doi: 10.15389/agrobiology.2017.1.37eng

UDC 633.491:577.127:547.973:577.21

Supported by Russian Science Foundation (grant № 16-16-04073).



K.V. Strygina1, E.K. Khlestkina1, 2

1Federal Research Center Institute of Cytology and Genetics SB RAS, Federal Agency of Scientific Organizations, 10, prosp. Akademika Lavrent’eva, Novosibirsk, 630090 Russia, e-mail;
2Novosibirsk State University, 2, ul. Pirogova, Novosibirsk, 630090 Russia

Khlestkina E.K.

Received November 5, 2016


Potato may have anthocyanin-colored tuber skin, tuber flesh, flowers, leaves, stems and eyes. Anthocyanins protect photosynthetic apparatus of plant cell, scavenge free radicals under stress conditions, increase efficiency of phosphorus and nitrogen uptake, possess osmoregulatory function, antimicrobial activity and have a number of other useful properties. Anthocyanins are also known for their health benefit: diabetes type II and cardiovascular diseases protection, anti-inflammatory effect, etc. Thus, anthocyanins are important for adaptation of plants to unfavorable environment conditions as well as for nutritional value when they are taken with food. Since potato Solanum tuberosum L. is one of the main crop species, possibility to increase anthocyanin content in tuber flesh is important. Anthocyanin concentration in pigmented tuber flesh is similar to that in blueberries, blackberries, cranberries and red grapes. It is important that cooking as well as long storage of potato tubers doesn’t affect anthocyanin content. Coloration traits (red or purple tuber flesh) are included in ongoing breeding programs. Therefore, development of tools (convenient diagnostic PCR-markers for anthocyanin biosynthesis genes) for accelerated and efficient selection is of importance. The goal of the current review is to summarize information on the genes regulating anthocyanin biosynthesis in potato and assess possibility of development of diagnostic marker for prediction of tuber flesh color before tuber formation. Anthocyanin biosynthesis takes place in cytosol with the help of enzymes CHS, CHI, DFR, F3H, F3'H, F3'5'H and ANS, after that anthocyanins are transported to vacuoles. Activation of biosynthesis is controlled by MBW complex consisting of transcription factors MYB, bHLH and WD40. This complex activates transcription of structural genes encoding the enzymes mentioned above. A number of MYB-encoding genes are identified in potato, among them StAN1 related with anthocyanin biosynthesis. This gene corresponds to the D locus previously revealed with genetic dissection approach and mapped to chromosome 10. The genes encoding bHLH (StJAF13 and StbHLH1) and WD40 (StWD40) have been revealed only by their homology with similar genes of other plant species, but not by genetic dissection, probably because they have no allelic diversity. Thus, the main gene determining high variability of potato by the coloration traits is StAN1. Its allelic variants are described and shown to be related with anthocyanin synthesis efficiency. The StAN1 alleles can be easily distinguished by PCR fragments lengths, what allows constructing convenient diagnostic markers for selection. In some cases, the lack of anthocyanins is due to mutation of a structural gene. This was described in the literature for the R locus encoding DFR enzyme. Mutation of other structural gene, StF3'5'H (locus P), just partially disrupts anthocyanin synthesis, not effecting red pigments, but blue and purple only. This makes the StF3'5'H an attractive target for marker-assisted identification of genotypes with different tuber flesh color — purple or red. Thus, there are two main targets for breeding anthocyanin-colored potato — StAN1 and StF3'5'H.

Keywords: Solanum tuberosum, potato, marker-assisted selection, anthocyanins, stress tolerance, nutrition value, genes, diagnostic markers.


