Advertisement

Planta

, Volume 246, Issue 2, pp 281–297 | Cite as

Metabolite profiling of red and blue potatoes revealed cultivar and tissue specific patterns for anthocyanins and other polyphenols

  • Anne Oertel
  • Andrea Matros
  • Anja Hartmann
  • Panagiotis Arapitsas
  • Klaus J. Dehmer
  • Stefan Martens
  • Hans-Peter MockEmail author
Original Article
Part of the following topical collections:
  1. Focus on polyphenols II

Abstract

Main conclusion

Metabolite profiling of tuber flesh and peel for selected colored potato varieties revealed cultivar and tissue specific profiles of anthocyanins and other polyphenols with variations in composition and concentration.

Starchy tubers of Solanum tuberosum are a staple crop and food in many countries. Among cultivated potato varieties a huge biodiversity exists, including an increasing number of red and purple colored cultivars. This coloration relates to the accumulation of anthocyanins and is supposed to offer nutritional benefits possibly associated with the antioxidative capacity of anthocyanins. However, the anthocyanin composition and its relation to the overall polyphenol constitution in colored potato tubers have not been investigated closely. This study focuses on the phytochemical characterization of the phenolic composition of a variety of colored potato tubers, both for peel and flesh tissues. First, liquid chromatography (LC) separation coupled to UV and mass spectrometry (MS) detection of polyphenolic compounds of potato tubers from 57 cultivars was used to assign groups of potato cultivars differing in their anthocyanin and polyphenol profiles. Tissues from 19 selected cultivars were then analyzed by LC separation coupled to multiple reaction monitoring (MRM) to detect quantitative differences in anthocyanin and polyphenol composition. The measured intensities of 21 anthocyanins present in the analyzed potato cultivars and tissues could be correlated with the specific tuber coloration. Besides secondary metabolites well-known for potato tubers, the metabolic profiling led to the detection of two anthocyanins not described for potato tuber previously, which we tentatively annotated as pelargonidin feruloyl-xylosyl-glucosyl-galactoside and cyanidin 3-p-coumaroylrutinoside-5-glucoside. We detected significant correlations between some of the measured metabolites, as for example the negative correlation between the main anthocyanins of red and blue potato cultivars. Mainly hydroxylation and methylation patterns of the B-ring of dihydroflavonols, leading to the formation of specific anthocyanidin backbones, can be assigned to a distinct coloring of the potato cultivars and tuber tissues. However, basically the same glycosylation and acylation reactions occur regardless of the main anthocyanidin precursor present in the respective red and blue/purple tissue. Thus, the different anthocyanin profiles in red and blue potato cultivars likely relate to superior regulation of the expression and activities of hydroxylases and methyltransferases rather than to differences for downstream glycosyl- and acyltransferases. In this regard, the characterized potato cultivars represent a valuable resource for the molecular analysis of the genetic background and the regulation of anthocyanin side chain modification.

Keywords

Colored potatoes Flavonoids LC–MS/MRM Metabolomics Solanum tuberosum

Abbreviations

ESI

Electrospray ionization

MRM

Multiple reaction monitoring

PCA

Principal component analysis

PDA

Photodiode array

TQMS

Triple quadrupole mass spectrometry

UHR-TOF-MS

Ultra-high resolution time-of-flight mass spectrometry

UPLC

Ultra-performance liquid chromatography

Notes

Acknowledgements

This research has been financially supported by the ERA-IB ANTHOPLUS project (031A336A0) and by the COST Action “The quest for tolerant varieties—Phenotyping at plant and cellular level” (FA1306).

