DOI QR코드

DOI QR Code

Carotenoid Metabolic Engineering in Flowering Plants

화색 변경을 위한 카로티노이드 대사공학

  • 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)
  • 하선화 (농촌진흥청 국립농업과학원 농업생명자원부) ;
  • 정예솔 (농촌진흥청 국립농업과학원 농업생명자원부) ;
  • 임선형 (농촌진흥청 국립농업과학원 농업생명자원부) ;
  • 김재광 (농촌진흥청 국립농업과학원 농업생명자원부) ;
  • 이동호 (고려대학교 생명과학대학 생명공학부) ;
  • 이종렬 (농촌진흥청 국립농업과학원 농업생명자원부) ;
  • 김영미 (농촌진흥청 국립농업과학원 농업생명자원부)
  • Received : 2011.09.28
  • Accepted : 2012.01.16
  • Published : 2012.04.30

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.

식물에서 화색은 종자를 퍼트리기 위해 꽃가루 매개충과 초식동물을 유인하는데 매우 중요한 도구이다. 사람에게 화색은 다채로운 시각적 다양성으로 큰 심미적 가치를 지님으로써 화훼산업의 발전은 새롭고 다양한 매력을 지닌 화색을 생산하는 방향으로 꾸준히 발전되어 왔다. 카로티노이드 성분은 화색 중에서 적색, 홍색, 황색을 나타내는 천연색소로서 이러한 카로티노이드 생합성 경로는 생명공학 기술을 이용하여 화색을 변화시키려는 대사공학의 주된 대상으로 여겨져 왔다. 본 총설에서는 카로티노이드 생합성 대사관련 유전자 발현 조절에 의한 색소 표현형의 변화를 소개하고자 하며, 최근 카로티노이드의 생합성을 넘어 절단과 축적 조절이 화색 변경을 위한 대표적인 기작으로 보고됨에 따라 다양한 화색만큼이나 다양한 조절 기작에 대한 현재까지의 지식을 총 동원하여 원하는 화색을 지닌 인공적인 꽃(engineered flower)을 생산하기 위한 전략을 종합해서 제시하고자 하였다.

