Browse > Article
http://dx.doi.org/10.7235/hort.2012.11116

Carotenoid Metabolic Engineering in Flowering Plants  

Ha, Sun-Hwa (National Academy of Agricultural Science, Rural Development Administration)
Jeong, Ye-Sol (National Academy of Agricultural Science, Rural Development Administration)
Lim, Sun-Hyung (National Academy of Agricultural Science, Rural Development Administration)
Kim, Jae-Kwang (National Academy of Agricultural Science, Rural Development Administration)
Lee, Dong-Ho (School of Life Sciences and Biotechnology, Korea University)
Lee, Jong-Yeol (National Academy of Agricultural Science, Rural Development Administration)
Kim, Young-Mi (National Academy of Agricultural Science, Rural Development Administration)
Publication Information
Horticultural Science & Technology / v.30, no.2, 2012 , pp. 107-122 More about this Journal
Abstract
In plants, color is a powerful tool to attract insects and herbivores which act as pollinators and vehicles of seed dispersion. In particular, flower color has held key post for human with aesthetic value. Horticultural industry has developed methods to produce new and attractive color varieties in flowering plants. Carotenoids are one of the main pigments being responsible for red, orange, and yellow colors. Their biosynthetic pathway has been considered as a major target of metabolic engineering for color modification of flowers and fruits. Here, we review the diverse efforts to modify pigment phenotype by the control of carotenogenic gene expression and enzyme levels. Recent reports about regulating degradation and storage of carotenoids will be also summarized to help the creation of engineered flower with novel color phenotype which is not existed in nature.
Keywords
apocarotenoid; chromoplast; flower color; ketocarotenoid; natural pigment; terpenoid;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Corona, V., B. Aracri, G. Kosturkova, G.E. Bartley, L. Pitto, L. Giorgetti, P.A. Scolnik, and G. Giuliano. 1996. Regulation of a carotenoid biosynthesis gene promoter during plant development. Plant J. 9:505-512.   DOI
2 Cunningham, F.X. Jr. and E. Gantt. 2005. A study in scarlet: Enzymes of ketocarotenoid biosynthesis in the flowers of Adonis aestivalis. Plant J. 41:478-492.   DOI
3 Dalal, M., V. Chinnusamy, and K.C. Bansal. 2010. Isolation and functional characterization of lycopene ${\beta}$-cyclase (CYC-B) promoter from Solanum habrochaites. BMC Plant Biol. 10:61.   DOI
4 Del Villar-Martinez, A.A., P.A. Garcia-Saucedo, A. Carabez-Trejo, A. Cruz-Hernandez, and O. Paredes-Lopez. 2005. Carotenogenic gene expression and ultrastructural changes during development in marigold. J. Plant Physiol. 162:1046-1056.   DOI
5 Deli, J., P. Molnar, Z. Matus, G. Toth, A. Steck, and H. Pfander. 1998. Isolation and characterization of 3,5,6-trihydroxy-carotenoids from petals of Lilium tigrinum. Chromatographia 48:27-31.   DOI
6 Demmig-Adams, B. and W.W. Adams III. 2002. Antioxidants in photosynthesis and human nutrition. Science 298:2149-2153.   DOI
7 Eisenreich, W., F. Rohdich, and A. Bacher. 2001. Deoxyxylulose phosphate pathway to terpenoids. Trends Plant Sci. 6:78-84.   DOI