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  1. Metodicheskie ukazaniya po podderzhaniyu i izucheniyu mirovoi kollektsii kartofelya /Pod redaktsiei S.D. Kiru [Potato world collection: recommendations on specimen maintenance and preservation. S.D. Kiru (ed.)]. St. Petersburg, 2010 (in Russ.).
  2. Chalker-Scott L. Environmental significance of anthocyanins in plant stress responses. Photochem. Photobiol., 1999, 70(1): 1-9 CrossRef
  3. Gould K.S. Nature's Swiss army knife: the diverse protective roles of anthocyanins in leaves. BioMed Research International, 2004, 2004(5): 314-320 CrossRef
  4. Hale K.L., Tufan H. A., Pickering I.J., George G.N., Terry N., Pilon M., Pilon-Smits E.A. Anthocyanins facilitate tungsten accumulation in Brassica. Physiologia Plantarum, 2002, 116(3): 351-358 CrossRef
  5. Khlestkina E. The adaptive role of flavonoids: emphasis on cereals. Cereal Res. Commun., 2013, 41(2): 185-198 CrossRef
  6. Cisowska A., Wojnicz D., Hendrich A.B. Anthocyanins as antimicrobial agents of natural plant origin. Nat. Prod. Commun., 2011, 6(1): 149-156.
  7. Wen H., Kang J., Li D., Wen W., Yang F., Hu H., Liu C. Antifungal activities of anthocyanins from purple sweet potato in the presence of food preservatives. Food Sci. Biotechnol., 2016, 25(1): 165-171 CrossRef
  8. Wegener C.B., Jansen G. Soft-rot resistance of coloured potato cultivars (Solanum tuberosum L.): the role of anthocyanins. Potato Res., 2007, 50(1): 31-44 CrossRef
  9. Beckman C.H. Phenolic-storing cells: keys to programmed cell death and periderm formation in wilt disease resistance and in general defense responses in plants. Physiological and Molecular Plant Pathology, 2000, 57(3): 101-110 CrossRef
  10. Cassidy A., O'Reilly É.J., Kay C., Sampson L., Franz M., Forman J.P., Curhan G., Rimm E.B. Habitual intake of flavonoid subclasses and incident hypertension in adults. Am. J. Clin. Nutr., 2011, 93(2): 338-347 CrossRef
  11. Howard B.V., Kritchevsky D., Nutrition Committee. Phytochemicals and cardiovascular disease a statement for healthcare professionals from the American heart association. Circulation, 1997, 95(11): 2591-2593 CrossRef
  12. Hui C., Bi Y., Xiaopin Y., Lon Y., Chunye C., Mantian M., Wenhua L. Anticancer activities of an anthocyanin-rich extract from black rice against breast cancer cells in vitro and in vivo. Nutrition and Cancer, 2010, 62(8): 1128-1136 CrossRef
  13. Sancho R.A.S., Pastore G.M. Evaluation of the effects of anthocyanins in type 2 diabetes. Food Res. Int., 2012, 46(1): 378-386.
  14. Lila M.A. Anthocyanins and human health: an in vitro investigative approach. BioMed Research International, 2004, 2004(5): 306-313 CrossRef
  15. Wang H., Nair M.G., Strasburg G.M., Chang Y.C., Booren A.M., Gray J.I., DeWitt D.L. Antioxidant and antiinflammatory activities of anthocyanins and their aglycon, cyanidin, from tart cherries. J. Nat. Prod., 1999, 62(2): 294-296 CrossRef
  16. Williams R.J., Spencer J.P., Rice-Evans C. Flavonoids: antioxidants or signalling molecules? Free Radical Bio. Med., 2004, 36(7): 838-849 CrossRef
  17. Aggarwal B.B., Shishodia S. Molecular targets of dietary agents for prevention and therapy of cancer. Biochem. Pharmacol., 2006, 71(10): 1397-1421 CrossRef
  18. Virgili F., Marino M. Regulation of cellular signals from nutritional molecules: a specific role for phytochemicals, beyond antioxidant activity. Free Radical Bio. Med., 2008, 45(9): 1205-1216 CrossRef
  19. Tsuda T., Horio F., Uchida K., Aoki H., Osawa T. Dietary cyanidin 3-O-β-D-glucoside-rich purple corn color prevents obesity and ameliorates hyperglycemia in mice. J. Nutr., 2003, 133(7): 2125-2130.
