoes using Perl. Nucleic Acids Res 39:1149–1155

    Article  Google Scholar 

  • Botella-Pavía P, Besumbes O, Phillips MA, Carretero-Paulet L, Boronat A, Rodriguez-Concepcion M (2004) Regulation of carotenoid biosynthesis in plants: evidence for a key role of hydroxymethylbutenyl diphosphate reductase in controlling the supply of plastidial isoprenoid precursors. Plant J 40:188–199

    Article  PubMed  Google Scholar 

  • Bülow L, Engelmann S, Schindler M, Hehl R (2009) AthaMap, integrating transcriptional and post-transcriptional data. Nucleic Acids Res 37:D983–D986

    Article  PubMed  Google Scholar 

  • Busk PK, Pages M (1998) Regulation of abscisic acid-induced transcription. Plant Mol Biol 37:425–435

    Article  CAS  PubMed  Google Scholar 

  • Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

    Article  CAS  PubMed  Google Scholar 

  • Carrari F, Fernie AR (2006) Metabolic regulation underlying tomato fruit development. J Exp Bot 57:1883–1897

    Article  CAS  PubMed  Google Scholar 

  • Carrari F, Baxter C, Usadel B, Urbanczyk-Wochniak E, Zanor MI, Nunes-Nesi A, Nikiforova V, Centero D, Ratzka A, Pauly M, Sweetlove L, Fernie AR (2006) Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behaviour. Plant Physiol 142:1380–1396

    Article  CAS  PubMed  Google Scholar 

  • Carretero-Paulet L, Cairó A, Botella-Pavía P, Besumbes O, Campos N, Boronat A, Rodríguez-Concepción M (2006) Enhanced flux through the methylerythritol 4-phosphate pathway in Arabidopsis plants overexpressing deoxyxylulose 5-phosphate reductoisomerase. Plant Mol Biol 62:683–695

    Article  CAS  PubMed  Google Scholar 

  • Clarke ND, Granek JA (2003) Rank order metrics for quantifying the association of sequence features with gene regulation. Bioinformatics 19:212–218

    Article  CAS  PubMed  Google Scholar 

  • Córdoba E, Salmi M, León P (2009) Unravelling the regulatory mechanisms that modulate the MEP pathway in higher plants. J Exp Bot 60:2933–2943

    Article  PubMed  Google Scholar 

  • Dal Cin V, Tiemana DM, Tohge T, McQuinn R, de Vos RCH, Osorio S, Schmelz EA, Taylor MG, Smits-Kroon MT, Schuurink RC, Haring MA, Giovannoni J, Fernie AR, Klee HJ (2011) Identification of genes in the phenylalanine metabolic pathway by ectopic expression of a MYB transcription factor in tomato fruit. Plant Cell 23:2738–2753

    Article  PubMed  Google Scholar 

  • DellaPenna D, Mène-Saffrané L (2011) Vitamin E. In: Kader JC, Delseny M (eds) Advances in botanical research, vol 59. Academic Press, London, pp 179–227

    Google Scholar 

  • Enfissi EMA, Fraser PD, Lois LM, Boronat A, Schuch W, Bramley PM (2005) Metabolic engineering of the mevalonate and non-mevalonate isopentenyl diphosphate-forming pathways for the production of health-promoting isoprenoids in tomato. Plant Biotech J 3:17–27

    Article  CAS  Google Scholar 

  • Enfissi EM, Barneche F, Ahmed I, Lichtlé C, Gerrish C, McQuinn RP, Giovannoni JJ, Lopez-Juez E, Bowler C, Bramley PM, Fraser PD (2010) Integrative transcript and metabolite analysis of nutritionally enhanced DE-ETIOLATED1 downregulated tomato fruit. Plant Cell 22:1190–1215

    Article  CAS  PubMed  Google Scholar 

  • Expósito-Rodríguez M, Borges AA, Borges-Pérez A, Pérez JA (2008) Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biol 8:131

    Article  PubMed  Google Scholar 

  • Ezcurra I, Ellerström M, Wycliffe P, Stalberg K, Rask L (1999) Interaction between composite elements in the napA promoter: both the B-box ABA-responsive complex and the RY/G complex are necessary for seed-specific expression. Plant Mol Biol 40:699–709

