Synergistic effects of light and temperature on anthocyanin biosynthesis in callus cultures of red-fleshed apple (Malus sieversii f. niedzwetzkyana)

Plant Cell, Tissue and Organ Culture

Volumn 127, Issue 1, 2016, Pages 217-227

  Wang, Nan ^a   Zhang, Zongying ^a   Jiang, Shenghui ^a   Xu, Haifeng ^a   Wang, Yicheng ^a   Feng, Shouqian ^a   Chen, Xuesen ^a  

^a SHANDONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

Anthocyanin; Callus; Light; Malus sieversii f. niedzwetzkyana; Temperature

Indexed keywords

ANTHOCYANINS; BIOCHEMISTRY; BIOSYNTHESIS; FRUITS; GENE EXPRESSION; GENES; LIGHT; POLYMERASE CHAIN REACTION; TEMPERATURE; TRANSCRIPTION;

ANTHOCYANIN ACCUMULATION; ANTHOCYANIN BIOSYNTHESIS; ANTHOCYANIN CONTENT; CALLUS; EXPRESSION PATTERNS; MALUS SIEVERSII; QUANTITATIVE REAL-TIME POLYMERASE CHAIN REACTION; TEMPERATURE-INDUCED;

GENE EXPRESSION REGULATION;

EID: 84982126588     PISSN: 01676857     EISSN: 15735044     Source Type: Journal    
DOI: 10.1007/s11240-016-1044-z     Document Type: Article

References (50)