  20. Shobana S., Sreerama Y.N., Malleshi N.G. Composition and enzyme inhibitory properties of finger millet (Eleusine coracana L.) seed coat phenolics: Mode of inhibition of a-glucosidase and pancreatic amylase. Food Chem., 2009, 115(4): 1268-1273 CrossRef
  21. Tadera K., Minami Y., Takamatsu K., Matsuoka T. Inhibition of α-glucosidase and a-amylase by flavonoids. J. Nutr. Sci. Vitaminol., 2006, 52(2): 149-153 CrossRef
  22. Rodriguez-Saona L.E., Wrolstad R.E., Pereira C. Glycoalkaloid content and anthocyanin stability to alkaline treatment of red-fleshed potato extracts. J. Food Sci., 1999, 64(3): 445-450 CrossRef
  23. Fossen T., Andersen Ø.M. Anthocyanins from tubers and shoots of the purple potato, Solanum tuberosum. The Journal of Horticultural Science and Biotechnology, 2000, 75(3): 360-363 CrossRef
  24. Eichhorn S., Winterhalter P. Anthocyanins from pigmented potato (Solanum tuberosum L.) varieties. Food Res. Int., 2005, 38(8): 943-948 CrossRef
  25. Andre C.M., Oufir M., Guignard C., Hoffmann L., Hausman J.F., Evers D., Larondelle Y. 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., 2007, 55(26): 10839-10849 CrossRef
  26. Kalita D., Jayanty S.S. Comparison of polyphenol content and antioxidant capacity of colored potato tubers, pomegranate and blueberries. Journal of Food Processing and Technology, 2014, 5: 358 CrossRef
  27. Lewis C.E., Walker J.R., Lancaster J.E., Sutton K.H. Determination of anthocyanins, flavonoids and phenolic acids in potatoes. I: Coloured cultivars of Solanum tuberosum L. J. Sci. Food Agr., 1998, 77(1): 45-57 CrossRef.
  28. Schieber A., Saldana M.A. Potato peels: a source of nutritionally and pharmacologically interesting compounds — a review. Food, 2009, 3(2): 23-29.
  29. Mulinacci N., Ieri F., Giaccherini C., Innocenti M., Andrenelli L., Canova G., Saracchi M., Casiraghi M.C. Effect of cooking on the anthocyanins, phenolic acids, glycoalkaloids, and resistant starch content in two pigmented cultivars of Solanum tuberosum L. J. Agr. Food Chem., 2008, 56(24): 11830-11837 CrosRef
  30. Lemos M.A., Aliyu M.M. Hungerford G. Influence of cooking on the levels of bioactive compounds in Purple Majesty potato observed via chemical and spectroscopic means. Food Chem., 2015, 173: 462-467 CrossRef
  31. Jansen G., Flamme W. Coloured potatoes (Solanum tuberosum L.) — anthocyanin content and tuber quality. Genet. Resour. Crop Ev., 2006, 53(7): 1321-1331 CrossRef
  32. Brown C.R., Wrolstad R., Durst R., Yang C.P., Clevidence B. Breeding studies in potatoes containing high concentrations of anthocyanins. Am. J. Potato Res., 2003, 80(4): 241-249 CrossRef
  33. Brown C.R., Culley D., Yang C.P., Durst R., Wrolstad R. Variation of anthocyanin and carotenoid contents and associated antioxidant values in potato breeding lines. J. Am. Soc. Hortic. Sci., 2005, 130(2): 174-180.
  34. Khlestkina E.K., Shumnyi V.K., Kolchanov N.A. Dostizheniya nauki i tekhniki APK, 2016, 30(10): 5-8 (in Russ.).
  35. Koes R., Verweij W., Quattrocchio F. Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci., 2005, 10(5): 236-242 CrossRef
  36. Grotewold E. Plant metabolic diversity: a regulatory perspective. Trends Plant Sci., 2005, 10(2): 57-62 CrossRef
  37. Cone K.C., Burr F.A., Burr B. Molecular analysis of the maize anthocyanin regulatory locus C1. PNAS, 1986, 83(24): 9631-9635.
  38. Ludwig S.R., Habera L.F., Dellaporta S.L., Wessler S.R. Lc, a member of the maize R gene family responsible for tissue-specific anthocyanin production, encodes a protein similar to transcriptional activators and contains the myc-homology region. PNAS, 1989, 86(18): 7092-7096.
  39. Quattrocchio F., Wing J.F., Va K., Mol J.N., Koes R. Analysis of bHLH and MYB domain proteins: species-specific regulatory differences are caused by divergent evolution of target anthocyanin genes. Plant J., 1998, 13(4): 475-488 CrossRef
