Metabolomics of dates (Phoenix dactylifera) reveals a highly dynamic ripening process accounting for major variation in fruit composition
Tóm tắt
Dates are tropical fruits with appreciable nutritional value. Previous attempts at global metabolic characterization of the date metabolome were constrained by small sample size and limited geographical sampling. In this study, two independent large cohorts of mature dates exhibiting substantial diversity in origin, varieties and fruit processing conditions were measured by metabolomics techniques in order to identify major determinants of the fruit metabolome. Multivariate analysis revealed a first principal component (PC1) significantly associated with the dates’ countries of production. The availability of a smaller dataset featuring immature dates from different development stages served to build a model of the ripening process in dates, which helped reveal a strong ripening signature in PC1. Analysis revealed enrichment in the dry type of dates amongst fruits with early ripening profiles at one end of PC1 as oppose to an overrepresentation of the soft type of dates with late ripening profiles at the other end of PC1. Dry dates are typical to the North African region whilst soft dates are more popular in the Gulf region, which partly explains the observed association between PC1 and geography. Analysis of the loading values, expressing metabolite correlation levels with PC1, revealed enrichment patterns of a comprehensive range of metabolite classes along PC1. Three distinct metabolic phases corresponding to known stages of date ripening were observed: An early phase enriched in regulatory hormones, amines and polyamines, energy production, tannins, sucrose and anti-oxidant activity, a second phase with on-going phenylpropanoid secondary metabolism, gene expression and phospholipid metabolism and a late phase with marked sugar dehydration activity and degradation reactions leading to increased volatile synthesis. These data indicate the importance of date ripening as a main driver of variation in the date metabolome responsible for their diverse nutritional and economical values. The biochemistry of the ripening process in dates is consistent with other fruits but natural dryness may prevent degenerative senescence in dates following ripening. Based on the finding that mature dates present varying extents of ripening, our survey of the date metabolome essentially revealed snapshots of interchanging metabolic states during ripening empowering an in-depth characterization of underlying biology.
Tài liệu tham khảo
Gasmi A. Le Palmier-Dattier: Elaourassia editions; 2012.
Eid NMS, Al-Awadi B, Vauzour D, Oruna-Concha MJ, Spencer JPE. Effect of cultivar type and ripening on the polyphenol content of date palm fruit. J Agr Food Chem. 2013;61(10):2453–60.
Hasnaoui L, Elhoumaizi M, Hakkou A, Wathlet B, Sindic M. Physico-chemical characterization, Classification and Quality Evaluation of Date Palm Fruits of some Moroccan Cultivars. J Sci Res. 2011;3(1):11.
Barreveld WH. Date palm products. In: Repository FCD, editor. Whole dates, vol. 101. Rome: Viale delle Terme di Caracalla; 1993.
El Hadrami AA-K, Jameel M. Socioeconomic and traditional importance of date palm. Emirates J Food Agric. 2012;24(5):15.
Ishurd O, Zahid M, Xiao P, Pan YJ. Protein and amino acids contents of Libyan dates at three stages of development. J Sci Food Agr. 2004;84(5):481–4.
Auda H, Alwandawi H, Aladhami L. Protein and Amino-Acid Composition of 3 Varieties of Iraqi Dates at Different Stages of Development. J Agr Food Chem. 1976;24(2):365–7.
Seymour BG, Poole M, Giovannoni J, Tucker GA. The molecular biology and biochemistry of fruit ripening. UK: Wiley-Blackwell; 2013.
Haider MS, Khan IA, Naqvi SA, Jaskani MJ, Khan RW, Nafees M, et al. Fruit Developmental Stages Effects on Biochemical Attributes in Date Palm. Pak J Agr Sci. 2013;50(4):577–83.
El Arem A, Saafi EB, Flamini G, Issaoui M, Ferchichi A, Hammami M, et al. Volatile and nonvolatile chemical composition of some date fruits (Phoenix dactylifera L.) harvested at different stages of maturity. Int J Food Sci Tech. 2012;47(3):549–55.
Ahmed IA, Ahmed AWK, Robinson RK. Chemical-Composition of Date Varieties as Influenced by the Stage of Ripening. Food Chem. 1995;54(3):305–9.
