Use of the cauliflower Or gene for improving crop nutritional quality

Biotechnology Annual Review

Volumn 14, Issue , 2008, Pages 171-190

  Zhou, Xiangjun ^a   Van Eck, Joyce ^b   Li, Li ^a  

^a ROBERT W HOLLEY CENTER FOR AGRICULTURE AND HEALTH   (United States)

^b United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

Author keywords

carotene; carotenoids; cauliflower; chromoplast; crop nutrition enhancement; metabolic sink; Or gene

Indexed keywords

CAROTENOID; PIGMENT; RETINOL; VEGETABLE PROTEIN;

BIOSYNTHESIS; CAULIFLOWER; CHROMOPLAST; CONTROLLED STUDY; CROP IMPROVEMENT; DIET; GENE FUNCTION; GENE INSERTION; GENE ISOLATION; GENETIC MANIPULATION; METABOLIC ENGINEERING; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRITIONAL VALUE; PLANT GENETICS; POTATO; PROTEIN DOMAIN; RETROPOSON; REVIEW; TRANSGENIC PLANT;

AGRICULTURE; BRASSICA; CAROTENOIDS; CROPS, AGRICULTURAL; GENETIC ENHANCEMENT; NUTRITIVE VALUE; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED;

BRASSICA OLERACEA VAR. BOTRYTIS; SOLANUM TUBEROSUM;

EID: 46149100287     PISSN: 13872656     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S1387-2656(08)00006-9     Document Type: Review

References (82)