Supplementary material

425_2017_2718_MOESM1_ESM.pptx (739 kb)
Supplemental Fig. 1 a-g 24 anthocyanin profile groups, six profiles found in tuber flesh (Group 1-6 F, a and b) and 18 profiles found in tuber peel (Group 1-18 P, b to f). Bar charts (left) show the peak area of up to 23 tentatively annotated anthocyanins (g), averaged within each group. Red and blue columns represent the dominating colors of the appropriate tissues. Anthocyanins mainly contributing to the group variance are blue-rimmed. Tables (right) comprise all varieties/tissues assorted to the appropriate group. *Cultivars with highest abundance in main anthocyanins of respective tissues, and therefore selected as group representative samples for MRM analysis. a-gReferences used for compound annotation included: (Goto et al. (1982); Takeda et al. (1988); Naito et al. (1998); Hillebrand et al. (2009); Zhang et al. (2009); Kim et al. (2012)); http://www.genome.jp/dbget-bin/www_bget?pathway+sot00942 (PPTX 738 kb)
425_2017_2718_MOESM2_ESM.pptx (2.3 mb)
Supplemental Fig. 2 19 colored potato genotypes with different anthocyanin profiles in tuber flesh/peel selected via LC-UV/MS profile analysis (PPTX 2315 kb)
425_2017_2718_MOESM3_ESM.pptx (1 mb)
Supplemental Fig. 3 a-d Pearson correlation analysis results representing correlation coefficient |r|-values and significance P values in categories *** P < 0.001, ** P < 0.01, * P < 0.05, . P < 0.1, as well as scatter plots (regression line (red), data point tissue wise separated (yellow = flesh, orange = peel)) for the correlation between all anthocyanins (A1 to A21) and additional polyphenolic compounds (P1 to P31) (a, b), within the group of anthocyanins (c), and within the other polyphenols (d) detected in potato tuber tissues via LC–MS/MRM. Abbreviations of compounds are displayed according to Table 2 and 3, respectively (PPTX 1055 kb)
425_2017_2718_MOESM4_ESM.docx (24 kb)
Supplemental Table 1 Colored potato genotypes analyzed by LC-UV/MS for initial anthocyanin profiling (DOCX 24 kb)