Amira E, Flamini G, Behija SE, Manel I, Nesrine Z, Ali F, et al. Chemical and aroma volatile compositions of date palm (Phoenix dactylifera L.) fruits at three maturation stages. Food Chem. 2011;127(4):1744–54.
Farag MA, Mohsen M, Heinke R, Wessjohann LA. Metabolomic fingerprints of 21 date palm fruit varieties from Egypt using UPLC/PDA/ESI-qTOF-MS and GC-MS analyzed by chemometrics. Food Res Int. 2014;64:218–26.
Mrabet A, Ferchichi A, Chaira N, BenSalah M, Baazi M, Threadgill Mrabet P. Physico-chemical characteristics and total quality of date palm varieties grown in the Southern of Tunisia. Pak J Biol Sci. 2008;11(7):5.
Johnson DV, Al-khayri JM, Jain SM. Date palm genetic resources and utilization, vol. 1. Africa and the Americas: Springer Science + Business Media Dordrecht; 2015.
Al-Khayri JM, Jain SM, Johnson DV. Date Palm Genetic Resources and utilization, vol. 2. Asia and Europe: Springer Science + Business Media Dordrecht; 2015.
Hamza H, Benabderrahim MA, Elbekkay M, Ferdaous G, Triki T, Ferchichi A. Investigation of genetic variation in Tunisian date palm (Phoenix dactylifera L.) cultivars using ISSR marker systems and their relation with fruit characteristics. Turk J Biol. 2012;36(4):449–58.
Hamza H, Vendramin GG, Ali F. Microsatellite Diversity among Tunisian Date Palm (Phoenix Dactylifera L.) Subpopulations. Pak J Bot. 2011;43(2):1257–64.
Hamza H, Rejeli M, Elbekkay M, Ferchichi A. New Approach for the morphological identification of date palm (Phoenix Dactylifera L.) cultivars in Tunisia. Pak J Bot. 2009;41(6):10.
Suhre K, Gieger C. Genetic variation in metabolic phenotypes: study designs and applications. Nat Rev Genet. 2012;13(11):759–69.
Steingass CB, Carle R, Schmarr HG. Ripening-dependent metabolic changes in the volatiles of pineapple (Ananas comosus (L.) Merr.) fruit: I. Characterization of pineapple aroma compounds by comprehensive two-dimensional gas chromatography–mass spectrometry. Anal Bioanal Chem. 2015;407(9):2591–608.
Cagliani LR, Pellegrino G, Giugno G, Consonni R. Quantification of Coffea arabica and Coffea canephora var. robusta in roasted and ground coffee blends. Talanta. 2013;106:169–73.
Giavalisco P, Li Y, Matthes A, Eckhardt A, Hubberten HM, Hesse H, et al. Elemental formula annotation of polar and lipophilic metabolites using C-13, N-15 and S-34 isotope labelling, in combination with high- resolution mass spectrometry. Plant J. 2011;68(2):364–76.
Cuadros-Inostroza A, Caldana C, Redestig H, Kusano M, Lisec J, Pena-Cortes H, et al. TargetSearch - a Bioconductor package for the efficient preprocessing of GC-MS metabolite profiling data. BMC Bioinformatics. 2009;10:428.
Kopka J, Schauer N, Krueger S, Birkemeyer C, Usadel B, Bergmuller E, et al. [email protected]: the Golm Metabolome Database. Bioinformatics. 2005;21(8):1635–8.
Evans AM, DeHaven CD, Barrett T, Mitchell M, Milgram E. Integrated, Nontargeted Ultrahigh Performance Liquid Chromatography/Electrospray Ionization Tandem Mass Spectrometry Platform for the Identification and Relative Quantification of the Small-Molecule Complement of Biological Systems. Anal Chem. 2009;81(16):6656–67.
DeHaven CD, Evans AM, Dai HP, Lawton KA. Organization of GC/MS and LC/MS metabolomics data into chemical libraries. J Cheminform. 2010;2:9.
DeHaven CD, Evans AM, Dai H, Lawton KA. Software Techniques for Enabling High-Throughput Analysis of Metabolomic Datasets, Metabolomics. 2012.
Eriksson L, Byrne T, Johansson E, Trugg J, Vikstrom C. Multi- and Megavariate Data Analysis. Basic principals and applications: MKS Umetrics AB.