1. Azuma A, Yakushiji H, Koshita Y, Kobayashi S (2012) Flavonoid biosynthesis-related genes in grape skin are differentially regulated by temperature and light conditions. Planta 236(4):1067–1080
2. Balasuriya N, Rupasinghe HPV (2012) Antihypertensive properties of flavonoid-rich apple peel extract. Food Chem 135(4):2320–2325
3. Ban Y, Honda C, Hatsuyama Y, Igarashi M, Bessho H, Moriguchi T (2007) 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(7):958–970
4. Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12(12):2383–2393
5. Butelli E, Titta L, Giorgio M, Mock HP, Matros A, Peterek S, Wijlen 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):1301–1308
6. Chandler VL, Radicella JP, Robbins TP, Chen J, Turks D (1989) Two regulatory genes of the maize anthocyanin pathway are homologous: isolation of B utilizing R genomic sequences. Plant Cell 1(12):1175–1183
7. Chen XS, Han MY, Su GL, Liu FZ, Guo GN, Jiang YM (2010) Discussion on today’s world apple industry trends and the suggestions on sustainable and efficient development of apple industry in China. J Fruit Sci 27:598–604
8. Christie PJ, Alfenito MR, Walbot V (1994) Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. Planta 194(4):541–549
9. Chun OK, Kim DO, Chang YL (2004) Superoxide radical scavenging activity of the major polyphenols in fresh plums. J Agric Food Chem 51(27):8067–8072
10. Cominelli E, Gusmaroli G, Allegra D, Galbiati M, Wade HK, Jenkins GI, Tonelli C (2008) Expression analysis of anthocyanin regulatory genes in response to different light qualities in Arabidopsis thaliana. J Plant Physiol 165(8):886–894
11. Dixon RA, Steele CL (1999) Flavonoids and isoflavonoids—a gold mine for metabolic engineering. Trends Plant Sci 4(10):394–400
12. Espley R, Hellens R, Putterill J, Stevenson DA, Allan AC (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J 49(3):414–427
13. Hall RD, Yeoman MM (1986) Factors determining anthocyanin yield in cell cultures of Catharanthus roseus (L.) G. Don. New Phytol 103:33–43
14. 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(11):955–962
15. Horbowicz M, Kosson R, Grzesiuk A, Debski H (2008) Anthocyanins of fruits and vegetables—their occurrence, analysis and role in human nutrition. Veg Crops Res Bull 68(68):5–22
16. Ji XH, Wang YT, Zhang R, Wu SJ, An MM, Li M, Wang CZ, Chen XL, Zhang YM, Chen XS (2015) Effect of auxin, cytokinin and nitrogen on anthocyanin biosynthesis in callus cultures of red-fleshed apple (Malus sieversii f. niedzwetzkyana). Plant Cell, Tissue Organ Cult 120(1):325–337
17. Kakegawa K, Kaneko Y, Hattori E, Koike K, Takeda K (1987) Cell cultures of Centaurea cyanus produces malonated anthocyanin in UV light. Phytochemistry 26:2261
18. Kim SH, Lee JR, Kim SR (2006) Characterization of an apple anthocyanidin synthase gene in transgenic tobacco plants. J Plant Biol 49(4):326–330
19. Kondo S, Hiraoka K, Kobayashi S, Honda C, Terahara N (2002) Changes in the expression of anthocyanin biosynthetic genes during apple development. J Am Soc Hortic Sci Am Soc Hortic Sci 127(6):971–976
20. Li YY, Mao K, Zhao C, Zhao XY, Zhang HL, Shu HR, Hao YJ (2012) MdCOP1 ubiquitin E3 ligases interact with MdMYB1 to regulate light-induced anthocyanin biosynthesis and red fruit coloration in apple 1, [W] [OA]. Plant Physiol 160(2):1011–1022
21. Lin-Wang K, Micheletti D, Palmer J, Volz R, Lozano L, Espley R, Hellens RP, Chagne D, Rowan DD, Troggio M, Iglesias I, Allen AC (2011) High temperature reduces apple fruit colour via modulation of the anthocyanin regulatory complex. Plant, Cell Environ 34(7):1176–1190
22. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 method. Methods 25(4):402–408
23. Lo Piero AR, Ivana P, Paolo R, Goffredo P (2005) Anthocyanins accumulation and related gene expression in red orange fruit induced by low temperature storage. J Agric Food Chem 53(23):9083–9088
24. Meng R, Zhang J, An L, Zhang B, Jiang X, Yang Y, Zhao Z (2016) Expression profiling of several gene families involved in anthocyanin biosynthesis in apple (Malus domestica. Borkh.) Skin during fruit development. J Plant Growth Regul 35(2):449–464
25. Mori K, Sugaya S, Gemma H (2005) Decreased anthocyanin biosynthesis in grape berries grown under elevated night temperature condition. Sci Hortic 105(3):319–330
26. Narayan MS, Thimmaraju R, Bhagyalakshmi B (2005) Interplay of growth regulators during solid-state and liquid-state batch cultivation of anthocyanin producing cell line of Daucus carota. Process Biochem 40:351–358