Keywords

References

  1. 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. https://doi.org/10.1093/jxb/erp283
  2. 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. https://doi.org/10.1046/j.1365-313X.1996.9050601.x
  3. 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. https://doi.org/10.1016/S0014-5793(00)02193-1
  4. Bartley, G.E. and P.A. Scolnik. 1995. Plant carotenoids: Pigments for photoprotection, visual attraction, and human health. Plant Cell 7:1027-1038. https://doi.org/10.1105/tpc.7.7.1027
  5. 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. https://doi.org/10.1111/j.1432-1033.1989.tb15000.x
  6. 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. https://doi.org/10.1038/nbt0791-635
  7. Bramley, P.M. 2002. Regulation of carotenoid formation during tomato fruit ripening and development. J. Exp. Bot. 53:2107-2113. https://doi.org/10.1093/jxb/erf059
  8. 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. https://doi.org/10.1007/s00425-004-1395-2
  9. 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. https://doi.org/10.1104/pp.111.3.931
  10. 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. https://doi.org/10.1046/j.1365-313X.1994.6010045.x
  11. 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. https://doi.org/10.1016/S0005-2760(98)00029-0
  12. 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. https://doi.org/10.1105/tpc.006536
  13. 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. https://doi.org/10.1104/pp.105.067827
  14. 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. https://doi.org/10.1104/pp.110.153916
  15. 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. https://doi.org/10.1007/s10529-008-9767-5
  16. 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. https://doi.org/10.1007/s00425-010-1222-x
  17. 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. https://doi.org/10.1046/j.1365-313X.1996.09040505.x
  18. 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. https://doi.org/10.1111/j.1365-313X.2004.02309.x
  19. 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. https://doi.org/10.1186/1471-2229-10-61
  20. 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. https://doi.org/10.1016/j.jplph.2004.12.004
  21. 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. https://doi.org/10.1007/BF02467511
  22. Demmig-Adams, B. and W.W. Adams III. 2002. Antioxidants in photosynthesis and human nutrition. Science 298:2149-2153. https://doi.org/10.1126/science.1078002
  23. Eisenreich, W., F. Rohdich, and A. Bacher. 2001. Deoxyxylulose phosphate pathway to terpenoids. Trends Plant Sci. 6:78-84. https://doi.org/10.1016/S1360-1385(00)01812-4
  24. 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. https://doi.org/10.1046/j.1432-1327.1998.2520229.x
  25. 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. https://doi.org/10.1105/tpc.105.039966
  26. 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. https://doi.org/10.1002/biot.200700040
  27. 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. https://doi.org/10.1038/nature07271
  28. Giuliano, G., G.E. Bartley, and P.A. Scolnik. 1993. Regulation of carotenoid biosynthesis during tomato development. Plant Cell 5:379-387. https://doi.org/10.1105/tpc.5.4.379
  29. 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. https://doi.org/10.1093/jxb/erm132
  30. Hattori, K. 1991. Inheritance of carotenoid pigmentation in flower color of chrysanthemum. Japan. J. Breed. 41:1-9. https://doi.org/10.1270/jsbbs1951.41.1
  31. 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.
  32. Holloway, G.M. and J.L. Gainer. 1988. The carotenoid crocetin enhances pulmonary oxygenation. J. Appl. Physiol. 65:683-686. https://doi.org/10.1152/jappl.1988.65.2.683
  33. 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. https://doi.org/10.1104/pp.104.052092
  34. 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. https://doi.org/10.1007/s10529-008-9861-8
  35. 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. https://doi.org/10.1093/pcp/pcm131
  36. Kishimoto, S., T. Maoka, M. Nakayama, and A. Ohmiya. 2004. Carotenoid composition in petals of chrysanthemum (Dendranthema grandiflorum (Ramat.) Kitamura). Phytochemistry 65:2781-2787. https://doi.org/10.1016/j.phytochem.2004.08.038
  37. Kishimoto, S. and A. Ohmiya. 2006. Regulation of carotenoid biosynthesis in petals and leaves of chrysanthemum (Chrysanthemum morifolium). Physiol. Plant 128:436-447. https://doi.org/10.1111/j.1399-3054.2006.00761.x
  38. Langton, F.A. 1980. Chimerical structure and carotenoid inheritance in Chrysanthemum morifolium (Ramat.). Euphytica 29:807-812. https://doi.org/10.1007/BF00023228
  39. 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. https://doi.org/10.1104/pp.106.082404
  40. 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. https://doi.org/10.1007/s00425-006-0332-y
  41. 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. https://doi.org/10.1104/pp.113.1.59
  42. Liedvogel, B. and H. Kleinig. 1977. Lipid metabolism in chromoplast membranes from the daffodil: glycosylation and acylation. Planta 133:249-253. https://doi.org/10.1007/BF00380685