8 Bird, C.R., J.A. Ray, J.D. Fletcher, J.M. Boniwell, A.S. Bird, C. Teulieres, I. Blain, P.M. Bramley, and W. Schuch. 1991. Using antisense RNA to study gene function: Inhibition of carotenoid biosynthesis in transgenic tomatoes. Bio/Technology 9:635-639.   DOI
9 Bramley, P.M. 2002. Regulation of carotenoid formation during tomato fruit ripening and development. J. Exp. Bot. 53:2107-2113.   DOI
10 Breitenbach, J. and G. Sandmann. 2005. ${\zeta}$-carotene cis isomers as products and substrates in the plant poly-cis carotenoid biosynthetic pathway to lycopene. Planta 220:785-793.   DOI
11 Bonk, M., M. Tadros, J. Vandekerckhove, S. Al-Babili, and P. Beyer. 1996. Purification and characterization of chaperonin 60 and heat-shock protein 70 from chromoplasts of Narcissus pseudonarcissus (Involvement of heat-shock protein 70 in a soluble protein complex containing phytoene desaturase). Plant Physiol. 111:931-939.   DOI
12 Bouvier, F., P. Hugueney, A. d'Harlingue, M. Kuntz, and B. Camara. 1994. Xanthophyll biosynthesis in chromoplasts: Isolation and molecular cloning of an enzyme catalyzing the conversion of 5,6-epoxycarotenoid into ketocarotenoid. Plant J. 6:45-54.   DOI
13 Bouvier, F., Y. Keller, A. d'Harlingue, and B. Camara. 1998. Xanthophyll biosynthesis: Molecular and functional characterization of carotenoid hydroxylases from pepper fruits (Capsicum annuum L.). Biochim. Biophys. Acta 1391:320-328.   DOI
14 Bouvier, F., C. Suire, J. Mutterer, and B. Camara. 2003. Oxidative remodeling of chromoplast carotenoids: Identification of the carotenoid dioxygenase CsCCD and CsZCD genes involved in Crocus secondary metabolite biogenesis. Plant Cell 15:47-62.   DOI
15 Castillo, R., J.A. Fernandez, and L. Gomez-Gomez. 2005. Implications of carotenoid biosynthetic genes in apocarotenoid formation during the stigma development of Crocus sativus and its closer relatives. Plant Physiol. 139:674-689.   DOI
16 Ahrazem, O., A. Rubio-Moraga, R.C. Lopez, and L. Gomez-Gomez. 2010. The expression of a chromoplast-specific lycopene beta cyclase gene is involved in the high production of saffron's apocarotenoid precursors. J. Exp. Bot. 61:105-119.   DOI
17 Beyer, P., M. Mayer, and H. Kleinig. 1989. Molecular oxygen and the state of geometric isomerism of intermediates are essential in the carotene desaturation and cyclization reactions in daffodil chromoplasts. Eur. J. Biochem. 184:141-150.   DOI
18 Al-Babili, S., J. von Lintig, H. Haubruck, and P. Beyer. 1996. A novel, soluble form of phytoene desaturase from Narcissus pseudonarcissus chromoplasts is Hsp70-complexed and competent for flavinylation, membrane association and enzymatic activation. Plant J. 9:601-612.   DOI
19 Al-Babili, S., P. Hugueney, M. Schledz, R. Welsch, H. Frohnmeyer, O. Laule, and P. Beyer. 2000. Identification of a novel gene coding for neoxanthin synthase from Solanum tuberosum. FEBS Lett. 485:168-172.   DOI
20 Bartley, G.E. and P.A. Scolnik. 1995. Plant carotenoids: Pigments for photoprotection, visual attraction, and human health. Plant Cell 7:1027-1038.   DOI
21 Zhu, C., S. Yamamura, M. Nishihara, H. Koiwa, and G. Sandmann. 2003. cDNAs for the synthesis of cyclic carotenoids in petals of Gentiana lutea and their regulation during flower development. Biochem. Biophys. Acta 1625:305-308.