27. Nie JL, Lv DG, Li J, Liu FZ, Li HF, Xu GF, Wu YL (2010) Studies on composition and content of flavonoids in fruit of ‘Nagafu 2’ apple. Acta Hortic Sin 37(37):1559–1566
28. Paz-Ares J, Ghosal D, Wienand U, Peterson PA, Saedler H (1988) The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. EMBO J 6(12):3553–3558
29. Quattrocchio F, Wing JF, Leppen H, Mol J, Koes RE (1993) Regulatory genes controlling anthocyanin pigmentation are functionally conserved among plant species and have distinct sets of target genes. Plant Cell 5(11):1497–1512
30. Regan BC, Julliot C, Simmen B, Viénot F, Charles-Dominique P, Mollon JD (2001) Fruits, foliage and the evolution of primate colour vision. Philos Trans R Soc B Biol Sci 356(1407):229–283
31. Rowan DD, Mingshu C, Kui LW, Cooney JM, Jensen DJ, Austin PT, Hunt MB, Cara N, Hellens RP, Schaffer RJ (2009) Environmental regulation of leaf colour in red 35S:PAP1 Arabidopsis thaliana. New Phytol 182(1):102–115
32. Sato K, Nakayama M, Shigeta JI (1996) Culturing conditions affecting the production of anthocyanin in suspended cell cultures of strawberry. Plant Sci 113:91–98
33. Schaefer HM, McGraw K, Catoni C (2008) Birds use fruit colour as honest signal of dietary antioxidant rewards. Funct Ecol 22(2):303–310
34. Shvarts M, Borochov A, Weiss D (1997) Low temperature enhances petunia flower pigmentation and induces chalcone synthase gene expression. Physiol Plant 99(1):67–72
35. Simões C, Albarello N, Castro TCD, Mansur E (2012) Production of anthocyanins by plant cell and tissue culture strategies. Biotechnol Prod Plant Second Metab (5):67–86
36. Smith MAL, Marley KA, Seigler D, Singletary KW, Meline B (2000) Bioactive properties of wild blueberry fruits. J Food Sci 65(2):352–356
37. Solfanelli C, Bartolini S, Vitagliano C, Lorenzi R (2006) Immunolocalization and quantification of IAA after self- and free-pollination in Olea europaea L. Sci Hortic 110(4):345–351
38. Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4(5):447–456
39. Szankowski I, Li H, Flachowsky H, Höfer M, Hanke MV, Fischer T, Forkmann G, Treutter D, Schwab W, Hoffmann T (2009) Metabolic engineering of flavonoid biosynthesis in apple (Malus domestica Borkh.). In: Proceedings of the 12th Eucarpia symposium on fruit breeding and genetics, Zaragoza, Spain, pp 511–516
40. Takos AM, Jaffé FW, Jacob SR, Jochen B, Robinson SP, Walker AR (2006) Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples & nbsp. Plant Physiol 142(3):1216–1232
41. Tian J, Han ZY, Zhang LR, Song TT, Zhang J, Li JY, Yao YC (2015) Induction of anthocyanin accumulation in crabapple (Malus cv.) leaves by low temperatures. Hortsci Publ Am Soc Hortic Sci 50(5):640–649
42. Treutter D (2001) Biosynthesis of phenolic compounds and its regulation in apple. Plant Growth Regul 34(1):71–89
43. Ubi B, Honda C, Bessho H, Kondo S, Wada M, Kobayashi ST (2006) Expression analysis of anthocyanin biosynthetic genes in apple skin: effect of UV-B and temperature. Plant Sci 170(3):571–578
44. Wang J, Mazza G (2002) Inhibitory effects of anthocyanins and other phenolic compounds on nitric oxide production in LPS/IFN-gamma-activated RAW 264.7 macrophages. J Agric Food Chem 50(4):850–857
45. Wang ZH, Tang GH, Li ZQ, Wang LJ (2006) Promotion of 5-am inolevulinic acid and genistein on anthocyanin accumulationin apples. Acta Hortic Sin 33:1055–1058
46. Wang Y, Chen XS, Liu DL, Wang CZ, Song Y, Chen XL, Zhang YM (2010) Antioxidant activity and anthocyanins analysis of pulp in ‘Zihong 1’ red-flesh apple. Acta Hortic Sin 39:1991–1998
47. Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126(2):485–493
48. Xie XB, Shen LI, Zhang RF, Zhao J, Chen YC, Zhao Q, Yao YX, You CX, Zhang XS, Hao YJ (2012) The bHLH transcription factor MdbHLH3 promotes anthocyanin accumulation and fruit colouration in response to low temperature in apples. Plant, Cell Environ 35(11):1884–1897
49. Zhong JJ, Yoshida M, Fujiyama K, Seki T, Yoshida T (1993) Enhancement of anthocyanin production by Perilla frutescens cells in a stirred bioreactor with internal light irradiation. J Ferment Bioeng 75(4):299–303
50. Zhou M, Sun Z, Wang C, Zhang X, Tang Y, Zhu X, Shao J, Wu Y (2015) Changing a conserved amino acid in R2R3-MYB transcription repressors results in their cytoplasmic accumulation and abolishes their repressive activity in Arabidopsis. Plant J 84(2):395–403