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Planta

, Volume 230, Issue 5, pp 871–881 | Cite as

UDP-sugar biosynthetic pathway: contribution to cyanidin 3-galactoside biosynthesis in apple skin

  • Yusuke Ban
  • Satoru Kondo
  • Benjamin Ewa Ubi
  • Chikako Honda
  • Hideo Bessho
  • Takaya Moriguchi
Original Article

Abstract

UDP-galactose:flavonoid 3-O-galactosyltransferase (UFGalT) is responsible for cyanidin 3-galactoside (cy3-gal) synthesis from cyanidin (cy) and UDP-galactose (UDP-gal) which are, respectively, catalyzed by anthocyanidin synthase (ANS) and UDP-glucose 4-epimerase (UGE). To clarify the contribution of UDP-galactose pathway to cy3-gal accumulation in apple skin, we analyzed the contents of UDP-gal and UDP-glucose (UDP-glu), cy, and, cy3-gal contents along with UGE activity. We confirmed that transcript levels for apple ANS and UDP-glucose: flavonoid 3-O-glucosyltransferase (UFGT) coincided with anthocyanin accumulation in three apple cultivars differing in their skin colors. During fruit development, changes in level of cy coincided with that of cy3-gal, whereas UDP-gal and UGE activity showed no similar trend with cy3-gal. Significant correlation was not observed between the changes in UGE activity and UDP-sugar contents. The effect of temperature and UV-B radiation (different environmental conditions) on the accumulation of UDP-sugars, cy and cy3-gal, and UGE activity were also investigated in a pale-red cultivar. High temperature tended to depress the accumulation of both UDP-sugars and cy concomitant with the decrease in cy3-gal content irrespective of UV-B radiation. Although there was no high inhibition of both cy and UDP-sugars at low-temperature without UV-B, cy3-gal accumulation was highly depressed. UGE activity was highest at low temperature with UV-B, but not much different under other conditions. Most of the parameters under different environmental conditions were significantly correlated with each other. Based on these results, contribution of UDP-sugar biosynthetic pathway to anthocyanin biosynthesis under different environmental conditions as well as during fruit development is discussed.

Keywords

Anthocyanidin synthase (ANSAnthocyanin Apple (Malus × domestica) skin Cyanidin Cyanidin 3-galactoside UDP-galactose UDP-glucose UDP-glucose 4-epimerase (UGEUDP-glucose: flavonoid 3-O-glucosyltransferase (UFGT