    Article  CAS  PubMed  Google Scholar 

  • Falk J, Munné-Bosch S (2010) Tocochromanol functions in plants: antioxidation and beyond. J Exp Bot 61:1549–1566

    Article  CAS  PubMed  Google Scholar 

  • Fitzpatrick TB, Basset GJC, Borel P, Carrari F, DellaPenna D, Fraser PH, Hellmann H, Osorio S, Rothan C, Valpuesta V, Caris-Veyrat C, Fernie AR (2012) Vitamin deficiencies in humans: can plant science help? Plant Cell 24:395–414

    Article  CAS  PubMed  Google Scholar 

  • Fraser PD, Enfissi EM, Halket JH, Truesdale MR, Yu DM, Gerrish C, Bramley PM (2007) Manipulation of phytoene levels in tomato fruit: effects on isoprenoids, plastids and intermediary metabolism. Plant Cell 19:3194–3211

    Article  CAS  PubMed  Google Scholar 

  • Frith MC (2011) A new repeat-masking method enables specific detection of homologous sequences. Nucleic Acids Res 39:e23

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Guevara-García A, San Roman C, Arroyo A, Cortes ME, De La Luz Gutierrez-Nava M, Leon P (2005) Characterization of the Arabidopsis clb6 mutant illustrates the importance of posttranscriptional regulation of the methyl-d-erythritol 4-phosphate pathway. Plant Cell 17:628–643

    Article  PubMed  Google Scholar 

  • Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19

    Article  PubMed  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300

    Article  CAS  PubMed  Google Scholar 

  • Holländer-Czytko H, Grabowski J, Sandorf I, Weckermann K, Weiler EW (2005) Tocopherol content and activities of tyrosine aminotransferase and cystine lyase in Arabidopsis under stress conditions. J Plant Physiol 162:767–770

    Article  PubMed  Google Scholar 

  • Horvath G, Wessjohann L, Bigirimana J, Jansen M, Guisez Y, Caubergs R, Horemans N (2006a) Differential distribution of tocopherols and tocotrienols in photosynthetic and non-photosynthetic tissues. Phytochemistry 67:1185–1195

    Article  CAS  PubMed  Google Scholar 

  • Horvath G, Wessjohann L, Bigirimana J, Monica H, Jansen M, Guisez Y, Caubergs R, Horemans N (2006b) Accumulation of tocopherols and tocotrienols during seed development of grape (Vitis vinifera L. cv. Albert Lavallee). Plant Physiol Biochem 44:724–731

    Article  CAS  PubMed  Google Scholar 

  • Ischebeck T, Zbierzak AM, Kanwischer M, Dormann P (2006) A salvage pathway for phytol metabolism in Arabidopsis. J Biol Chem 281:2470–2477

    Article  CAS  PubMed  Google Scholar 

  • Jiménez A, Creissen G, Kular B, Firmin J, Robinson S, Verhoeyen M, Mullineaux P (2002) Changes in oxidative processes and components of the antioxidant system during tomato fruit ripening. Planta 214:751–758

    Article  PubMed  Google Scholar 

  • Klee HJ (2010) Improving the flavor of fresh fruits: genomics, biochemistry, and biotechnology. New Phytol 187:44–56

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi N, DellaPenna D (2008) Tocopherol metabolism, oxidation and recycling under high light stress in Arabidopsis. Plant J 55:607–618

    Article  CAS  PubMed  Google Scholar 

  • Krieger-Liszkay A, Trebst A (2006) Tocopherol is the scavenger of singlet oxygen produced by the triplet states of chlorophyll in the PSII reaction centre. J Exp Bot 57:1677–1684

    Article  CAS  PubMed  Google Scholar 

  • Lois R, Dietrich A, Hahlbrock K, Schulz W (1989) A phenylalanine ammonia-lyase gene from parsley: structure, regulation and identification of elicitor and light responsive cis-acting elements. EMBO J 8:1641–1648

