Qualitative and quantitative control of carotenoid accumulation in flower petals

Scientia Horticulturae

Volumn 163, Issue , 2013, Pages 10-19

  Ohmiya, Akemi ^a  

^a NATIONAL INSTITUTE OF VEGETABLE AND TEA SCIENCE   (Japan)

Author keywords

Carotenoid; Carotenoid biosynthesis; Carotenoid degradation; Chromoplast; Petal color

Indexed keywords

BIOACCUMULATION; CAROTENOID; COLOR; DEVELOPMENTAL BIOLOGY; FLOWER; MOLECULAR ANALYSIS; PIGMENT; POLLINATOR; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS;

EID: 84888852143     PISSN: 03044238     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.scienta.2013.06.018     Document Type: Review

References (96)

1. Barsan C., Zouine M., Maza E., Bian W., Egea I., Rossignol M., Bouyssie D., Pichereaux C., Purgatto E., Bouzayen M., Latché A., Pech J.-C. Proteomic analysis of chloroplast-to-chromoplast transition in tomato reveals metabolic shifts coupled with disrupted thylakoid biogenesis machinery and elevated energy-production components. Plant Physiol. 2012, 160:708-725.
2. Bouvier F., Hugueney P., d'Harlingue A., Kuntz M., Camara B. Xanthophyll biosynthesis in chromoplasts: isolation and molecular cloning of an enzyme catalyzing the conversion of 5,6-epoxycarotenoid into ketocarotenoid. Plant J. 1994, 6:45-54.
3. Bouvier F., Suire C., Mutterer J., Camara B. Oxidative remodeling of chromoplast carotenoids: identification of the carotenoid dioxygenase CsCCD and CsZCD genes involved in crocus secondary metabolite biogenesis. Plant Cell 2003, 15:47-62.
4. Breitenbach J., Sandmann G. δ-Carotene cis isomers as products and substrates in the plant poly-cis carotenoid biosynthetic pathway to lycopene. Planta 2005, 220:785-793.
5. Britton G., Liaaen-Jensen S., Pfander H. Carotenoids Handbook 2004, Birkhäuser, Basel.
6. Buckner B., Miguel P.S., Janick-Buckner D., Bennetzen J.L. The y1 gene of maize codes for phytoene synthase. Genetics 1996, 143:479-488.
7. Chiou C.-Y., Pan H.-A., Chuang Y.-N., Yeh K.-W. Differential expression of carotenoid-related genes determines diversified carotenoid coloration in floral tissues of Oncidium cultivars. Planta 2010, 232:937-948.
8. Cooper C.M., Davies N.W., Menary R.C. Changes in some carotenoids and apocarotenoids during flower development in Boronia megastigma (Nees). J. Agr. Food Chem. 2009, 57:1513-1520.
9. Corona V., Aracri B., Kosturkova G., Bartley G.E., Pitto L., Giorgetti L., Scolnik P.A., Giuliano G. Regulation of a carotenoid biosynthesis gene promoter during plant development. Plant J. 1996, 9:505-512.
10. Cunningham F.X., Pogson B., Sun Z., McDonald K.A., DellaPenna D., Gantt E. Functional analysis of the β and e lycopene cyclase enzymes of Arabidopsis reveals a mechanism for control of cyclic carotenoid formation. Plant Cell 1996, 8:1613-1626.
11. Cunningham F.X., Gantt E. Genes and enzymes of carotenoid biosynthesis in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998, 49:557-583.
12. Cunningham F.X., Gantt E. One ring or two? Determination of ring number in carotenoids by lycopene e-cyclases. PNAS 2001, 98:2905-2910.
13. Cunningham F.X., Gantt E. A study in scarlet: enzymes of ketocarotenoid biosynthesis in the flowers of Adonis aestivalis. Plant J 2005, 41:478-492.
14. Cunningham F.X., Gantt E. Elucidation of the pathway to astaxanthin in the flowers of Adonis aestivalis. Plant Cell 2011, 23:3055-3069.
15. DellaPenna D., Pogson B.J. Vitamin synthesis in plants: tocopherols and carotenoids. Annu. Rev. Plant Biol. 2006, 57:711-738.
16. Dun E.A., Philip B., Brewer P.B., Beveridge C.A. Strigolactones: discovery of the elusive shoot branching hormone. Trends Plant Sci. 2009, 14:364-372.
17. Eugster C.H., Märki-Fisher E. The chemistry of rose pigments. Angew. Chem. Int. Ed. Engl. 1991, 30:654-672.