  40. Dodds K., Long D.H. The inheritance of colour in diploid potatoes. J. Genet., 1955, 53(1): 136-149 CrossRef
  41. van Eck H.J., Jacobs J.M., van Dijk J., Stiekema W.J., Jacobsen E. Identification and mapping of three flower colour loci of potato (S. tuberosum L.) by RFLP analysis. Theor. Appl. Genet., 1993, 86(2-3): 295-300 CrossRef
  42. van Eck H.J., Jacobs J.M., van den Berg P.M., Stiekema W.J., Jacobsen E. The inheritance of anthocyanin pigmentation in potato (Solanum tuberosum L.) and mapping of tuber skin colour loci using RFLPs. Heredity, 1994, 73: 410-421 CrossRef
  43. Gebhardt C., Ritter E., Debener T., Schachtschabel U., Walkemeier B., Uhrig H., Salamini F. RFLP analysis and linkage mapping in Solanum tuberosum. Theor. Appl. Genet., 1989, 78(1): 65-75 CrossRef
  44. Jacobs J.M.E., van Eck H.J., Arens P., Verkerk-Bakker B., te Lintel Hekkert B., Bastiaanssen H.J.M., El-Kharbotly A., Pereira A., Jacobsen E.,  Stiekema W.J. A genetic map of potato (Solanum tuberosum) integrating molecular markers, including transposons, and classical markers. Theor. Appl. Genet., 1995, 91(2): 289-300 CrossRef
  45. Jung C.S., Griffiths H.M., De Jong D.M., Cheng S., Bodis M., De Jong W.S. The potato P locus codes for flavonoid 3',5'-hydroxylase. Theor. Appl. Genet., 2005, 110(2): 269-275 CrossRef
  46. Zhang Y., Cheng S., De Jong D., Griffiths H., Halitschke R., De Jong W. The potato R locus codes for dihydroflavonol 4-reductase. Theor. Appl. Genet., 2009, 119(5): 931-937 CrossRef
  47. De Jong W.S., Eannetta N.T., De Jong D.M., Bodis M. Candidate gene analysis of anthocyanin pigmentation loci in the Solanaceae. Theor. Appl. Genet., 2004, 108(3): 423-432 CrossRef
  48. De Jong W.S., De Jong D.M., De Jong H., Kalazich J., Bodis M. An allele of dihydroflavonol 4-reductase associated with the ability to produce red anthocyanin pigments in potato (Solanum tuberosum L.). Theor. Appl. Genet., 2003, 107(8): 1375-1383 CrossRef
  49. Zhang Y., Jung C.S., De Jong W.S. Genetic analysis of pigmented tuber flesh in potato. Theor. Appl. Genet., 2009, 119(1): 143-150 CrossRef
  50. Spelt C., Quattrocchio F., Mol J.N., Koes R. anthocyanin1 of petunia encodes a basic helix-loop-helix protein that directly activates transcription of structural anthocyanin genes. Plant Cell, 2000, 12(9): 1619-1631 CrossRef
  51. Grotewold E. The genetics and biochemistry of floral pigments. Annu. Rev. Plant Biol., 2006, 57: 761-780 CrossRef
  52. De Jong H. Inheritance of anthocyanin pigmentation in the cultivated potato: a critical review. Am. Potato J., 1991, 68(9): 585-593 CrossRef
  53. Stushnoff C., Ducreux L. J., Hancock R.D., Hedley P.E., Holm D.G., McDougall G.J., McNicol J.W., Morris J., Morris W.L., Sungurtas J.A., Verrall S.R., Zuber T., Taylor M.A. Flavonoid profiling and transcriptome analysis reveals new gene—metabolite correlations in tubers of Solanum tuberosum L. J. Exp. Bot., 2010, 61 (4): 1225-1238 CrossRef
  54. Feller A., Machemer K., Braun E.L., Grotewold E. Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J., 2011, 66(1): 94-116 CrossRef
  55. Dubos C., Stracke R., Grotewold E., Weisshaar B., Martin C., Lepiniec L. MYB transcription factors in Arabidopsis. Trends Plant Sci., 2010, 15(10): 573-581 CrossRef
  56. Allan A.C., Hellens R.P., Laing W.A. MYB transcription factors that colour our fruit. Trends Plant Sci., 2008, 13(3): 99-102 CrossRef
  57. Jung C.S., Griffiths H.M., De Jong D.M., Cheng S., Bodis M., Kim T.S., De Jong W.S. The potato developer (D) locus encodes an R2R3 MYB transcription factor that regulates expression of multiple anthocyanin structural genes in tuber skin. Theor. Appl. Genet., 2009, 120(1): 45-57 CrossRef