    CAS  PubMed  Google Scholar 

  • Lois LM, Rodríguez-Concepción M, Gallego F, Campos N, Boronat A (2000) Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-D-xylulose 5-phosphate synthase. Plant J 22:503–513

    Article  CAS  PubMed  Google Scholar 

  • Loyola J, Verdugo I, González E, Casaretto JA, Ruiz-Lara S (2012) Plastidic isoprenoid biosynthesis in tomato: physiological and molecular analysis in genotypes resistant and sensitive to drought stress. Plant Biol (Stuttg) 14:149–156

    CAS  Google Scholar 

  • Lytovchenko A, Eickmeier I, Pons C, Osorio S, Szecowka M, Lehmberg K, Arrivault S, Tohge T, Pineda B, Anton MT, Hedtke B, Lu Y, Fisahn J, Bock R, Stitt M, Grimm B, Granell A, Fernie AR (2011) Tomato fruit photosynthesis is seemingly unimportant in primary metabolism and ripening but plays a considerable role in seed development. Plant Physiol 157:1650–1663

    Article  CAS  PubMed  Google Scholar 

  • Mahony S, Benos PV (2007) STAMP: a web tool for exploring DNA-binding motif similarities. Nucleic Acids Res 35:253–258

    Article  Google Scholar 

  • Marshall DR, Brown AHD (1975) Optimum sampling strategies in genetic conservation. In: Frankel OH, Hawkes JG (eds) Crop genetic resources today and tomorrow. Cambridge University Press, Cambridge, pp 15–36

    Google Scholar 

  • Meléndez-Martínez AJ, Fraser PD, Bramley PM (2010) Accumulation of health promoting phytochemicals in wild relatives of tomato and their contribution to in vitro antioxidant activity. Phytochemistry 71:1104–1114

    Article  PubMed  Google Scholar 

  • Milone D, Stegmayer G, Kamenetzky L, Lopez M, Lee JM, Giovannoni JJ, Carrari F (2010) *omeSOM: a software for clustering and visualization of transcriptional and metabolite data mined from interspecific crosses of crop plants. BMC Bioinformatics 11:438–447

    Article  PubMed  Google Scholar 

  • Moco S, Capanoglu E, Tikunov Y, Bino RJ, Boyacioglu D, Hall RD, Vervoort J, De Vos CH (2007) Tissue specialization at the metabolite level is perceived during the development of tomato fruit. J Exp Bot 58:4131–4146

    Article  CAS  PubMed  Google Scholar 

  • Munné-Bosch S, Alegre L (2002) The function of tocopherols and tocotrienols in plants. Crit Rev Plant Sci 21:31–57

    Google Scholar 

  • Naqvi S, Farré G, Zhu C, Sandmann G, Capell T, Christou P (2010) Simultaneous expression of Arabidopsis ρ-hydroxyphenylpyruvate dioxygenase and MPBQ methyltransferase in transgenic corn kernels triples the tocopherol content. Transgenic Res 20:177–181

    Article  PubMed  Google Scholar 

  • Norris SR, Barrette TR, DellaPenna D (1995) Genetic dissection of carotenoid synthesis in Arabidopsis defines plastoquinone as an essential component of phytoene desaturation. Plant Cell 7:2139–2149

    CAS  PubMed  Google Scholar 

  • Paetzold H, Garms S, Bartram S, Wieczorek J, Uros-Gracia EM, Rodriguez-Concepción M, Boland W, Strack D, Hause B, Walter MH (2010) The isogene 1-deoxy-D-xylulose 5-phosphate synthase II controls isoprenoid profiles, precursor pathway allocation and density of tomato trichomes. Molecular Plant ssq032v1-ssq032

  • Pavesi G, Pesole G (2006) Using Weeder for the discovery of conserved transcription factor binding sites. Curr Protoc Bioinformatics Chapter 2: Unit 2.11

  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36

    Article  PubMed  Google Scholar 

  • Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper–Excel-based tool using pair-wise correlations. Biotechnol Lett 26:509–515