  43. 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. https://doi.org/10.1093/jxb/erm299
  44. 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. https://doi.org/10.1016/0014-5793(95)00368-J
  45. 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. https://doi.org/10.1105/tpc.106.046417
  46. Mann, V., M. Harker, I. Pecker, and J. Hirschberg. 2000. Metabolic engineering of astaxanthin production in tobacco flowers. Nat. Biotechnol. 18:888-892. https://doi.org/10.1038/78515
  47. 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. https://doi.org/10.1093/oxfordjournals.jbchem.a124656
  48. 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. https://doi.org/10.1023/A:1006417009203
  49. 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. https://doi.org/10.1104/pp.106.087130
  50. Ohmiya, A. 2009. Carotenoid cleavage dioxygenases and their apocarotenoid products in plants. Plant Biotechnol. 26:351-358. https://doi.org/10.5511/plantbiotechnology.26.351
  51. 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. https://doi.org/10.1007/BF00019013
  52. Pfander, H. 1992. Carotenoids part A: Chemistry, separation, quantitation, and antioxidation. Methods Enzymology 213:3-13. https://doi.org/10.1016/0076-6879(92)13105-7
  53. Pfander, H. and H. Schurtenberger. 1982. Biosynthesis of $C_{20}$-carotenoids in Crocus sativus. Phytochemistry 21:1039-1042. https://doi.org/10.1016/S0031-9422(00)82412-7
  54. 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. https://doi.org/10.1111/j.1365-313X.2004.02151.x
  55. 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. https://doi.org/10.1104/pp.007138
  56. 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. https://doi.org/10.1073/pnas.0337742100
  57. 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. https://doi.org/10.1073/pnas.190177497
  58. 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. https://doi.org/10.1007/s00425-004-1299-1
  59. 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. https://doi.org/10.1074/jbc.M804000200
  60. 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. https://doi.org/10.1016/j.phytochem.2009.04.022
  61. Seybold, A. and T.W. Goodwin. 1959. Occurrence of astaxanthin in the flower petals of Adonis Annua L. Nature 184:1714-1715. https://doi.org/10.1038/1841714a0
  62. 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. https://doi.org/10.1046/j.1365-313X.1996.10050781.x
  63. 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. https://doi.org/10.1126/science.276.5320.1872
  64. 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. https://doi.org/10.1104/pp.102.017921
  65. Scott, M.I., I. Ascarelli, and G. Olson. 1968. Studies of egg yolk pigmentation. Poult. Sci. 47:863. https://doi.org/10.3382/ps.0470863
  66. 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. https://doi.org/10.1111/j.1365-313X.2004.02263.x
  67. 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. https://doi.org/10.1104/pp.102.2.491
  68. 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. https://doi.org/10.1007/s00299-006-0302-7
  69. 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. https://doi.org/10.1016/0021-9673(94)80628-4
  70. 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. https://doi.org/10.1073/pnas.94.22.12235
  71. Tanaka, Y., N. Sasaki, and A. Ohmiya. 2008. Biosynthesis of plant pigments: Anthocyanins, betalains and carotenoids. Plant J. 54:733-749. https://doi.org/10.1111/j.1365-313X.2008.03447.x
  72. 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. https://doi.org/10.1002/hlca.19790620821
  73. 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. https://doi.org/10.1038/nature07272
  74. 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. https://doi.org/10.1042/bj1060479
  75. 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. https://doi.org/10.1074/jbc.272.40.24747
  76. Vishnevetsky, M., M. Ovadis, and A. Vainstein. 1999a. Carotenoid sequestration in plants: The role of carotenoid associated proteins. Trends Plant Sci. 4:232-235. https://doi.org/10.1016/S1360-1385(99)01414-4
  77. 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. https://doi.org/10.1046/j.1365-313x.1999.00615.x
  78. 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. https://doi.org/10.1093/jn/134.1.251S
  79. 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. https://doi.org/10.1111/j.1439-0523.2009.01656.x
  80. Yamamizo, C., S. Kishimoto, and A. Ohmiya. 2010. Carotenoid composition and carotenogenic gene expression during Ipomoea petal development. J. Exp. Bot. 61:709-719. https://doi.org/10.1093/jxb/erp335
  81. 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. https://doi.org/10.1007/s00425-006-0455-1
  82. 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. https://doi.org/10.1093/jxb/err070
  83. 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. https://doi.org/10.1023/A:1013383120392
  84. 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.
  85. 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. https://doi.org/10.1007/s11248-007-9151-6

Cited by

  1. Effect of Cold Stress on Carotenoids in Kale Leaves (Brassica oleracea) vol.36, pp.2, 2017, https://doi.org/10.5338/KJEA.2017.36.2.19