Abbreviations

Cy

Cyanidin

Cy3-gal

Cyanidin 3-galactoside

DAFB

Days after full bloom

UDP-gal

UDP-galactose

UDP-glu

UDP-glucose

UV

Ultraviolet

References

  1. Alfenito MR, Souer E, Goodman CD, Buell R, Mol J, Koes R, Walbot V (1998) Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferase. Plant Cell 10:1135–1149PubMedCrossRefGoogle Scholar
  2. Ban Y, Honda C, Hatsuyama Y, Igarashi M, Bessho H, Moriguchi T (2007a) Isolation and functional analysis of a MYB transcription factor gene that is a key regulator for the development of red coloration in apple skin. Plant Cell Physiol 48:958–970PubMedCrossRefGoogle Scholar
  3. Ban Y, Honda C, Bessho H, Pang XM, Moriguchi T (2007b) Suppression subtractive hybridization identifies genes induced in response to UV-B radiation in apple skin: isolation of a putative UDP-glucose 4-epimerase. J Exp Bot 58:25–834CrossRefGoogle Scholar
  4. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  5. Brown AB, Cloix C, Jiang GH, Kaiserli E, Herzyk P, Kliebenstein DJ, Jenkins GI (2005) A UV-B-specific signaling component orchestrates plant UV protection. Proc Natl Acad Sci USA 102:18225–18230PubMedCrossRefGoogle Scholar
  6. Dong Y, Mitra D, Kootstra A (1995) Postharvest stimulation of skin color in Royal Gala apple. J Am Soc Hortic Sci 120:95–100Google Scholar
  7. Dörmann P, Benning C (1998) The role of UDP-glu epimerase in carbohydrate metabolism of Arabidopsis. Plant J 13:641–652PubMedCrossRefGoogle Scholar
  8. Goodman CD, Casati P, Walbot V (2004) A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell 16:1812–1826PubMedCrossRefGoogle Scholar
  9. Gyulakhmedov SG, Omarov YA, Mamedov ZM, Kuliev AA (2006) Isolation and study of active ATP-dependent phosphofructokinase from apple fruits Pyrus domestica Borkh. Appl Biochem Microbiol 42:534–538CrossRefGoogle Scholar
  10. Holland N, Menezes HC, Lafuente MT (2005) Carbohydrate metabolism as related to high-temperature conditioning and peel disorders occurring during storage of citrus fruit. J Sci Food Agri 53:8790–8796CrossRefGoogle Scholar
  11. Honda C, Kotoda N, Wada M, Kondo S, Kobayashi S, Soejima J, Zhang Z, Tsuda T, Moriguchi T (2002) Anthocyanin biosynthetic genes are coordinately expressed during red coloration in apple skin. Plant Physiol Biochem 40:955–962CrossRefGoogle Scholar
  12. Kitamura S, Shikazono N, Tanaka A (2004) TRANSPARENT TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. Plant J 37:104–114PubMedCrossRefGoogle Scholar
  13. Lancaster JE (1992) Regulation of skin color in apples. Crit Rev Plant Sci 10:487–502CrossRefGoogle Scholar
  14. Li Z, Sugaya S, Gemma H, Iwahori S (2002) Flavonoid biosynthesis and accumulation and related enzyme activities in the skin of ‘Fuji’ and ‘Oorin’ apples during their development. J Jpn Soc Hortic Sci 71:317–321CrossRefGoogle Scholar
  15. Lingle SE, Lester GE, Dunlap JR (1987) Effect of postharvest heat treatment and storage on sugar metabolism in polyethylene-wrapped muskmelon fruit. HortScience 22:917–919Google Scholar
  16. Marrs KA, Alfenito MR, Lloyd AM, Walbot V (1995) A glutathione S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature 375:397–400PubMedCrossRefGoogle Scholar
  17. Mori K, Goto-Yamamoto N, Kitayama M, Hashizume K (2007) Loss of anthocyanins in red-wine grape under high temperature. J Exp Bot 58:1935–1945PubMedCrossRefGoogle Scholar
  18. Moyrand F, Lafontaine I, Fontaine T, Janbon G (2008) UGE1 and UGE2 regulate the UDP-glucose/UDP-galactose equilibrium in Cryptococcus neoformans. Eukaryot Cell 7:2069–2077PubMedCrossRefGoogle Scholar
  19. Oomen RJFJ, Dao-Thi B, Tzitzikas EN, Bakx EJ, Schols HA, Visser RGF, Vincken J-P (2004) Overexpression of two different potato UDP-Glc 4-epimerases can increase the galactose content of potato tuber cell walls. Plant Sci 166:1097–1104CrossRefGoogle Scholar
  20. Rudell DR, Mattheis JP, Curry EA (2008) Prestorage ultraviolet-white light irradiation alters apple peel metabolome. J Agri Food Chem 56:1138–1147CrossRefGoogle Scholar
  21. Ryll T, Wagner R (1991) Improved ion-pair high-performance liquid chromatographic method for the quantification of a wide variety of nucleotides and sugar-nucleotides in animal cells. J Chromatogr 570:77–88PubMedCrossRefGoogle Scholar
  22. Saure MC (1990) External control of anthocyanin formation in apple. Sci Hortic 42:181–218CrossRefGoogle Scholar
  23. Seifert GJ, Barber C, Wells B, Dolan L, Roberts K (2002) Galactose biosynthesis in Arabidopsis: genetic evidence for substrate channeling from UDP-D-galactose into cell wall polymers. Curr Biol 12:1840–1845PubMedCrossRefGoogle Scholar
  24. Tada H, Terahara N, Motoyama E, Shimomura K, Ishimaru K (1996) Anthocyanins in Lobelia chinensis hairy roots. Plant Tiss Cult Lett 13:85–86Google Scholar
  25. Takos AM, Jaffé FW, Jacob SR, Bogs J, Robinson SP, Walker AR (2006) Light induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiol 142:1216–1232PubMedCrossRefGoogle Scholar
  26. Terahara N, Sakanashi T, Tsukui A (1993) Anthocyanins from the berries of haskaap, Lonicera caerulea L. J Home Econ Jan 44:197–201Google Scholar
  27. Ubi BE (2004) External stimulation of anthocyanin biosynthesis in apple fruit. J Food Agric Environ 2:65–70Google Scholar
  28. Ubi BE, Honda C, Bessho H, Kondo S, Wada M, Kobayashi S, Moriguchi T (2006) Expression analysis of anthocyanin biosynthetic genes in apple skin: Effect of UV-B and temperature. Plant Sci 170:571–578CrossRefGoogle Scholar
  29. Wan C, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 223:7–12PubMedCrossRefGoogle Scholar
  30. Yonekura-Sakakibara K, Tohge T, Matsuda F, Nakabayashi R, Takayama H, Niida R, Watanabe-Takahashi A, Inoue E, Saito K (2008) Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding gene-metabolite correlations in Arabidopsis. Plant Cell 20:2160–2176PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Yusuke Ban
    • 1
    • 2
  • Satoru Kondo
    • 3
  • Benjamin Ewa Ubi
    • 2
    • 4
  • Chikako Honda
    • 5
  • Hideo Bessho
    • 5
  • Takaya Moriguchi
    • 1
    • 2
  1. 1.Graduate School of Life and Environmental SciencesUniversity of TsukubaTsukubaJapan
  2. 2.National Institute of Fruit Tree ScienceTsukubaJapan
  3. 3.Graduate School of HorticultureChiba UniversityMatsudoJapan
  4. 4.Biotechnology Research and Development CentreEbonyi State UniversityAbakalikiNigeria
  5. 5.National Institute of Fruit Tree ScienceMoriokaJapan

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