    Article  CAS  PubMed  Google Scholar 

  • Phatthiyaa A, Takahashib S, Chareonthiphakornc N, Koyamab T, Wititsuwannakuld D, Wititsuwannakul R (2007) Cloning and expression of the gene encoding solanesyl diphosphate synthase from Hevea brasiliensis. Plant Sci 4:824–831

    Article  Google Scholar 

  • Quadrana L, Rodriguez MC, Lopez M, Bermudez L, Nunes-Nesi A, Fernie AR, Descalzo A, Asis R, Rossi MM, Asurmendi S, Carrari F (2011) Coupling virus induced gene silencing to exogenous green fluorescence protein expression provides a highly efficient system for functional genomics, in Arabidopsis and across all stages of tomato fruit development. Plant Physiol 56:1278–1291

    Article  Google Scholar 

  • Rasmussen S, Dixon RA (1999) Transgene-mediated and elicitor-induced perturbation of metabolic channeling at the entry point into the phenylpropanoid pathway. Plant Cell 11:1537–1551

    CAS  PubMed  Google Scholar 

  • Riewe D, Koohi M, Lisec J, Pfeiffer M, Lippmann R, Schmeichel J, Willmitzer L, Altmann T (2012) A tyrosine aminotransferase involved in tocopherol synthesis in Arabidopsis. Plant J. doi:10.1111/j.1365-313X.2012.05035.x

    Google Scholar 

  • Rippert P, Scimemi C, Dubald M, Matringe M (2004) Engineering plant shikimate pathway for production of tocotrienol and improving herbicide resistance. Plant Physiol 134:92–100

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Villalón A, Gas E, Rodriguez-Concepcion M (2009) Phytoene synthase activity controls the biosynthesis of carotenoids and the supply of their metabolic precursors in dark-grown Arabidopsis seedlings. Plant J 60:424–435

    Article  PubMed  Google Scholar 

  • Ronen G, Carmel-Goren L, Zamir D, Hirschberg J (2000) An alternative pathway to ß-carotene formation in plant chromoplasts discovered by map-based cloning of Beta and old-gold color mutations in tomato. Proc Natl Acad Sci USA 97:11102–11107

    Article  CAS  PubMed  Google Scholar 

  • Rose JKC, Bashir S, Giovannoni JJ, Jahn MM, Saravanan RS (2004) Tackling the plant proteome: practical approaches, hurdles and experimental tools. Plant J 39:715–733

    Article  CAS  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    CAS  PubMed  Google Scholar 

  • Ruijter JM, Ramakers C, Hoogaars WM, Karlen Y, Bakker O, van den Hoff MJ, Moorman AF (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37:e45

    Article  CAS  PubMed  Google Scholar 

  • Sablowski RW, Moyano E, Culianez-Macia FA, Schuch W, Martin C, Bevan M (1994) A flower-specific Myb protein activates transcription of phenylpropanoid biosynthetic genes. EMBO J 13:128–137

    CAS  PubMed  Google Scholar 

  • Sadre R, Gruber J, Frentzen M (2006) Characterization of homogentisate prenyltransferases involved in plastoquinone-9 and tocochromanol biosynthesis. FEBS Lett 580:5357–5362

    Article  CAS  PubMed  Google Scholar 

  • Sattler SE, Gilliland LU, Magallanes-Lundback M, Pollard M, DellaPenna D (2004) Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. Plant Cell 16:1419–1432

    Article  CAS  PubMed  Google Scholar 

  • Schelbert S, Aubry S, Burla B, Agne B, Kessler F, Krupinska K, Hörtensteiner S (2009) Pheophytin pheophorbide hydrolase (pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis. Plant Cell 21:767–785

    Article  CAS  PubMed  Google Scholar 

  • Seo YS, Kim SJ, Harn CH, Kim WT (2011) Ectopic expression of apple fruit homogentisate phytyltransferase gene (MdHPT1) increases tocopherol in transgenic tomato (Solanum lycopersicum cv. Micro-Tom) leaves and fruits. Phytochemistry 72:321–329

    Article  CAS  PubMed  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    Article  CAS  PubMed  Google Scholar 

  • Shen Q, Ho TH (1995) Functional dissection of an abscisic acid(ABA)-inducible gene reveals two independent ABA-responsive complexes each containing a G-box and a novel cis-acting element. Plant Cell 7:295–307

