Temporal and spatial regulation of anthocyanin biosynthesis provide diverse flower colour intensities and patterning in Cymbidium orchid

Planta

Volumn 240, Issue 5, 2014, Pages 983-1002

  Wang, Lei ^a,b   Albert, Nick W ^a   Zhang, Huaibi ^a   Arathoon, Steve ^a   Boase, Murray R ^a   Ngo, Hanh ^a   Schwinn, Kathy E ^a   Davies, Kevin M ^a   Lewis, David H ^a  

^a THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

^b MASSEY UNIVERSITY   (New Zealand)

Author keywords

Anthocyanin; Carotenoid; Flavonoid; Flower colour; Orchid

Indexed keywords

CYMBIDIUM; CYMBIDIUM HYBRID;

ACYLTRANSFERASE; ALCOHOL DEHYDROGENASE; ANTHOCYANIDIN SYNTHASE; ANTHOCYANIN; BETA CAROTENE; CHALCONE SYNTHASE; CYANIDIN 3-RUTINOSIDE; CYTOCHROME P450; DIHYDROFLAVANOL 4-REDUCTASE; FLAVONOID 3'-HYDROXYLASE; FLAVONOL SYNTHASE; GLUCOSIDE; KAEMPFEROL; KAEMPFEROL DERIVATIVE; OXIDOREDUCTASE; OXYGENASE; PEONIDIN-3-RUTINOSIDE; QUERCETIN; VEGETABLE PROTEIN;

BIOSYNTHESIS; CLASSIFICATION; COLOR; FLOWER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; ORCHIDACEAE; PHYLOGENY; PIGMENTATION; SPECIES DIFFERENCE;

ACYLTRANSFERASES; ALCOHOL OXIDOREDUCTASES; ANTHOCYANINS; BETA CAROTENE; BIOSYNTHETIC PATHWAYS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COLOR; CYTOCHROME P-450 ENZYME SYSTEM; FLOWERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GLUCOSIDES; KAEMPFEROLS; MASS SPECTROMETRY; ORCHIDACEAE; OXIDOREDUCTASES; OXYGENASES; PHYLOGENY; PIGMENTATION; PLANT PROTEINS; QUERCETIN; SPECIES SPECIFICITY;

EID: 84919394676     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-014-2152-9     Document Type: Article

References (73)