Bylesjo M, Eriksson D, Kusano M, Moritz T, Trygg J. Data integration in plant biology: the O2PLS method for combined modeling of transcript and metabolite data. Plant J. 2007;52(6):1181–91.
Coulon D, Faure L, Salmon M, Wattelet V, Bessoule JJ. Occurrence, biosynthesis and functions of N-acylphosphatidylethanolamines (NAPE): not just precursors of N-acylethanolamines (NAE). Biochimie. 2012;94(1):75–85.
Khan MS, Maden BE. Conformation of methylated sequences in HeLa cell 18-S ribosomal RNA: nuclease S1 as a probe. Eur J Biochem. 1978;84(1):241–50.
Funk C, Brodelius PE. Phenylpropanoid Metabolism in Suspension Cultures of Vanilla planifolia Andr. : III. Conversion of 4-Methoxycinnamic Acids into 4-Hydroxybenzoic Acids. Plant Physiol. 1990;94(1):102–8.
Murkovic M, Pichler N. Analysis of 5-hydroxymethylfurfual in coffee, dried fruits and urine. Mol Nutr Food Res. 2006;50(9):842–6.
Hasegawa S, Smolensk D. Date Invertase - Properties and Activity Associated with Maturation and Quality. J Agr Food Chem. 1970;18(5):902.
Hussein F, Hussein MA. Effect of irrigation on growth, yield and fruit quality of dry dates grown at Asswan. In: Proceedings of the First Symposium on the Date Palm in Saudi Arabia: 1983; Al-Hassa, Saudi Arabia.
Al-Yahyai R, Al-Kharusi L. Sub-optimal irrigation affects chemical quality attributes of dates during fruit development. Afr J Agric Res. 2012;7(10):6.
Mathew LS, Seidel MA, George B, Mathew S, Spannagl M, Haberer G, et al. A Genome-Wide Survey of Date Palm Cultivars Supports Two Major Subpopulations in Phoenix dactylifera. G3. 2015;5(7):1429–38.
Kausch KD, Sobolev AP, Goyal RK, Fatima T, Laila-Beevi R, Saftner RA, et al. Methyl jasmonate deficiency alters cellular metabolome, including the aminome of tomato (Solanum lycopersicum L.) fruit. Amino Acids. 2012;42(2–3):843–56.
Teixeira PF, Glaser E. Processing peptidases in mitochondria and chloroplasts. Biochim Biophys Acta. 2013;1833(2):360–70.
Li L, Yuan H. Chromoplast biogenesis and carotenoid accumulation. Arch Biochem Biophys. 2013;539(2):102–9.
Bischof S, Baerenfaller K, Wildhaber T, Troesch R, Vidi PA, Roschitzki B, et al. Plastid proteome assembly without Toc159: photosynthetic protein import and accumulation of N-acetylated plastid precursor proteins. Plant Cell. 2011;23(11):3911–28.
Resende ECO, Fabiane Martins P, Antunes De Azevedo R, Jacomino AP, Urbano Bron I. Oxidative processes during ‘Golden’ papaya fruit ripening. Brazilian Soc Plant Physiol. 2012;24(2):9.
Gallego PP, Whotton L, Picton S, Grierson D, Gray JE. A role for glutamate decarboxylase during tomato ripening: the characterisation of a cDNA encoding a putative glutamate decarboxylase with a calmodulin-binding site. Plant Mol Biol. 1995;27(6):1143–51.
Tieman D, Taylor M, Schauer N, Fernie AR, Hanson AD, Klee HJ. Tomato aromatic amino acid decarboxylases participate in synthesis of the flavor volatiles 2-phenylethanol and 2-phenylacetaldehyde. Proc Natl Acad Sci U S A. 2006;103(21):8287–92.
Al-daihan S, Shafi Bhat R. Antibacterial activities of extracts of leaf, fruit, seed and bark of Phoenix Dactylifera. Afr J Biotechnol. 2012;11(42):10021–5.
Sun Q, Zhang N, Wang J, Zhang H, Li D, Shi J, et al. Melatonin promotes ripening and improves quality of tomato fruit during postharvest life. J Exp Bot. 2015;66(3):657–68.