    CAS  PubMed  Google Scholar 

  • Singh RK, Ali SA, Nath P, Sane VA (2011) Activation of ethylene-responsive p-hydroxyphenylpyruvate dioxygenase leads to increased tocopherol levels during ripening in mango. J Exp Bot 62:3375–3385

    Article  CAS  PubMed  Google Scholar 

  • Swanson CI, Evans NC, Barolo S (2010) Structural rules and complex regulatory circuitry constrain expression of a notch- and EGFR-regulated eye enhancer. Dev Cell 18:359–370

    Article  CAS  PubMed  Google Scholar 

  • Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60

    Article  CAS  PubMed  Google Scholar 

  • Takeda J, It Y, Maeda K, Ozeki Y (2002) Assignment of UVB-responsive cis-element and protoplastization-(dilution-) and elicitor-responsive ones in the promoter region of a carrot phenylalanine ammonia-lyase Gene (gDcPAL1). Photochem Photobiol 76:232–238

    Article  CAS  PubMed  Google Scholar 

  • Tharakaraman K, Mariño-Ramírez L, Sheetlin S, Landsman D, Spouge JL (2005) Alignments anchored on genomic landmarks can aid in the identification of regulatory elements. Bioinformatics 21(Suppl 1):i440–i448

    Article  CAS  PubMed  Google Scholar 

  • The Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–197

    Article  Google Scholar 

  • The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641

    Article  Google Scholar 

  • Thijs G, Moreau Y, De Smet F, Mathys J, Lescot M, Rombauts S, Rouze P, De Moor B, Marchal K (2002) INCLUSive: integrated clustering, upstream sequence retrieval and motif sampling. Bioinformatics 18:331–332

    Article  CAS  PubMed  Google Scholar 

  • Tian L, DellaPenna D, Dixon RA (2007) The pds2 mutation is a lesion in the Arabidopsis homogentisate solanesyltransferase gene involved in plastoquinone biosynthesis. Planta 226:1067–1073

    Article  CAS  PubMed  Google Scholar 

  • Traber MG, Sies H (1996) Vitamin E in humans: demand and delivery. Annual Rev Nut 16:321–347

    Article  CAS  Google Scholar 

  • Tzin V, Malitsky S, Zvi MMB, Bedair M, Sumner L, Aharoni A, Galili G (2012) Expression of a bacterial feedback-insensitive 3-deoxy-d-arabino-heptulosonate 7-phosphate synthase of the shikimate pathway in Arabidopsis elucidates potential metabolic bottlenecks between primary and secondary metabolism. New Phytol 194:301–598

    Article  Google Scholar 

  • Valentin HE, Lincoln K, Moshiri F, Jensen PK, Qi Q, Venkatesh TV, Karunanandaa B, Baszis SR, Norris SR, Savidge B, Gruys KJ, Last RL (2006) The Arabidopsis vitamin E pathway gene5-1 mutant reveals a critical role for phytol kinase in seed tocopherol biosynthesis. Plant Cell 18:212–224

    Article  CAS  PubMed  Google Scholar 

  • van Heeringen SJ, Veenstra GJ (2011) GimmeMotifs: a de novo motif prediction pipeline for ChIP-sequencing experiments. Bioinformatics 27:270–271

    Article  PubMed  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3. RESEARCH0034

  • Vranová E, Coman D, Gruissem W (2012) Structure and dynamics of the isoprenoid pathway network. Molecular Plant 5:318–333

    Article  PubMed  Google Scholar 

  • Williams CE, St. Clair DA (1993) Phenetic relationships and levels of variability detected by restriction fragment length polymorphism and random amplified polymorphic DNA analysis of cultivated and wild accessions of Lycopersicon esculentum. Genome 36:619–630

    Article  CAS  PubMed  Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493

    Article  CAS  PubMed  Google Scholar 

  • Witcombe JR, Gilani MM (1979) Variation in cereals from the Himalayas and the optimum strategy for sampling germplasm. J Appl Ecol 16:633–640

    Article  Google Scholar 

  • Wittkopp PJ, Kalay G (2012) Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet 13:59–69