22 Yu, B., D.J. Lydiate, U.A. Schafer, and A. Hannoufa. 2007. Characterization of a ${\beta}$-carotene hydroxylase of Adonis aestivalis and its expression in Arabidopsis thaliana. Planta 226:181-192.   DOI
23 Zhong, Y.J., J.C. Huang, J. Liu, Y. Li, Y. Jiang, Z.F. Xu, G. Sandmann, and F. Chen. 2011. Functional characterization of various algal carotenoid ketolases reveals that ketolating zeaxanthin efficiently is essential for high production of astaxanthin in transgenic. J. Exp. Bot. 62:3659-3669.   DOI
24 Zhu, C., S. Yamamura, H. Koiwa, M. Nishihara, and G. Sandmann. 2002. cDNA cloning and expression of carotenogenic genes during flower development in Gentiana lutea. Plant Mol. Biol. 48:277-285.   DOI
25 Zhu, C., T. Gerjets, and G. Sandmann. 2007. Nicotiana glauca engineered for the production of ketocarotenoids in flowers and leaves by expressing the cyanobacterial crtO ketolase gene. Transgenic Res. 16:813-821.   DOI
26 Valadon, L.R.G. and R.S. Mummery. 1968. Carotenoids in floral parts of a narcissus, a daffodil and a tulip. Biochem. J. 106:479-484.   DOI
27 Tanaka, Y., N. Sasaki, and A. Ohmiya. 2008. Biosynthesis of plant pigments: Anthocyanins, betalains and carotenoids. Plant J. 54:733-749.   DOI
28 Tandon, J.S., S.B. Katti, P. Ruedi, and C.H. Eugster. 1979. Crocetin-dialdehyde from Coleus forskohlii BRIQ., Labiatae. Helv. Chim. Acta 62:2706-2707.   DOI
29 Umehara, M., A. Hanada, S. Yoshida, K. Akiyama, T. Arite, N. Takeda-Kamiya, H. Magome, Y. Kamiya, K. Shirasu, K. Yoneyama, J. Kyozuka, and S. Yamaguchi. 2008. Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195-200.   DOI
30 Vishnevetsky, M., M. Ovadis, H. Itzhaki, and A. Vainstein. 1997. CHRC, encoding a chromoplast-specific carotenoid-associated protein, is an early gibberellic acid-responsive gene. J. Biol. Chem. 272:24747-24750.   DOI
31 Vishnevetsky, M., M. Ovadis, and A. Vainstein. 1999a. Carotenoid sequestration in plants: The role of carotenoid associated proteins. Trends Plant Sci. 4:232-235.   DOI
32 Vishnevetsky, M., M. Ovadis, A. Zuker, and A. Vainstein. 1999b. Molecular mechanisms underlying carotenogenesis in the chromoplast: Multilevel regulation of carotenoid-associated genes. Plant J. 20:423-431.   DOI
33 Von Lintig, J. and K. Vogt. 2004. Vitamin a formation in animals: molecular identification and functional characterization of carotene cleaving enzymes. J. Nutr. 134:251S-256S.   DOI
34 Schledz, M., S. Al-Babili, J. Von Lintig, H. Haubruck, S. Rabbani, H. Kleinig, and P. Beyer. 1996. Phytoene synthase from Narcissus pseudonarcissus: Functional expression, galactolipid requirement, topological distribution in chromoplasts and induction during flowering. Plant J. 10:781-792.   DOI
35 Yamagishi, M., S. Kishimoto, and M. Nakayama. 2010. Carotenoid composition and changes in expression of carotenoid biosynthetic genes in tepals of asiatic hybrid lily. Plant Breed. 129:100-107.   DOI
36 Yamamizo, C., S. Kishimoto, and A. Ohmiya. 2010. Carotenoid composition and carotenogenic gene expression during Ipomoea petal development. J. Exp. Bot. 61:709-719.   DOI
37 Seybold, A. and T.W. Goodwin. 1959. Occurrence of astaxanthin in the flower petals of Adonis Annua L. Nature 184:1714-1715.   DOI
38 Schwartz, S.H., B.C. Tan, D.A. Gage, J.A. Zeevaart, and D.R. McCarty. 1997. Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872-1874.   DOI