References

  1. Algarra M, Fernandes A, Mateus N, de Freitas V, da Silva JCE, Casado J (2014) Anthocyanin profile and antioxidant capacity of black carrots (Daucus carota L. ssp. sativus var. atrorubens Alef.) from Cuevas Bajas, Spain. J Food Compos Anal 33(1):71–76CrossRefGoogle Scholar
  2. Ampomah YA, Friend J (1988) Insoluble phenolic compounds and resistance of potato tuber disc to Phytophthora and Phoma. Phytochemistry 27(8):2533–2541CrossRefGoogle Scholar
  3. Andersen ØM, Opheim S, Aksnes DW, Frøystein NÅ (1991) Structure of petanin, an acylated anthocyanin isolated from Solanum tuberosum, using homo-and hetero-nuclear two-dimensional nuclear magnetic resonance techniques. Phytochem Anal 2(5):230–236CrossRefGoogle Scholar
  4. Andre CM, Oufir M, Guignard C, Hoffmann L, Hausman J-F, Evers D, Larondelle Y (2007) Antioxidant profiling of native Andean potato tubers (Solanum tuberosum L.) reveals cultivars with high levels of β-carotene, α-tocopherol, chlorogenic acid, and petanin. J Agr Food Chem 55(26):10839–10849CrossRefGoogle Scholar
  5. Bagchi D, Sen C, Bagchi M, Atalay M (2004) Anti-angiogenic, antioxidant, and anti-carcinogenic properties of a novel anthocyanin-rich berry extract formula. Biochemistry (Moscow) 69(1):75–80CrossRefGoogle Scholar
  6. Bridle P, Timberlake C (1997) Anthocyanins as natural food colours—selected aspects. Food Chem 58(1):103–109CrossRefGoogle Scholar
  7. Brown C (2006) Anthocyanin and carotenoid contents in potato: breeding for the specialty market. Proc Ida Winter Commod Sch 39:157–163Google Scholar
  8. Butelli E, Titta L, Giorgio M, Mock H-P, Matros A, Peterek S, Schijlen EG, Hall RD, Bovy AG, Luo J (2008) Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nat Biotechnol 26(11):1301–1308PubMedCrossRefGoogle Scholar
  9. Castaneda-Ovando A, de Lourdes Pacheco-Hernández M, Páez-Hernández ME, Rodríguez JA, Galán-Vidal CA (2009) Chemical studies of anthocyanins: a review. Food Chem 113(4):859–871CrossRefGoogle Scholar
  10. Chalker-Scott L (1999) Environmental significance of anthocyanins in plant stress responses. Photochem Photobiol 70:1–9CrossRefGoogle Scholar
  11. Chen S-M, Coe E Jr (1977) Control of anthocyanin synthesis by the C locus in maize. Biochem Genet 15(3–4):333–346PubMedCrossRefGoogle Scholar
  12. De Jong W, De Jong D, De Jong H, Kalazich J, Bodis M (2003) An allele of dihydroflavonol 4-reductase associated with the ability to produce red anthocyanin pigments in potato (Solanum tuberosum L.). Theor Appl Genet 107(8):1375–1383PubMedCrossRefGoogle Scholar
  13. Eichhorn S, Winterhalter P (2005) Anthocyanins from pigmented potato (Solanum tuberosum L.) varieties. Food Res Int 38(8):943–948CrossRefGoogle Scholar
  14. Fournier-Level A, Hugueney P, Verriès C, This P, Ageorges A (2011) Genetic mechanisms underlying the methylation level of anthocyanins in grape (Vitis vinifera L.). BMC Plant Biol 11(1):179PubMedPubMedCentralCrossRefGoogle Scholar
  15. Friedman M (1997) Chemistry, biochemistry, and dietary role of potato polyphenols. A review. J Agr Food Chem 45(5):1523–1540CrossRefGoogle Scholar
  16. Gopu V, Kothandapani S, Shetty PH (2015) Quorum quenching activity of Syzygium cumini (L.) Skeels and its anthocyanin malvidin against Klebsiella pneumoniae. Microb Pathog 79:61–69PubMedCrossRefGoogle Scholar
  17. Goto T, Kondo T, Tamura H, Imagawa H, Iino A, Takeda K (1982) Structure of gentiodelphin, an acylated anthocyanin isolated from Gentiana makinoi, that is stable in dilute aqueous solution. Tetrahedron Lett 23(36):3695–3698CrossRefGoogle Scholar
  18. Harrison HF, Peterson JK, Snook ME, Bohac JR, Jackson DM (2003) Quantity and potential biological activity of caffeic acid in sweet potato [Ipomoea batatas (L.) Lam.] storage root periderm. J Agr Food Chem 51(10):2943–2948CrossRefGoogle Scholar
  19. He J, Giusti MM (2010) Anthocyanins: natural colorants with health-promoting properties. Annu Rev Food Sci Technol 1:163–187PubMedCrossRefGoogle Scholar
  20. Hillebrand S, Naumann H, Kitzinski N, Köhler N, Winterhalter P (2009) Isolation and characterization of anthocyanins from blue-fleshed potatoes (Solanum tuberosum L.). Food 3(1):96–101Google Scholar
  21. Innocenzi V, Arnone S, Lai A, Musmeci S, Gambino P (2004) Eliciting of resistance against potato tuber moth larvae in tubers of Solanum tuberosum (+) S. pinnatisectum hybrids. In: Meeting of the physiology section of the european association for potato research, vol 684, pp 135–142Google Scholar
  22. Janson CH (1983) Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science (Washington) 219(4581):187–189CrossRefGoogle Scholar