18. Fraser P.D., Kiano J.W., Truesdale M.R., Schuch W., Bramley P.M. Phytoene synthase-2 enzyme activity in tomato does not contribute to carotenoid synthesis in ripening fruit. Plant Mol. Biol. 1999, 40:687-698.
19. Fraser P.D., Bramley P.M. The biosynthesis and nutritional uses of carotenoids. Prog. Lipid Res. 2004, 43:228-265.
20. Galpaz N., Ronen G., Khalfa Z., Zamir D., Hirschberg J. A chromoplast-specific carotenoid biosynthesis pathway is revealed by cloning of the tomato white-flower locus. Plant Cell 2006, 18:1947-1960.
21. Giuliano G., Bartley G.E., Scolnik P.A. Regulation of carotenoid biosynthesis during tomato development. Plant Cell 1993, 5:379-387.
22. Green B.R., Durnford D.G. The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Ann. Rev. Plant Physiol. Plant Mol. Biol. 1996, 47:685-714.
23. Hai N.T.L., Masuda J., Miyajima I., Thien N.Q., Mojtahedi N., Hiramatsu M., Kim J.-H., Okubo H. Involvement of carotenoid cleavage dioxygenase 4 gene in tepal color change in Lilium brownii var. colchesteri. J. Jpn. Soc. Hort. Sci. 2012, 81:366-373.
24. Hattori K. Inheritance of carotenoid pigmentation in flower color of chrysanthemum. Jpn. J. Breed. 1991, 41:1-9.
25. Hieber A.D., Mudalige-Jayawickrama R.G. Color genes in the orchid Oncidium Gower Ramsey: identification, expression, and potential genetic instability in an interspecific cross. Planta 2006, 223:521-531.
26. Huang F.-C., Horvath G., Molnar P., Turcsi E., Deli J., Schrader J., Sandmann G., Schmidt H., Schwab W. Substrate promiscuity of RdCCD1, a carotenoid cleavage oxygenase from Rosa damascena. Phytochemistry 2009, 70:457-464.
27. Huang F.-C., Molnar P., Schwab W. Cloning and functional characterization of carotenoid cleavage dioxygenase 4 genes. J. Exp. Bot. 2009, 60:3011-3022.
28. Isaacson T., Ronen G., Zamir D., Hirschberg J. Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of β-carotene and xanthophylls in plants. Plant Cell 2002, 14:333-342.
29. Isaacson T., Ohad I., Beyer P., Hirschberg J. Analysis in vitro of the enzyme CRTISO establishes a poly-cis-carotenoid biosynthesis pathway in plants. Plant Physiol. 2004, 136:4246-4255.
30. Jeknić Z., Morré J.T., Jeknić S., Jevremović S., Subotić A., Chen T.H.H. Cloning and functional characterization of a gene for capsanthin/capsorubin synthase from tiger lily (Lilium lancifolium Thunb 'Splendens'). Plant Cell Physiol. 2012, 53:1899-1912.
31. Kachanovsky D.E., Filler S., Isaacson T., Hirschberg J. Epistasis in tomato color mutations involves regulation of Phytoene synthase 1 expression by cis-carotenoids. PNAS 2012, 109:19021-19026.
32. Kaiser R. Carotenoid-derived aroma compounds in flower scents. ACS Symposium Series 802 2001, 160-182. American Chemical Society, Washington, DC. P. Winterhalter, R.L. Rouseff (Eds.).
33. Kim J., DellaPenna D. Defining the primary route for lutein synthesis in plants: the role of Arabidopsis carotenoid β-ring hydroxylase CYP97A3. PNAS 2006, 103:3474-3479.
34. Kim J., Smith J.J., Tian L., DellaPenna D. The evolution and function of carotenoid hydroxylases in Arabidopsis. Plant Cell Physiol. 2009, 50:463-479.
35. Kishimoto S., Maoka T., Nakayama M., Ohmiya A. Carotenoid composition in petals of chrysanthemum (Dendranthema grandiflorum (Ramat.) Kitamura). Phytochemistry 2004, 65:2781-2787.
36. Kishimoto S., Maoka T., Sumitomo K., Ohmiya A. Analysis of carotenoid composition in petals of calendula (Calendula officinalis L.). Biosci. Biotechnol. Biochem. 2005, 69:2122-2128.
37. Kishimoto S., Ohmiya A. Regulation of carotenoid biosynthesis in petals and leaves of chrysanthemum (Chrysanthemum morifolium Ramat.). Physiol. Plant. 2006, 128:437-447.
38. Kishimoto S., Sumitomo K., Yagi M., Nakayama M., Ohmiya A. Three routes to orange petal color via carotenoid component in 9 Compositae species. J. Jpn. Soc. Hort. Sci. 2007, 76:250-257.