39 Schwartz, S.H., X. Qin, and J.A. Zeevaart. 2003. Elucidation of the indirect pathway of abscisic acid biosynthesis by mutants, genes, and enzymes. Plant Physiol. 131:1591-1601.   DOI
40 Scott, M.I., I. Ascarelli, and G. Olson. 1968. Studies of egg yolk pigmentation. Poult. Sci. 47:863.   DOI
41 Simkin, A.J., S.H. Schwartz, M. Auldridge, M.G. Taylor, and H.J. Klee. 2004. Circadian regulation of the PhCCD1 carotenoid cleavage dioxygenase controls emission of ${\beta}$-Ionone, a fragrance volatile of petunia flowers. Plant J. 40:882-892.   DOI
42 Smirra, I., A.H. Halevy, and A. Vainstein. 1993. Isolation and characterization of a chromoplast-specific carotenoid-associated protein from Cucumis sativus corollas. Plant Physiol. 102:491-496.   DOI
43 Pfander, H. 1992. Carotenoids part A: Chemistry, separation, quantitation, and antioxidation. Methods Enzymology 213:3-13.   DOI
44 Suzuki, S., M. Nishihara, T. Nakatsuka, N. Misawa, I. Ogiwara, and S. Yamamura. 2007. Flower color alteration in Lotus japonicus by modification of the carotenoid biosynthetic pathway. Plant Cell Rep. 26:951-959.   DOI
45 Tarantilis, P.A., M. Polissiou, and M. Manfait. 1994. Separation of picrocrocin, cis-trans-crocins and safranal of saffron using high-performance liquid chromatography with photodiode-array detection. J. Chromatogr. 664:55-61.   DOI
46 Tan, B.C., S.H. Schwartz, J.A. Zeevaart, and D.R. McCarty. 1997. Genetic control of abscisic acid biosynthesis in maize. Proc. Natl Acad. Sci. USA 94:12235-12240.   DOI
47 Pfander, H. and H. Schurtenberger. 1982. Biosynthesis of $C_{20}$-carotenoids in Crocus sativus. Phytochemistry 21:1039-1042.   DOI
48 Ralley, L., E.M. Enfissi, N. Misawa, W. Schuch, P.M. Bramley, and P.D. Fraser. 2004. Metabolic engineering of ketocarotenoid formation in higher Plants. Plant J. 39:477-486.   DOI
49 Rodrıguez-Concepción, M. and A. Boronat. 2002. Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol. 130:1079-1089.   DOI
50 Rohdich, F., F. Zepeck, P. Adam, S. Hecht, J. Kaiser, R. Laupitz, T. Grawert, S. Amslinger, W. Eisenreich, A. Bacher, and D. Arigoni. 2003. The deoxyxylulose phosphate pathway of isoprenoid biosynthesis: Studies on the mechanisms of the reactions catalyzed by IspG and IspH protein. PNAS 100: 1586-1591.   DOI
51 Ronen, G., L. Carmel-Goren, D. Zamir, and J. Hirschberg. 2000. An alternative pathway to ${\beta}$-carotene formation in plant chromoplasts discovered by map-based cloning of Beta and old-gold color mutations in tomato. Proc. Natl Acad. Sci. USA 97:11102-11107.   DOI
52 Lopez, A.B., J. Van Eck, B.J. Conlin, D.J. Paolillo, J. O'Neill, and L. Li. 2008. Effect of the cauliflower Or transgene on carotenoid accumulation and chromoplast formation in transgenic potato. J. Exp. Bot. 59:213-223.   DOI
53 Rubio, A., P.F. Nohales, J.A. Perez, and L. Gomez-Gomez. 2004. Glucosylation of the saffron apocarotenoid crocetin by a glucosyltransferase isolated from Crocus sativus stigmas. Planta 219:955-966.   DOI
54 Rubio, A., J.L. Rambla, M. Santaella, M.D. Gomez, D. Orzaez, A. Granell, and L. Gomez-Gomez. 2008. Cytosolic and plastoglobule-targeted carotenoid dioxygenases from Crocus sativus are both involved in ${\beta}$-ionone release. J. Biol. Chem. 283:24816-24825.   DOI