1. Albert NW, Lewis DH, Zhang H, Irving LJ, Jameson PE, Davies KM (2009) Light-induced vegetative anthocyanin pigmentation in Petunia. J Exp Bot 60:2191–2202
2. Albert NW, Arathoon S, Collette VE, Schwinn KE, Jameson PE, Lewis DH, Zhang H, Davies KM (2010) Activation of anthocyanin synthesis in Cymbidium orchids: variability between known regulators. Plant Cell Tissue Organ Cult 100:355–360
3. Albert NW, Lewis DH, Zhang H, Schwinn KE, Jameson PE, Davies KM (2011) Members of an R2R3-MYB transcription factor family in Petunia are developmentally and environmentally regulated to control complex floral and vegetative pigmentation patterning. Plant J 65:771–784
4. Albert NW, Davies KM, Lewis DH, Zhang H, Montefiori M, Brendolise C, Boase MR, Ngo H, Jameson PE, Schwinn KE (2014) A conserved network of transcriptional activators and repressors regulates anthocyanin pigmentation in eudicots. Plant Cell 26:962–980
5. Ampomah-Dwamena C, Dejnoprat S, Lewis D, Sutherland P, Volz RK, Allan AC (2012) Metabolic and gene expression analysis of apple (Malus × domestica) carotenogenesis. J Exp Bot 63:4497–4511
6. Arditti J (1992) Phytochemistry. In: Arditti J (ed) Fundamentals of orchid biology. Wiley, New York, pp 243–259
7. Austin MB, Noel AJP (2003) The chalcone synthase superfamily of type III polyketide synthases. Nat Prod Rep 20:79–110
8. Baudry A, Heim MA, Dubreucq B, Caboche M, Weisshaar B, Lepiniec L (2004) TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. Plant J 39:366–380
9. Bechtel H, Cribb P, Launert E (1992) The manual of cultivated orchid species, 3rd edn. The MIT Press, Cambridge
10. Boddu J, Svabek C, Sekhon R, Gevens A, Nicholson RL, Jones AD, Pedersen JF, Gustine DL, Chopra S (2004) Expression of a putative flavonoid 3′-hydroxylase in sorghum mesocotyls synthesizing 3-deoxyanthocyanidin phytoalexins. Physiol Mol Plant Pathol 65:101–113
11. Brugliera F, Barri-Rewell G, Holton TA, Mason JG (1999) Isolation and characterization of a flavonoid 3′-hydroxylase cDNA clone corresponding to the Ht1 locus of Petunia hybrida. Plant J 19:441–451
12. Cazzonelli CI, Pogson BJ (2010) Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci 15:266–274
13. Chapple C (1998) Molecular-genetic analysis of plant cytochrome P450-dependent monooxygenases. Annu Rev Plant Physiol Plant Mol Biol 49:311–343
14. Chiou C-Y, Yeh K-W (2008) Differential expression of MYB gene (OgMYB1) determines color patterning in floral tissue of Oncidium Gower Ramsey. Plant Mol Biol 66:379–388
15. Chiou CY, Pan HA, Chuang YN, Yeh KW (2010) Differential expression of carotenoid-related genes determines diversified carotenoid coloration in floral tissues of Oncidium cultivars. Planta 232:937–948
16. Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995
17. Collette VE, Jameson PE, Schwinn KE, Umaharan P, Davies KM (2004) Temporal and spatial expression of flavonoid biosynthetic genes in flowers of Anthurium andraeanum. Physiol Plant 122:297–304
18. Davies KM, Bradley JM, Schwinn KE, Markham KR, Podivinsky E (1993) Flavonoid biosynthesis in flower petal lines of lisianthus (Eustoma grandiflora Grise.). Plant Sci 95:67–77
19. Davies KM, Albert NW, Schwinn KE (2012) From landing lights to mimicry: the molecular regulation of flower colouration and mechanisms for pigmentation patterning. Funct Plant Biol 39:619–638
20. de Rosso VV, Mercadante AZ (2007) Identification and quantification of carotenoids, by HPLC-PDA-MS/MS, from Amazonian fruits. J Agric Food Chem 55:5062–5072
21. Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13
22. Feller A, Machemer K, Braun EL, Grotewold E (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66:94–116
23. Fraser PD, Pinto ES, Holloway DE, Bramley PM (2000) Application of high-performance liquid chromatography with photodiode array detection to the metabolic profiling of plant isoprenoids. Plant J 24:551–558
24. Griesbach RJ (1984) Effects of carotenoid-anthocyanin combinations on flower color. J Hered 75:145–147
25. Griesbach RJ (1990) Flavonoid copigments and anthocyanin of Phalaenopsis schilleriana. Lindleyana 5:231–234
26. Grotewold E (2006) The genetics and biochemistry of floral pigments. Annu Rev Plant Biol 57:761–780
27. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
28. Han Y, Ming F, Wang J, Ye M, Shen D (2005) A novel chalcone synthase gene from Phalaenopsis orchid that alters floral morphology in transgenic tobacco plants. Plant Mol Biol Rep 23:193–194
29. Han YY, Ming F, Wang JW, Wen JG, Ye MM, Shen DL (2006a) Cloning and characterization of a novel chalcone synthase gene from Phalaenopsis hybrida orchid flowers. Russ J Plant Physiol 53:223–230
30. Han YY, Ming F, Wang W, Wang JW, Ye MM, Shen DL (2006b) Molecular evolution and functional specialization of chalcone synthase superfamily from Phalaenopsis orchid. Genetica 128:429–438
31. Hartmann U, Sagasser M, Mehrtens F, Stracke R, Weisshaar B (2005) Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control light-responsive and tissue-specific activation of phenylpropanoid biosynthesis genes. Plant Mol Biol 57:155–171
32. Hasemann CA, Kurumbail RG, Boddupalli SS, Peterson JA, Deisenhofer J (1995) Structure and function of cytochromes-P450—a comparative analysis of 3 crystal structures. Structure 3:41–62
33. Helariutta Y, Elomaa P, Kotilainen M, Griesbach RJ, Schroder J, Teeri TH (1995) Chalcone synthase-like genes active during corolla development are differentially expressed and encode enzymes with different catalytic properties in Gerbera hybrida. Plant Mol Biol 28:47–60
34. Hendry GAF, Houghton JD, Brown SB (1987) The degradation of chlorophyll—a biological enigma. New Phytol 107:255–302
35. Hew CS (2001) Ancient Chinese orchid cultivation: a fresh look at an age-old practice. Sci Hortic 87:1–10
36. Hieber AD, Mudalige-Jayawickrama RG, Kuehnle AR (2006) Color genes in the orchid Oncidium Gower Ramsey: identification, expression, and potential genetic instability in an interspecific cross. Planta 223:521–531
37. Holton T, Cornish EC (1995) Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7:1071–1083
38. Hörtensteiner S (2009) Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends Plant Sci 14:155–162
39. Hunter DA, Steele BC, Reid MS (2002) Identification of genes associated with perianth senescence in daffodil (Narcissus pseudonarcissus L. ‘Dutch Master’). Plant Sci 163:13–21
40. Johnson ET, Yi HK, Shin BC, Oh BJ, Cheong HS, Choi G (1999) Cymbidium hybrida dihydroflavonol 4-reductase does not efficiently reduce dihydrokaempferol to produce orange pelargonidin-type anthocyanins. Plant J 19:81–85
41. Kamffer Z, Bindon KA, Oberholster A (2010) Optimization of a method for the extraction and quantification of carotenoids and chlorophylls during ripening in grape berries (Vitis vinifera cv. Merlot). J Agric Food Chem 58:6578–6586
42. Kuehnle AR, Lewis DH, Markham KR, Mitchell KA, Davies KM, Jordan BR (1997) Floral flavonoids and pH in Dendrobium orchid species and hybrids. Euphytica 95:187–194
43. Lai YS, Shimoyamada Y, Nakayama M, Yamagishi M (2012) Pigment accumulation and transcription of LhMYB12 and anthocyanin biosynthesis genes during flower development in the Asiatic hybrid lily (Lilium spp.). Plant Sci 193:136–147
44. Liew C-F, Loh C-S, Goh C-J, Lim S-H (1998a) The isolation, molecular characterization and expression of dihydroflavonol 4-reductase cDNA in the orchid, Bromheadia finlaysoniana. Plant Sci 135:161–169
45. Liew CF, Goh CJ, Loh CS, Lim SH (1998b) Cloning and characterization of full-length cDNA clones encoding chalcone synthase from the orchid Bromheadia finlaysoniana. Plant Physiol Biochem 36:647–656
46. Liu XJ, Chuang YN, Chiou CY, Chin DC, Shen FQ, Yeh KW (2012) Methylation effect on chalcone synthase gene expression determines anthocyanin pigmentation in floral tissues of two Oncidium orchid cultivars. Planta 236:401–409
47. Ma H, Pooler M, Griesbach R (2008) Ratio of Myc and Myb transcription factors regulates anthocyanin production in orchid flowers. J Am Soc Hortic Sci 133:133–138
48. Ma H, Pooler M, Griesbach R (2009) Anthocyanin regulatory/structural gene expression in Phalaenopsis. J Am Soc Hortic Sci 134:88–96
49. Martens S, Forkmann G, Britsch L, Wellmann F, Matern U, Lukacin R (2003) Divergent evolution of flavonoid 2-oxoglutarate-dependent dioxygenases in parsley. FEBS Lett 544:93–98