39. Kishimoto S., Ohmiya A. Carotenoid isomerase is a key determinant of the petal color of Calendula officinalis. J. Biol. Chem. 2012, 287:276-285.
40. Leitner-Dagan Y., Ovadis M., Shklarman E., Elad Y., David D.R., Vainstein A. Expression and functional analyses of the plastid lipid-associated protein CHRC suggest its role in chromoplastogenesis and stress. Plant Physiol. 2006, 142:233-244.
41. Li F., Murillo C., Wurtzel E.T. Maize Y9 encodes a product essential for 15-cis-δ-carotene isomerization. Plant Physiol. 2007, 144:1181-1189.
42. Li L., Paolillo D.J., Parthasarathy M.V., DiMuzio E.M., Garvin D.F. A novel gene mutation that confers abnormal patterns of β-carotene accumulation in cauliflower (Brassica oleracea var. botrytis). Plant J. 2001, 26:59-67.
43. Li L., Yang Y., Xu Q., Owsiany K., Welsch R., Chitchumroonchokchai C., Lu S., Eck J.V., Deng X-X., Failla M., Thannhauser T.W. The Or gene enhances carotenoid accumulation and stability during post-harvest storage of potato tubers. Mol. Plant 2012, 5:339-352.
44. Liu H., Kishimoto S., Yamamizo C., Fukuta N., Ohmiya A. Carotenoid accumulations and carotenogenic gene expressions in the petals of Eustoma grandiflorum. Plant Breed. 2013, 10.1111/pbr.12043.
45. Liu Y., Roof S., Ye Z., Barry C., Tuinen A., Vrebalov J., Bowler C., Giovannoni J. Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. PNAS 2004, 101:9897-9902.
46. Lopez A.B., Van Eck J., Conlin B.J., Paolillo D.J., O'Neill J., Li L. Effect of the cauliflower Or transgene on carotenoid accumulation and chromoplast formation in transgenic potato tubers. J. Exp. Bot. 2008, 59:213-223.
47. Lu S., Van Eck J., Zhou X., Lopez A.B., O'Halloran D.M., Cosman K.M., Conlin B.J., Polillo D.J., Garvin D.F., Vrebalov J., Kochian L.V., Küpper H., Earle E.D., Cao J., Li L. The cauliflower Or gene encodes a DnaJ cysteine-rich domain-containing protein that mediates high levels of β-carotene accumulation. Plant Cell 2006, 18:3594-3605.
48. Machin B., Scope N. Breeding and selection. Chrysanthemums: Year-Round Growing 1978, 30-39. Blandford Press, Dorset, UK.
49. Misawa N., Satomi Y., Kondo K., Yokoyama A., Kajiwara S., Saito T., Ohtani T., Miki W. Structure and functional analysis of a marine bacterial carotenoid biosynthesis gene cluster and astaxanthin biosynthetic pathway proposed at the gene level. J. Bacteriol. 1995, 177:6575-6584.
50. Misawa N. Pathway engineering of plants toward astaxanthin production. Plant Biotechnol. 2009, 26:93-99.
51. Moehs C.P., Tian L., Osteryoung K.W., DellaPenna D. Analysis of carotenoid biosynthetic gene expression during marigold petal development. Plant Mol. Biol. 2001, 45:281-293.
52. Nakayama M., Miyasaka M., Maoka T., Yagi M., Fukuta N. A carotenoid-derived yellow Eustoma screened under blue and ultraviolet lights. J. Jpn. Soc. Hort. Sci. 2006, 75:161-165.
53. Nambara E., Marion-Poll A. Abscisic acid biosynthesis and catabolism. Annu. Rev. Plant Biol. 2005, 56:165-185.
54. Nielsen K.M., Lewis D.H., Morgan E.R. Characterization of carotenoid pigments and their biosynthesis in two yellow flowered lines of Sandersonia aurantiaca (Hook). Euphytica 2003, 130:25-34.
55. Niyogi K. Safety valves for photosynthesis. Curr. Opin. Plant Biol. 2000, 3:455-460.
56. Ohmiya A., Kishimoto S., Aida R., Yoshioka S., Sumitomo K. Carotenoid cleavage dioxygenase (CmCCD4a) contributes to white color formation in chrysanthemum petals. Plant Physiol. 2006, 142:1193-1201.
57. Ohmiya A., Sumitomo K., Aida R. Yellow Jimba: suppression of carotenoid cleavage dioxygenase (CmCCD4a) expression turns white chrysanthemum petals yellow. J. Jpn. Soc. Hort. Sci. 2009, 78:450-455.
58. Ohmiya A. Carotenoid cleavage dioxygenases and their apocarotenoid products in plants. Plant Biotechnol. 2009, 26:351-358.