55 Rubio, A., J.L. Rambla, O. Ahrazem, A. Granell, and L. Gomez-Gomez. 2009. Metabolite and target transcript analyses during Crocus sativus stigma development. Phytochemistry 70:1009-1016.   DOI
56 Lotan, T. and J. Hirschberg. 1995. Cloning and expression in Escherichia coli of the gene encoding ${\beta}$-C-4-oxygenase, that converts ${\beta}$-carotene to the ketocarotenoid canthaxanthin in Haematococcus pluvialis. FEBS Lett. 364:125-128.   DOI
57 Lu, S., J. Van Eck, X. Zhou, A.B. Lopez, D.M. O'Halloran, K.M. Cosman, B.J. Conlin, D.J. Paolillo, D.F. Garvin, J. Vrebalov, L.V. Kochian, H. Kupper, E.D. Earle, J. Cao, and L. Li. 2006. The cauliflower Or gene encodes a DnaJ cysteine-rich domaincontaining protein that mediates high levels of ${\beta}$-carotene accumulation. Plant Cell 18:3594-3605.   DOI
58 Mann, V., M. Harker, I. Pecker, and J. Hirschberg. 2000. Metabolic engineering of astaxanthin production in tobacco flowers. Nat. Biotechnol. 18:888-892.   DOI
59 Misawa, N., M.R. Truesdale, G. Sandmann, P.D. Fraser, C. Bird, W. Schuch, and P.M. Bramley. 1994. Expression of a tomato cDNA coding for phytoene synthase in Escherichia coli, phytoene formation in vivo and in vitro, and functional analysis of the various truncated gene products. J. Biochem. 116:980-985.   DOI
60 Moehs, C.P., L. Tian, K.W. Osteryoung, and D. DellaPenna. 2001. Analysis of carotenoid biosynthetic gene expression during marigold petal development. Plant Mol. Biol. 45:281-293.   DOI
61 Ohmiya, A., S. Kishimoto, R. Aida, S. Yoshioka, and K. Sumitomo. 2006. Carotenoid cleavage dioxygenase (CmCCD4a) contributes to white color formation in chrysanthemum petals. Plant Physiol. 142:1193-1201.   DOI
62 Ohmiya, A. 2009. Carotenoid cleavage dioxygenases and their apocarotenoid products in plants. Plant Biotechnol. 26:351-358.   DOI
63 Pecker, I., R. Gabbay, F.X. Cunningham Jr., and J. Hirschberg. 1996. Cloning and characterization of the cDNA for lycopene beta-cyclase from tomato reveals decrease in its expression during fruit ripening. Plant Mol. Biol. 30:807-819.   DOI
64 Ji, J., G. Wang, J. Wang, and P. Wang. 2009. Functional analysis of multiple carotenogenic genes from Lycium barbarum and Gentiana lutea L. for their effects on ${\beta}$-carotene production in transgenic tobacco. Biotechnol. Lett. 31:305-312.   DOI
65 Katsumoto, Y., M. Fukuchi-Mizutani, Y. Fukui, F. Brugliera, T.A. Holton, M. Karan, N. Nakamura, K. Yonekura-Sakakibara, J. Togami, A. Pigeaire, G.Q. Tao, N.S. Nehra, C.Y. Lu, B.K. Dyson, S. Tsuda, T. Ashikari, T. Kusumi, J.G. Mason, and Y. Tanaka. 2007. Engineering of the rose flavonoid biosynthetic pathway successfully generated blue-hued flowers accumulating delphinidin. Plant Cell Physiol. 48:1589-1600.   DOI
66 Kishimoto, S., T. Maoka, M. Nakayama, and A. Ohmiya. 2004. Carotenoid composition in petals of chrysanthemum (Dendranthema grandiflorum (Ramat.) Kitamura). Phytochemistry 65:2781-2787.   DOI
67 Kishimoto, S. and A. Ohmiya. 2006. Regulation of carotenoid biosynthesis in petals and leaves of chrysanthemum (Chrysanthemum morifolium). Physiol. Plant 128:436-447.   DOI
68 Leitner-Dagan, Y., M. Ovadis, A. Zuker, E. Shklarman, I. Ohad, T. Tzfira, and A. Vainstein. 2006b. CHRD, a plant member of the evolutionarily conserved YjgF family, influences photosynthesis and chromoplastogenesis. Planta 225:89-102.   DOI