  23. Kammerer D, Carle R, Schieber A (2003) Detection of peonidin and pelargonidin glycosides in black carrots (Daucus carota ssp. sativus var. atrorubens Alef.) by high performance liquid chromatography/electrospray ionization mass spectrometry. Rapid Commun Mass Spectrom 17(21):2407–2412PubMedCrossRefGoogle Scholar
  24. Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M (2015) KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res. doi: 10.1093/nar/gkv1070 PubMedPubMedCentralGoogle Scholar
  25. Kim HW, Kim JB, Cho SM, Chung MN, Lee YM, Chu SM, Che JH, Kim SN, Kim SY, Cho YS (2012) Anthocyanin changes in the Korean purple-fleshed sweet potato, Shinzami, as affected by steaming and baking. Food Chem 130(4):966–972CrossRefGoogle Scholar
  26. Kiple KF, Ornelas KC (2000) The Cambridge world history of food, vol 1. Cambridge University Press, Cambridge, pp 2000–2153Google Scholar
  27. Kovinich N, Kayanja G, Chanoca A, Riedl K, Otegui MS, Grotewold E (2014) Not all anthocyanins are born equal: distinct patterns induced by stress in Arabidopsis. Planta 240(5):931–940PubMedPubMedCentralCrossRefGoogle Scholar
  28. Lachman J, Hamouz K (2005) Red and purple coloured potatoes as a significant antioxidant source in human nutrition-a review. Plant Soil Environ 51(11):477Google Scholar
  29. Lewis CE, Walker JR, Lancaster JE, Sutton KH (1998) Determination of anthocyanins, flavonoids and phenolic acids in potatoes. I: Coloured cultivars of Solanum tuberosum L. J Sci Food Agr 77(1):45–57CrossRefGoogle Scholar
  30. Liakopoulos G, Nikolopoulos D, Klouvatou A, Vekkos K-A, Manetas Y, Karabourniotis G (2006) The photoprotective role of epidermal anthocyanins and surface pubescence in young leaves of grapevine (Vitis vinifera). Ann Bot-London 98(1):257–265CrossRefGoogle Scholar
  31. Lila MA (2004) Anthocyanins and human health: an in vitro investigative approach. Biomed Res Int 2004(5):306–313Google Scholar
  32. Lopez-Lazaro M (2009) Distribution and biological activities of the flavonoid luteolin. Mini reviews in Med Chem 9(1):31–59CrossRefGoogle Scholar
  33. Mano H, Ogasawara F, Sato K, Higo H, Minobe Y (2007) Isolation of a regulatory gene of anthocyanin biosynthesis in tuberous roots of purple-fleshed sweet potato. Plant Physiol 143(3):1252–1268PubMedPubMedCentralCrossRefGoogle Scholar
  34. Mateus N, de Pascual-Teresa S, Rivas-Gonzalo JC, Santos-Buelga C, de Freitas V (2002) Structural diversity of anthocyanin-derived pigments in port wines. Food Chem 76(3):335–342CrossRefGoogle Scholar
  35. Mazza G (2007) Anthocyanins and heart health. Ann Ist Super Sanità 43(4):369PubMedGoogle Scholar
  36. Mazzaracchio P, Pifferi P, Kindt M, Munyaneza A, Barbiroli G (2004) Interactions between anthocyanins and organic food molecules in model systems. Int J Food Sci Technol 39(1):53–59CrossRefGoogle Scholar
  37. Naito K, Umemura Y, Mori M, Sumida T, Okada T, Takamatsu N, Okawa Y, Hayashi K, Saito N, Honda T (1998) Acylated pelargonidin glycosides from a red potato. Phytochemistry 47(1):109–112CrossRefGoogle Scholar
  38. Nara K, Miyoshi T, Honma T, Koga H (2006) Antioxidative activity of bound-form phenolics in potato peel. Biosci Biotech Bioch 70(6):1489–1491CrossRefGoogle Scholar
  39. Navarre DA, Pillai SS, Shakya R, Holden MJ (2011) HPLC profiling of phenolics in diverse potato genotypes. Food Chem 127(1):34–41CrossRefGoogle Scholar
  40. Ohgami K, Ilieva I, Shiratori K, Koyama Y, Jin X-H, Yoshida K, Kase S, Kitaichi N, Suzuki Y, Tanaka T (2005) Anti-inflammatory effects of aronia extract on rat endotoxin-induced uveitis. Invest Ophthalmol Vis Sci 46(1):275–281PubMedCrossRefGoogle Scholar
  41. Pattanaik S, Kong Q, Zaitlin D, Werkman JR, Xie CH, Patra B, Yuan L (2010) Isolation and functional characterization of a floral tissue-specific R2R3 MYB regulator from tobacco. Planta 231(5):1061–1076PubMedCrossRefGoogle Scholar
  42. Payyavula RS, Shakya R, Sengoda VG, Munyaneza JE, Swamy P, Navarre DA (2015) Synthesis and regulation of chlorogenic acid in potato: rerouting phenylpropanoid flux in HQT-silenced lines. Plant Biotech J 13(4):551–564CrossRefGoogle Scholar
  43. Prior RL (2003) Fruits and vegetables in the prevention of cellular oxidative damage. Am J Clin Nutr 78(3):570S–578SPubMedGoogle Scholar
  44. Rodriguez-Saona LE, Giusti MM, Wrolstad RE (1998) Anthocyanin pigment composition of red-fleshed potatoes. J Food Sci 63(3):458–465CrossRefGoogle Scholar