59. Ohmiya A. Diversity of carotenoid composition in flower petals. Jpn. Agric. Res. Q. (JARQ) 2011, 45:163-171.
60. Ohmiya A., Toyoda T., Watanabe H., Emoto K., Hase Y., Yoshioka S. Mechanism behind petal color mutation induced by heavy-ion-beam irradiation of recalcitrant chrysanthemum cultivar. J. Jpn. Soc. Hort. Sci. 2012, 81:269-274.
61. Ohmiya, A., Tanase, K., Hirashima, M., Yamamizo, C., Yagi, M., 2013. Analysis of carotenogenic gene expression in petals and leaves of carnation (Dianthus caryophyllus L.). Plant Breed, doi:10.1111/pbr.12061, in press.
62. Ootani S., Hayashi K. Further search for water-soluble carotenoids in yellow flowers of several plants. Res. Inst. Evolut. Biol. Sci. Rep. 1982, 1:71-76. (in Japanese with English abstract).
63. Paolillo D.J., Garvin D.F., Parthasarathy M.V. The chromoplasts of Or mutants of cauliflower (Brassica oleracea L. var. botrytis). Protoplasma 2004, 224:245-253.
64. Park H., Kreunen S.S., Cuttriss A.J., DellaPenna D., Pogson B.J. Identification of the carotenoid isomerase provides insight into carotenoid biosynthesis, prolamellar body formation, and photomorphogenesis. Plant Cell 2002, 14:321-332.
65. Pecker I., Gabbay R., Cunningham F.X., Hirschberg J. Cloning and characterization of the cDNA for lycopene β-cyclase from tomato reveals decrease in its expression during fruit ripening. Plant Mol. Biol. 1996, 30:807-819.
66. Pyke K.A., Howells C.A. Plastid and stromule morphogenesis in tomato. Ann. Bot. 2002, 90:559-566.
67. Ro D.-K. Terpenoid biosynthesis. Plant Metabolism and Biotechnology 2011, 217-240. John Wiley & Sons, Ltd, West Sussex, UK. A. Crozier, H. Ashihara (Eds.).
68. Rodríguez-Villalón A., Gas E., Rodríguez-Concepción M. Phytoene synthase activity controls the biosynthesis of carotenoids and the supply of their metabolic precursors in dark-grown Arabidopsis seedlings. Plant J. 2009, 60:424-435.
69. Romer S., Hugueney P., Bouvier F., Camara B., Kuntz M. Expression of the genes encoding the early carotenoid biosynthetic-enzymes in Capsicum annuum. Biochem. Biophys. Res. Commun. 1993, 196:1414-1421.
70. Ronen G., Carmel-Goren L., Zamir D., Hirschberg J. An alternative pathway to β-carotene formation in plant chromoplasts discovered by map-based cloning of beta and old-gold color mutations in tomato. PNAS 2000, 97:11102-11107.
71. Rubio A., Rambla J.L., Santaella M., Gómez M.D., Orzaez D., Granell A., Gómez-Gómez L. Cytosolic and plastoglobule-targeted carotenoid dioxygenases from Crocus sativus are both involved in β-ionone release. J. Biol. Chem. 2008, 283:24816-24825.
72. Ruiz-Sola M.Á., Rodríguez-Concepción M. Carotenoid biosynthesis in Arabidopsis: a colorful pathway. The Arabidopsis Book 2012, vol. 10:e0158. http://dx.doi.org/10.1199/tab.0158.
73. Sakuta M., Ohmiya A. Pigment biosynthesis II: betacyanins and carotenoids. Plant Metabolism and Biotechnology 2011, 343-371. John Wiley & Sons, Ltd, West Sussex, UK. A. Crozier, H. Ashihara (Eds.).
74. Schledz M., Al-Babili S., von Lintig J., Haubruck H., Rabbani S., Kleinig H., Beyer P. Phytoene synthase from Narcissus pseudonarcissus: functional expression, galactolipid requirement, topological distribution in chromoplasts and induction during flowering. Plant J. 1996, 10:781-792.
75. Simkin A.J., Schwartz S.H., Auldridge M., Taylor M.G., Klee H.J. The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles β-ionone, pseudoionone, and geranylacetone. Plant J. 2004, 40:882-892.
76. Simkin A.J., Underwood B.A., Auldridge M., Loucas H.M., Shibuya K., Schmelz E., Clark D.G., Klee H.J. Circadian regulation of the PhCCD1 carotenoid cleavage dioxygenase controls emission of β-ionone, a fragrance volatile of petunia flowers. Plant Physiol. 2004, 136:3504-3514.