69 Langton, F.A. 1980. Chimerical structure and carotenoid inheritance in Chrysanthemum morifolium (Ramat.). Euphytica 29:807-812.   DOI
70 Leitner-Dagan, Y., M. Ovadis, E. Shklarman, Y. Elad, D. Rav David, and A. Vainstein. 2006a. Expression and functional analyses of the plastid lipid-associated protein CHRC suggest its role in chromoplastogenesis and stress. Plant Physiol. 142:233-244.   DOI
71 Libal-Weksler, Y., M. Vishnevetsky, M. Ovadis, and A. Vainstein. 1997. Isolation and regulation of accumulation of a minor chromoplast-specific protein from cucumber corollas. Plant Physiol. 113:59-63.   DOI
72 Liedvogel, B. and H. Kleinig. 1977. Lipid metabolism in chromoplast membranes from the daffodil: glycosylation and acylation. Planta 133:249-253.   DOI
73 Fraser, P.D., H. Shimada, and N. Misawa. 1998. Enzymic confirmation of reactions involved in routes to astaxanthin formation, elucidated using a direct substrate in vitro assay. Eur. J. Biochem. 252:229-236.   DOI
74 Galpaz, N., G. Ronen, Z. Khalfa, D. Zamir, and J. Hirschberg. 2006. A Chromoplast-specific carotenoid biosynthesis pathway is revealed by cloning of the tomato white-flower locus. Plant Cell 18:1947-1960.   DOI
75 Gerjets, T., M. Sandmann, C. Zhu, and G. Sandmann. 2007. Metabolic engineering of ketocarotenoid biosynthesis in leaves and flowers of tobacco species. Biotechnol. J. 2:1263-1269.   DOI
76 Gomez-Roldan, V., S. Fermas, P.B. Brewer, V. Puech-Pages, E.A. Dun, J.P. Pillot, F. Letisse, R. Matusova, S. Danoun, J.C. Portais, H. Bouwmeester, G. Becard, C.A. Beveridge, C. Rameau, and S.F. Rochange. 2008. Strigolactone inhibition of shoot branching. Nature 455:189-194.   DOI
77 He, Y., C. Zhu, D. Wang, D. Kong, and J. Sun. 2002. Cloning of plastid division gene GlFtsZ from Gentiana lutea and its expression during petal development. Prog. Nat. Sci. 12:592-597.
78 Giuliano, G., G.E. Bartley, and P.A. Scolnik. 1993. Regulation of carotenoid biosynthesis during tomato development. Plant Cell 5:379-387.   DOI
79 Ha, S.H., J.B. Kim, J.S. Park, S.W. Lee, and K.J. Cho. 2007. A comparison of the carotenoid accumulation in Capsicum varieties that show different ripening colours: Deletion of the capsanthin-capsorubin synthase gene is not a prerequisite for the formation of a yellow pepper. J. Exp. Bot. 58:3135-3144.   DOI
80 Hattori, K. 1991. Inheritance of carotenoid pigmentation in flower color of chrysanthemum. Japan. J. Breed. 41:1-9.   DOI
81 Holloway, G.M. and J.L. Gainer. 1988. The carotenoid crocetin enhances pulmonary oxygenation. J. Appl. Physiol. 65:683-686.   DOI
82 Isaacson, T., I. Ohad, P. Beyer, and J. Hirschberg. 2004. Analysis in vitro of the enzyme CRTISO establishes a poly-cis-carotenoid biosynthesis pathway in plants. Plant Physiol. 136:4246-4255.   DOI
83 Chen, Y., F. Li, and E.T. Wurtzel. 2010. Isolation and characterization of the Z-ISO gene encoding a missing component of carotenoid biosynthesis in plants. Plant Physiol. 153:66-79.   DOI
84 Chiou, C.Y., K. Wu, and K.W. Yeh. 2008. Characterization and promoter activity of chromoplast specific carotenoid associated gene (CHRC) from Oncidium Gower Ramsey. Biotechnol. Lett. 30:1861-1866.   DOI
85 Chiou, C.Y., H.A. Pan, Y.N. Chuang, and K.W. Yeh. 2010. Differential expression of carotenoid-related genes determines diversified carotenoid coloration in floral tissues of Oncidium cultivars. Planta 232:937-948.   DOI