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.
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Abbreviations
- Cy:
-
Cyanidin
- Cy3-gal:
-
Cyanidin 3-galactoside
- DAFB:
-
Days after full bloom
- UDP-gal:
-
UDP-galactose
- UDP-glu:
-
UDP-glucose
- UV:
-
Ultraviolet
References
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 10:1135–1149
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 48:958–970
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 58:25–834
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
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 102:18225–18230
Dong Y, Mitra D, Kootstra A (1995) Postharvest stimulation of skin color in Royal Gala apple. J Am Soc Hortic Sci 120:95–100
Dörmann P, Benning C (1998) The role of UDP-glu epimerase in carbohydrate metabolism of Arabidopsis. Plant J 13:641–652
Goodman CD, Casati P, Walbot V (2004) A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell 16:1812–1826
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 42:534–538
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 53:8790–8796
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 40:955–962
Kitamura S, Shikazono N, Tanaka A (2004) TRANSPARENT TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. Plant J 37:104–114
Lancaster JE (1992) Regulation of skin color in apples. Crit Rev Plant Sci 10:487–502
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 71:317–321
Lingle SE, Lester GE, Dunlap JR (1987) Effect of postharvest heat treatment and storage on sugar metabolism in polyethylene-wrapped muskmelon fruit. HortScience 22:917–919
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 375:397–400
Mori K, Goto-Yamamoto N, Kitayama M, Hashizume K (2007) Loss of anthocyanins in red-wine grape under high temperature. J Exp Bot 58:1935–1945
Moyrand F, Lafontaine I, Fontaine T, Janbon G (2008) UGE1 and UGE2 regulate the UDP-glucose/UDP-galactose equilibrium in Cryptococcus neoformans. Eukaryot Cell 7:2069–2077
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 166:1097–1104
Rudell DR, Mattheis JP, Curry EA (2008) Prestorage ultraviolet-white light irradiation alters apple peel metabolome. J Agri Food Chem 56:1138–1147
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 570:77–88
Saure MC (1990) External control of anthocyanin formation in apple. Sci Hortic 42:181–218
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 12:1840–1845
Tada H, Terahara N, Motoyama E, Shimomura K, Ishimaru K (1996) Anthocyanins in Lobelia chinensis hairy roots. Plant Tiss Cult Lett 13:85–86
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 142:1216–1232
Terahara N, Sakanashi T, Tsukui A (1993) Anthocyanins from the berries of haskaap, Lonicera caerulea L. J Home Econ Jan 44:197–201
Ubi BE (2004) External stimulation of anthocyanin biosynthesis in apple fruit. J Food Agric Environ 2:65–70
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 170:571–578
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 223:7–12
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 20:2160–2176
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Ban, Y., Kondo, S., Ubi, B.E. et al. UDP-sugar biosynthetic pathway: contribution to cyanidin 3-galactoside biosynthesis in apple skin. Planta 230, 871–881 (2009). https://doi.org/10.1007/s00425-009-0993-4
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DOI: https://doi.org/10.1007/s00425-009-0993-4