77. Singh D.K., McNellis T.W. Fibrillin protein function: the tip of the iceberg?. Trends Plant Sci. 2011, 16:432-441.
78. Smith M., Butler R.D. Ultrastructural aspects of petal development in Cucumis sativus with particular reference to the chromoplasts. Protoplasma 1971, 73:1-13.
79. Suzuki S., Nishihara M., Nakatsuka T., Misawa N., Ogiwara I., Yamamura S. Flower color alteration in Lotus japonicus by modification of the carotenoid biosynthetic pathway. Plant Cell Rep. 2007, 26:951-959.
80. Tan B.C., Joseph L.M., Deng W.T., Liu L., Li Q.B., Cline K., McCarty D.R. Molecular characterization of the Arabidopsis 9-cis-epoxycarotenoid dioxygenase gene family. Plant J. 2003, 35:44-56.
81. Tanaka Y., Sasaki N., Ohmiya A. Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J. 2008, 54:733-749.
82. Tanase K., Nishitani C., Hirakawa H., Isobe S., Tabata S., Ohmiya A., Onozaki T. Transcriptome analysis of carnation (Dianthus caryophyllus L.) based on next-generation sequencing technology. BMC Genet. 2012, 11:24.
83. Tanikawa N., Yamamizo C., Ohmiya A. Carotenoid components in petals of yellow-flowered Camellia species. Bull. Natl. Inst. Flor. Sci. 2010, 10:75-79. (in Japanese with English abstract).
84. Tian L., Musetti V., Kim J., Magallanes-Lundback M., DellaPenna D. The Arabidopsis LUT1 locus encodes a member of the cytochrome P450 family that is required for carotenoid e-ring hydroxylation activity. PNAS 2004, 101:402-407.
85. Vishnevetsky M., Ovadis M., Vainstein A. Carotenoid sequestration in plants: the role of carotenoid-associated proteins. Trends Plant Sci. 1999, 4:232-235.
86. Wakelin A.M., Lister C.E., Conner A.J. Inheritance and biochemistry of pollen pigmentation in California poppy (Eschscholzia californica Cham.). Int. J. Plant Sci. 2003, 164:867-875.
87. Welsch R., Maass D., Voegel T., DellaPenna D., Beyer P. Transcription factor RAP2. 2 and its interacting partner SINAT2: stable elements in the carotenogenesis of Arabidopsis leaves. Plant Physiol. 2007, 145:1073-1085.
88. Welsch R., Wust F., Bǎr C., Al-Babili S., Beyer P. A third phytoene synthase is devoted to abiotic stress-induced abscisic acid formation in rice and defines functional diversification of phytoene synthase genes. Plant Physiol. 2008, 147:367-380.
89. Yamagishi M., Kishimoto S., Nakayama M. Carotenoid composition and changes in expression of carotenoid biosynthetic genes in tepals of Asiatic hybrid lily. Plant Breed. 2009, 128:172-177.
90. Yamamizo C., Kishimoto S., Ohmiya A. Carotenoid composition and carotenogenic gene expression during Ipomoea petal development. J. Exp. Bot. 2010, 61:709-719.
91. Yoshioka S., Aida R., Yamamizo C., Shibata M., Ohmiya A. The carotenoid cleavage dioxygenase 4 (CmCCD4a) gene family encodes a key regulator of petal color mutation in chrysanthemum. Euphytica 2012, 184:377-387.
92. Ytterberg A.J., Peltier J., van Wijk K.J. Protein profiling of plastoglobules in chloroplasts and chromoplasts: a surprising site for differential accumulation of metabolic enzymes. Plant Physiol. 2006, 140:984-997.
93. Zhu C., Yamamura S., Koiwa H., Nishihara M., Sandmann G. cDNA cloning and expression of carotenogenic genes during flower development in Gentiana lutea. Plant Mol. Biol. 2002, 48:277-285.
94. Zhu C., Yamamura S., Nishihara M., Koiwa H., Sandmann G. cDNA for the synthesis of cyclic carotenoids in petals of Gentiana lutea and their regulation during flower development. Biochim. Biophys. Acta 2003, 1625:305-308.
95. Zhu C., Naqvi S., Capell T., Christou P. Metabolic engineering of ketocarotenoid biosynthesis in higher plants. Arch. Biochem. Biophys. 2009, 483:182-190.
96. Zhu C., Bai C., Sanahuja G., Yuan D., Farré G., Naqvi S., Shi L., Capell T., Christou P. The regulation of carotenoid pigmentation in flowers. Arch. Biochem. Biophys. 2010, 504:132-141.