    Article  CAS  Google Scholar 

  • Yelle S, Chetelat RT, Dorais M, Deverna JW, Bennett AB (1991) Sink metabolism in tomato fruit. IV. Genetic and biochemical analysis of sucrose accumulation. Plant Physiol 95:1026–1035

    Article  CAS  PubMed  Google Scholar 

  • Yilmaz A, Mejia-Guerra MK, Kurz K, Liang X, Welch L, Grotewold E (2011) AGRIS: the Arabidopsis Gene Regulatory Information Server, an update. Nucleic Acids Res 39 (database issue)

  • Zbierzak AM, Kanwischer M, Wille C, Vidi PA, Giavalisco P, Lohmann A, Briesen I, Porfirova S, Bréhélin C, Kessler F, Dörmann P (2009) Intersection of the tocopherol and plastoquinol metabolic pathways at the plastoglobule. Biochem J 425:389–399

    Article  PubMed  Google Scholar 

  • Zhang B, Horvath S (2005) A general framework for weighted gene co-expression network analysis. Stat Appl Genet Mol Biol 4. Article 17

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Acknowledgments

L.Q. was recipient of a fellowship of Agencia Nacional de Promoción Científica y Tecnológica and Consejo Nacional de Investigaciones Científicas y Técnicas (Argentina). J.A. L.B. and F.G. were recipients of a fellowship of Fundação à Amparo da Pesquisa do Estado de São Paulo (Brazil). J.C.S. was recipient of a fellowship of Conselho Nacional de Desenvolvimento Científico e Tecnológico (Brazil). R.A. and F.C. are members of Consejo Nacional de Investigaciones Científicas y Técnicas (Argentina). This work was carried out in compliance with current laws governing genetic experimentation in Brazil and in Argentina. This work was partially supported with grants from Fundação à Amparo da Pesquisa do Estado de São Paulo, Conselho Nacional de Desenvolvimento Científico e Tecnológico and Universidade de São Paulo (Brazil); Max Planck Society (Germany); Instituto Nacional de Tecnologia Agropecuária, Consejo Nacional de Investigaciones Científicas y Técnicas and Agencia Nacional de Promoción Científica y Tecnológica (Argentina); and under the auspices of the European Solanaceae Integrated Project FOOD-CT-2006-016214.

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Authors and Affiliations

  1. Instituto de Biotecnología, Instituto Nacional de Tecnología Agropecuaria and Consejo Nacional de Investigaciones Científicas y Técnicas, PO Box 25, B1712WAA, Castelar, Argentina

    Leandro Quadrana, Tomas Duffy & Fernando Carrari

  2. Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, São Paulo, SP, 05508-900, Brazil

    Juliana Almeida, Junia V. Corrêa da Silva, Fabiana de Godoy, Luisa Bermúdez & Magdalena Rossi

  3. CIBICI, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, CC 5000, Córdoba, Argentina

    Santiago N. Otaiza & Ramon Asís

  4. Max Planck Institute for Molecular Plant Physiology, Wissenschaftspark Gölm, Am Mühlenberg 1, 14476, Potsdam-Golm, Germany

    Alisdair R. Fernie

Authors
  1. Leandro Quadrana
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  2. Juliana Almeida
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  3. Santiago N. Otaiza
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  4. Tomas Duffy
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  5. Junia V. Corrêa da Silva
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  6. Fabiana de Godoy
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  7. Ramon Asís
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  8. Luisa Bermúdez
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  9. Alisdair R. Fernie
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  10. Fernando Carrari
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  11. Magdalena Rossi
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Corresponding author

Correspondence to Magdalena Rossi.

Additional information

Leandro Quadrana, Juliana Almeida, Fernando Carrari and Magdalena Rossi contributed equally to this work.

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Quadrana, L., Almeida, J., Otaiza, S.N. et al. Transcriptional regulation of tocopherol biosynthesis in tomato. Plant Mol Biol 81, 309–325 (2013). https://doi.org/10.1007/s11103-012-0001-4

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  • DOI: https://doi.org/10.1007/s11103-012-0001-4

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