  58. Payyavula R.S., Singh R.K., Navarre D.A. Transcription factors, sucrose, and sucrose metabolic genes interact to regulate potato phenylpropanoid metabolism. J. Exp. Bot., 2013, 64(16): 5115-5131 CrossRef
  59. D'Amelia V., Aversano R., Batelli G., Caruso I., Castellano Moreno M., Castro-Sanz A.B., Chiaiese P., Fasano C., Palomba F., Carputo D. High AN1 variability and interaction with basic helix-loop-helix co-factors related to anthocyanin biosynthesis in potato leaves. Plant J., 2014, 80(3): 527-540 CrossRef
  60. Tai H.H., Goyer C., Murphy A.M. Potato MYB and bHLH transcription factors associated with anthocyanin intensity and common scab resistance. Botany, 2013, 91(10): 722-730 CrossRef
  61. Liu Y., Lin-Wang K., Espley R.V., Wang L., Yang H., Yu B., Dare A., Varkonyi-Gasic E., Wang J., Zhang J., Wang D., Allan A.C. Functional diversification of the potato R2R3 MYB anthocyanin activators AN1, MYBA1, and MYB113 and their interaction with basic helix-loop-helix cofactors. J. Exp. Bot., 2016, 67(8): 2159-2176 CrossRef
  62. Liu Y., Lin-Wang K., Deng C., Warran B., Wang L., Yu B., Yang H., Wang D., Espley R.V., Zhang J., Wang D., Allan A.C. Comparative transcriptome analysis of white and purple potato to identify genes involved in anthocyanin biosynthesis. PloS ONE, 2015, 10(6): e0129148 CrossRef
  63. André C.M., Schafleitner R., Legay S., Lefèvre I., Aliaga C.A.A., Nomberto G., Hoffmanna L., Hausmana J., Larondelleb Y., Evers D. Gene expression changes related to the production of phenolic compounds in potato tubers grown under drought stress. Phytochemistry, 2009, 70(9): 1107-1116 CrossRef
  64. Koch K.E. Carbohydrate-modulated gene expression in plants. Annu. Rev. Plant Biol., 1996, 47(1): 509-540 CrossRef
  65. Teng S., Keurentjes J., Bentsink L., Koornneef M., Smeekens S. Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene. Plant Physiol., 2005, 139(4): 1840-1852 CrossRef
  66. Solfanelli C., Poggi A., Loreti E., Alpi A., Perata P. Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol., 2006, 140(2): 637-646 CrossRef
  67. Kobayashi S., Goto-Yamamoto N., Hirochika H. Retrotransposon-induced mutations in grape skin color. Science, 2004, 304(5673): 982-982 CrossRef
  68. Walker A.R., Lee E., Bogs J., McDavid D.A., Thomas M.R., Robinson S.P. White grapes arose through the mutation of two similar and adjacent regulatory genes. Plant J., 2007, 49(5): 772-785 CrossRef
  69. Telias A., Lin-Wang K., Stevenson D.E., Cooney J.M., Hellens R.P., Allan A.C., Hoover E.E., Bradeen J.M. Apple skin patterning is associated with differential expression of MYB10. BMC Plant Biol., 2011, 11: 93 CrossRef
  70. Butelli E., Licciardello C., Zhang Y., Liu J., Mackay S., Bailey P., Reforgiato-Recupero G., Martin C. Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell, 2012, 24(3): 1242-1255 CrossRef
  71. Lisch D. How important are transposons for plant evolution? Nat. Rev. Genet., 2013, 14(1): 49-61 CrossRef
  72. Borevitz J.O., Xia Y., Blount J., Dixon R.A., Lamb C. Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell, 2000, 12(12): 2383-2393 CrossRef
  73. Gordeeva E.I., Shoeva O.Y., Khlestkina E.K. Marker-assisted development of bread wheat near-isogenic lines carrying various combinations of purple pericarp (Pp) alleles. Euphytica, 2015, 203(2): 469-476 CrossRef
  74. Pattanaik S., Kong Q., Zaitlin D., Werkman J.R., Xie C.H., Patra B., Yuan L. Isolation and functional characterization of a floral tissue-specific R2R3 MYB regulator from tobacco. Planta, 2010, 231(5): 1061-1076 CrossRef
  75. Neer E.J., Schmidt C.J., Nambudripad R., Smith T.F. The ancient regulatory-protein family of WD-repeat proteins. Nature, 1994, 371(6495): 297-300 CrossRef
  76. Khlestkina E.K., Shumnyi V.K. Genetika, 2016, 52(7): 774-787 CrossRef (in Russ.).