Snowden CJ, Thomas B, Baxter CJ, Smith JA, Sweetlove LJ. A tonoplast Glu/Asp/GABA exchanger that affects tomato fruit amino acid composition. Plant J. 2015;81(5):651–60.
Pandey R, Gupta A, Chowdhary A, Pal RK, Rajam MV. Over-expression of mouse ornithine decarboxylase gene under the control of fruit-specific promoter enhances fruit quality in tomato. Plant Mol Biol. 2015;87(3):249–60.
Sobolev AP, Neelam A, Fatima T, Shukla V, Handa AK, Mattoo AK. Genetic introgression of ethylene-suppressed transgenic tomatoes with higher-polyamines trait overcomes many unintended effects due to reduced ethylene on the primary rnetabolome. Front Plant Sci. 2014;5:632.
Amira E, Behija SE, Beligh M, Lamia L, Manel I, Mohamed H, et al. Effects of the Ripening Stage on Phenolic Profile, Phytochemical Composition and Antioxidant Activity of Date Palm Fruit. J Agr Food Chem. 2012;60(44):10896–902.
Joslyn MA, Goldstein JL. Astringency of Fruits and Fruit Products in Relation to Phenolic Content. Adv Food Res. 1964;13:179–217.
Wade NL, Bishop DG. Changes in the lipid composition of ripening banana fruits and evidence for an associated increase in cell membrane permeability. Biochim Biophys Acta. 1978;529(3):454–60.
Lurie S, Ben-Arie R. Microsomal Membrane Changes during the Ripening of Apple Fruit. Plant Physiol. 1983;73(3):636–8.
Rouet-Mayer MA, Valentova O, Simond-Cote E, Daussant J, Thevenot C. Critical analysis of phospholipid hydrolyzing activities in ripening tomato fruits. Study by spectrofluorimetry and high-performance liquid chromatography. Lipids. 1995;30(8):739–46.
Zhang B, Shen JY, Wei WW, Xi WP, Xu CJ, Ferguson I, et al. Expression of genes associated with aroma formation derived from the fatty acid pathway during peach fruit ripening. J Agric Food Chem. 2010;58(10):6157–65.
Whitaker BD, Smith DL, Green KC. Cloning, characterization and functional expression of a phospholipase Dalpha cDNA from tomato fruit. Physiol Plant. 2001;112(1):87–94.
Wang X. The role of phospholipase D in signaling cascades. Plant Physiol. 1999;120(3):645–52.
Okazaki Y, Saito K. Roles of lipids as signaling molecules and mitigators during stress response in plants. Plant J. 2014;79(4):584–96.
Zhang W, QIN C, Ahao J, Wang X. Phospholipase D alpha1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signalling. Proc Natl Acad Sci. 2004;101:5.
Marondedze C, Gehring C, Thomas L. Dynamic changes in the date palm fruit proteome during development and ripening. Hortic Res. 2014;1(1):14039.
Wirtz M, Hell R. Functional analysis of the cysteine synthase protein complex from plants: structural, biochemical and regulatory properties. J Plant Physiol. 2006;163(3):273–86.
Abbas MF, Ibrahim MA. The role of ethylene in the regulation of fruit ripening in the hillawi date palm (Phoenix dactylifera L). J Sci Food Agr. 1996;72(3):306–8.
Desai N, Chism GW. Changes in Cytokinin Activity in Ripening Tomato Fruit. J Food Sci. 1978;43(4):1324–6.
Wu J, Xu Z, Zhang Y, Chai L, Yi H, Deng X. An integrative analysis of the transcriptome and proteome of the pulp of a spontaneous late-ripening sweet orange mutant and its wild type improves our understanding of fruit ripening in citrus. J Exp Bot. 2014;65(6):1651–71.
Sun L, Sun Y, Zhang M, Wang L, Ren J, Cui M, et al. Suppression of 9-cis-epoxycarotenoid dioxygenase, which encodes a key enzyme in abscisic acid biosynthesis, alters fruit texture in transgenic tomato. Plant Physiol. 2012;158(1):283–98.
Leng P, Yuan B, Guo Y. The role of abscisic acid in fruit ripening and responses to abiotic stress. J Exp Bot. 2014;65(16):4577–88.