  45. Rohn H, Junker A, Hartmann A, Grafahrend-Belau E, Treutler H, Klapperstück M, Czauderna T, Klukas C, Schreiber F (2012) VANTED v2: a framework for systems biology applications. BMC Syst Biol 6(1):1CrossRefGoogle Scholar
  46. Sachse J (1973) Anthocyane in den Kartoffelsorten Urgenta und Desirée (Solanum tuberosum L.). FOOD SCIENCE AND TECHNOLOGY-LEBENSMITTEL-WISSENSCHAFT & TECHNOLOGIE 153(5):294–300Google Scholar
  47. Smoliński A, Walczak B, Einax J (2002) Hierarchical clustering extended with visual complements of environmental data set. Chemometr Intell Lab 64(1):45–54CrossRefGoogle Scholar
  48. Spooner DM, McLean K, Ramsay G, Waugh R, Bryan GJ (2005) A single domestication for potato based on multilocus amplified fragment length polymorphism genotyping. P Natl Acad Sci USA 102(41):14694–14699CrossRefGoogle Scholar
  49. Steyn W, Wand S, Holcroft D, Jacobs G (2002) Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytol 155(3):349–361CrossRefGoogle Scholar
  50. Stushnoff C, Ducreux LJ, Hancock RD, Hedley PE, Holm DG, McDougall GJ, McNicol JW, Morris J, Morris WL, Sungurtas JA (2010) Flavonoid profiling and transcriptome analysis reveals new gene–metabolite correlations in tubers of Solanum tuberosum L. J Exp Bot 61(4):1225–1238PubMedPubMedCentralCrossRefGoogle Scholar
  51. Takeda K, Kumegawa C, Harborne JB, Self R (1988) Pelargonidin 3-(6″-succinyl glucoside)-5-glucoside from pink Centaurea cyanus flowers. Phytochemistry 27(4):1228–1229CrossRefGoogle Scholar
  52. Team RC (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2015. http.www.R-project.orgGoogle Scholar
  53. Tsuda T (2016) Recent progress in anti-obesity and anti-diabetes effect of berries. Antioxidants 5(2):13PubMedCentralCrossRefGoogle Scholar
  54. Valiñas MA, Lanteri ML, ten Have A, Andreu AB (2015) Chlorogenic acid biosynthesis appears linked with suberin production in potato tuber (Solanum tuberosum). J Agr Food Chem 63(19):4902–4913CrossRefGoogle Scholar
  55. Vrhovsek U, Masuero D, Gasperotti M, Franceschi P, Caputi L, Viola R, Mattivi F (2012) A versatile targeted metabolomics method for the rapid quantification of multiple classes of phenolics in fruits and beverages. J Agr Food Chem 60(36):8831–8840CrossRefGoogle Scholar
  56. Wang H, Cao G, Prior RL (1997) Oxygen radical absorbing capacity of anthocyanins. J Agr Food Chem 45(2):304–309CrossRefGoogle Scholar
  57. Wang Q, Cao Y, Zhou L, Jiang C-Z, Feng Y, Wei S (2015) Effects of postharvest curing treatment on flesh colour and phenolic metabolism in fresh-cut potato products. Food Chem 169:246–254PubMedCrossRefGoogle Scholar
  58. Warnes G, Bolker B, Bonebakker L, Gentleman R, Liaw W, Lumley T (2015) Pachage “gplots”: various R programming tools for plotting data. R package version 3.0. 1. https://cran r-project org/web/packages/gplots/gplots pdfGoogle Scholar
  59. Wegener CB, Jansen G (2007) Soft-rot resistance of coloured potato cultivars (Solanum tuberosum L.): the role of anthocyanins. Potato Res 50(1):31–44CrossRefGoogle Scholar
  60. Willson MF, Whelan CJ (1990) The evolution of fruit color in fleshy-fruited plants. Am Nat 136(6):790–809CrossRefGoogle Scholar
  61. Xie S, Song C, Wang X, Liu M, Zhang Z, Xi Z (2015) Tissue-specific expression analysis of anthocyanin biosynthetic genes in white-and red-fleshed grape cultivars. Molecules 20(12):22767–22780PubMedCrossRefGoogle Scholar
  62. Zhang Y, Cheng S, De Jong D, Griffiths H, Halitschke R, De Jong W (2009) The potato R locus codes for dihydroflavonol 4-reductase. Theor Appl Genet 119(5):931–937PubMedPubMedCentralCrossRefGoogle Scholar
  63. Zubko MK, Schmeer K, Gläßgen WE, Bayer E, Seitz HU (1993) Selection of anthocyanin-accumulating potato (Solanum tuberosum L.) cell lines from calli derived from seedlings produced by gamma-irradiated seeds. Plant Cell Rep 12(10):555–558PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Anne Oertel
    • 1
    • 2
  • Andrea Matros
    • 2
  • Anja Hartmann
    • 2
  • Panagiotis Arapitsas
    • 4
  • Klaus J. Dehmer
    • 3
  • Stefan Martens
    • 1
    • 4
  • Hans-Peter Mock
    • 2
    Email author
  1. 1.TRANSMIT GmbH, Project Division: PlantMetaChem (PMC)GiessenGermany
  2. 2.Department of Physiology and Cell BiologyLeibniz Institute of Plant Genetics and Crop Plant Research (IPK-Gatersleben)Stadt Seeland OT GaterslebenGermany
  3. 3.Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Genebank Department/GLKSGross LuesewitzGermany
  4. 4.Department of Food Quality and NutritionEdmund Mach Foundation, Research and Innovation CentreSan Michele all’Adige (TN)Italy

Personalised recommendations