50. Mori S, Otani M, Kobayashi H, Nakano M (2014) Isolation and characterization of the dihydroflavonol 4-reductase gene in the monocotyledonous ornamental Agapanthus praecox ssp. orientalis (Leighton) Leighton. Sci Hortic 166:24–30
51. Mudalige RG, Kuehnle AR, Amore TD (2003) Pigment distribution and epidermal cell shape in Dendrobium species and hybrids. HortScience 38:573–577
52. Mudalige-Jayawickrama RG, Champagne MM, Hieber AD, Kuehnle AR (2005) Cloning and characterization of two anthocyanin biosynthetic genes from Dendrobium orchid. J Am Soc Hortic Sci 130:611–618
53. Mullen W, Marks SC, Crozier A (2007) Evaluation of phenolic compounds in commercial fruit juices and fruit drinks. J Agric Food Chem 55:3148–3157
54. Nakatsuka A, Izumi Y, Yamagishi M (2003) Spatial and temporal expression of chalcone synthase and dihydroflavonol 4-reductase genes in the Asiatic hybrid lily. Plant Sci 165:759–767
55. Noda N, Kanno Y, Kato N, Kazuma K, Suzuki M (2004) Regulation of gene expression involved in flavonol and anthocyanin biosynthesis during petal development in lisianthus (Eustoma grandiflorum). Physiol Plant 122:305–313
56. Saito N, Toki K, Uesato K, Shigihara A, Honda T (1994) An acylated cyanidin glycoside from the red-purple flowers of Dendrobium. Phytochemistry 37:245–248
57. Schwinn KE, Davies KA (2004) Flavonoids. In: Davies K (ed) Plant pigments and their manipulation, vol 14., Blackwell PublishingOxford, UK, pp 92–149
58. Schwinn K, Venail J, Shang YJ, Mackay S, Alm V, Butelli E, Oyama R, Bailey P, Davies K, Martin C (2006) A small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum. Plant Cell 18:831–851
59. Sharma M, Cortes-Cruz M, Ahern KR, McMullen M, Brutnell TP, Chopra S (2011) Identification of the pr1 gene product completes the anthocyanin biosynthesis pathway of maize. Genetics 188:69–79
60. Shirley BW (1996) Flavonoid biosynthesis: ‘new’ functions for an old pathway. Trends Plant Sci 1:377–382
61. Sugiyama A, Kinoshita M, Kako S, Ohno H, Sakakibara K (1977) Studies on the flower colour of Cymbidium. I. Properties of anthocyanins in the flowers. J Japan Soc Hortic Sci 46:72–80
62. Tanaka Y, Katsumoto Y, Brugliera F, Mason J (2005) Genetic engineering in floriculture. Plant Cell Tissue Organ Cult 80:1–24
63. Tanaka Y, Sasaki N, Ohmiya A (2008) Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J 54:733–749
64. Tatsuzawa F, Saito N, Yokoi M (1996) Anthocyanins in the flowers of Cymbidium. Lindleyana 11:214–219
65. Tatsuzawa F, Saito N, Seki H, Hara R, Yokoi M, Honda T (1997) Acylated cyanidin glycosides in the red-purple flowers of Phalaenopsis. Phytochemistry 45:173–177
66. Thammasiri K, Tang CS, Yamamoto HY, Kamemoto H (1986) Carotenoids and chlorophylls in yellow flowered Dendrobium species. Lindleyana 1:215–218
67. Tian Q, Giusti MM, Stoner GD, Schwartz SJ (2005) Screening for anthocyanins using high-performance liquid chromatography coupled to electrospray ionization tandem mass spectrometry with precursor-ion analysis, product-ion analysis, common-neutral-loss analysis, and selected reaction monitoring. J Chromatogr 1091:72–82
68. Tomlinson PC (1985) Cymbidiums: a cultural guide, 2nd edn. Wellington Orchid Society, Wellington
69. Turnbull JJ, Nakajima J, Welford RWD, Yamazaki M, Saito K, Schofield CJ (2004) Mechanistic studies on three 2-oxoglutarate-dependent oxygenases of flavonoid biosynthesis—anthocyanidin synthase, flavonol synthase, and flavanone 3 ß-hydroxylase. J Biol Chem 279:1206–1216
70. Wang JW, Ming F, Han YY, Shen DL (2006) Flavonoid 3′, 5′-hydroxylase from Phalaenopsis: a novel member of cytochrome P450s, its cDNA cloning, endogenous expression and molecular modeling. Biotechnol Lett 28:327–334
71. Weiss D (2000) Regulation of flower pigmentation and growth: multiple signaling pathways control anthocyanin synthesis in expanding petals. Physiol Plant 110:152–157
72. Whang S, Um W, Song I-J, Lim P, Choi K, Park K-W, Kang K-W, Choi M, Koo J (2011) Molecular analysis of anthocyanin biosynthetic genes and control of flower coloration by flavonoid 3′, 5′-hydroxylase (F3′5′H) in Dendrobium moniliforme. J Plant Biol 54:209–218
73. Woltering EJ, Somhorst D (1990) Regulation of anthocyanin synthesis in Cymbidium flowers: effects of emasculation and ethylene. J Plant Physiol 136:295–299