1. Combs G.F. The Vitamins: Fundamental Aspects in Nutrition and Health. 2nd edn (1998), Academic Press, New York, USA pp. 107-153
2. Giovannucci E. Nutritional factors in human cancers. Adv Exp Med Biol 472 (1999) 29-42
3. Hadley C.W., Miller E.C., Schwartz S.J., and Clinton S.K. Tomatoes, lycopene, and prostate cancer: progress and promise. Exp Biol Med 227 (2002) 869-880
4. Cunningham F.X., and Gantt E. Genes and enzymes of carotenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 49 (1998) 557-583
5. Fraser P.D., and Bramley P.M. The biosynthesis and nutritional uses of carotenoids. Prog Lipid Res 43 (2004) 228-265
6. DellaPenna D., and Pogson B.J. Vitamin synthesis in plants: tocopherols and carotenoids. Annu Rev Plant Biol 57 (2006) 711-738
7. Botella-Pavia P., and Rodriguez-Concepcion M. Carotenoid biotechnology in plants for nutritionally improved foods. Physiol Plant 126 (2006) 369-381
8. Sandmann G., Römer S., and Fraser P.D. Understanding carotenoid metabolism as a necessity for genetic engineering of crop plants. Metab Eng 8 (2006) 291-302
9. Taylor M., and Ramsay G. Carotenoid biosynthesis in plant storage organs: recent advances and prospects for improving plant food quality. Physiol Plant 124 (2005) 143-151
10. Paine J.A., Shipton C.A., Chaggar S., Howells R.M., Kennedy M.J., Vernon G., Wright S.Y., Hinchliffe E., Adams J.L., Silverstone A.L., and Drake R. Improving the nutritional value of Golden Rice through increased pro-vitamin A content. Nat Biotechnol 23 (2005) 482-487
11. Fray R.G., Wallace A., Fraser P.D., Valero D., Hedden P., Bramley P.M., and Grierson D. Constitutive expression of a fruit phytoene synthase gene in transgenic tomatoes causes dwarfism by redirecting metabolites from the gibberellin pathway. Plant J 8 (1995) 693-701
12. Crisp P., Walkey D.G.A., Bellman E., and Roberts E. A mutation affecting curd colour in cauliflower (Brassica oleracea L. var. botrytis DC). Euphytica 24 (1975) 173-176
13. Dickson M.H., Lee C.Y., and Bramble A.E. Orange-curd high carotene cauliflower inbreds, NY156, NY163, and NY165. HortScience 23 (1988) 778-779
14. Li L., Paolillo D.J., Parthasarathy M.V., DiMuzio E.M., and Garvin D.F. A novel gene mutation that confers abnormal patterns of beta-carotene accumulation in cauliflower (Brassica oleracea var. botrytis). Plant J 26 (2001) 59-67
15. Lu S., Van Eck J., Zhou X., Lopez A.B., O'Halloran D.M., Cosman K.M., Conlin B.J., Paolillo D.J., Garvin D.F., Vrebalov J., Kochian L.V., Kupper H., Earle E.D., Cao J., and Li L. The cauliflower Or gene encodes a DnaJ cysteine-rich domain-containing protein that mediates high levels of β-carotene accumulation. Plant Cell 18 (2006) 3594-3605
16. Lopez A.B., Van Eck J., Conlin B., Paolillo D.J., O'Neill J., and Li L. Effect of the cauliflower Or transgene on carotenoid accumulation and chromoplast formation in transgenic potato tubers. J Exp Bot 59 (2008) 213-223
17. Howitt C.A., and Pogson B.J. Carotenoid accumulation and function in seeds and non-green tissues. Plant Cell Environ 29 (2006) 435-445
18. Qin X., and Zeevaart J.A.D. The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci USA 96 (1999) 15354-15361
19. Schwartz S.H., Tan B.C., Gage D.A., Zeevaart J.A., and McCarty D.R. Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276 (1997) 1872-1874
20. Gallagher C.E., Cervantes-Cervantes M., and Wurtzel E.T. Surrogate biochemistry: use of Escherichia coli to identify plant cDNAs that impact metabolic engineering of carotenoid accumulation. Appl Microbiol Biotechnol 60 (2003) 713-719
21. Mandel M.A., Feldmann K.A., Herrera-Estrella L., Rocha-Sosa M., and Leon P. CLA1, a novel gene required for chloroplast development, is highly conserved in evolution. Plant J 9 (1996) 649-658
22. Estevez J.M., Cantero A., Romero C., Kawaide H., Jimenez L.F., Kuzuyama T., Seto H., Kamiya Y., and Leon P. Analysis of the expression of CLA1, a gene that encodes the 1-deoxyxylulose 5-phosphate synthase of the 2-C-methyl-D-erythritol-4-phosphate pathway in Arabidopsis. Plant Physiol 124 (2000) 95-104
23. Crowell D.N., Packard C.E., Pierson C.A., Giner J.L., Downes B.P., and Chary S.N. Identification of an allele of CLA1 associated with variegation in Arabidopsis thaliana. Physiol Plant 118 (2003) 29-37
24. Botella-Pavia P., Besumbes O., Phillips M.A., Carretero-Paulet L., Boronat A., and Rodriguez-Concepcion M. Regulation of carotenoid biosynthesis in plants: evidence for a key role of hydroxymethylbutenyl diphosphate reductase in controlling the supply of plastidial isoprenoid precursors. Plant J 40 (2004) 188-199
25. Cunningham F.X. Regulation of carotenoid synthesis and accumulation in plants. Pure Appl Chem 74 (2002) 1409-1417
26. Simkin A.J., Zhu C., Kuntz M., and Sandmann G. Light-dark regulation of carotenoid biosynthesis in pepper (Capsicum annuum) leaves. J Plant Physiol 160 (2003) 439-443
27. von Lintig J., Welsch R., Bonk M., Giuliano G., Batschauer A., and Kleinig H. Light-dependent regulation of carotenoid biosynthesis occurs at the level of phytoene synthase expression and is mediated by phytochrome in Sinapis alba and Arabidopsis thaliana seedlings. Plant J 12 (1997) 625-634
28. Welsch R., Medina J., Giuliano G., Beyer P., and von Lintig J. Structural and functional characterization of the phytoene synthase promoter from Arabidopsis thaliana. Planta 216 (2003) 523-534
29. Giuliano G., Bartley G.E., and Scolnik P.A. Regulation of carotenoid biosynthesis during tomato development. Plant Cell 5 (1993) 379-387
30. Corona V., Aracri B., Kosturkova G., Bartley G.E., Pitto L., Giorgetti L., Scolnik P.A., and Giuliano G. Regulation of a carotenoid biosynthesis gene promoter during plant development. Plant J 9 (1996) 505-512
31. Kato M., Ikoma Y., Matsumoto H., Sugiura M., Hyodo H., and Yano M. Accumulation of carotenoids and expression of carotenoid biosynthetic genes during maturation in citrus fruit. Plant Physiol 134 (2004) 824-837
32. Simkin A.J., Schwartz S.H., Auldridge M., Taylor M.G., and Klee H.J. The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles beta-ionone, pseudoionone, and geranylacetone. Plant J 40 (2004) 882-892
33. Schwartz S.H., Qin X., and Zeevaart J.A. Elucidation of the indirect pathway of abscisic acid biosynthesis by mutants, genes, and enzymes. Plant Physiol 131 (2003) 1591-1601
34. Schwartz S.H., Qin X., and Loewen M.C. The biochemical characterization of two carotenoid cleavage enzymes from Arabidopsis indicates that a carotenoid-derived compound inhibits lateral branching. J Biol Chem 279 (2004) 46940-46945
35. Kato M., Matsumoto H., Ikoma Y., Okuda H., and Yano M. The role of carotenoid cleavage dioxygenases in the regulation of carotenoid profiles during maturation in citrus fruit. J Exp Bot 57 (2006) 2153-2164
36. Iuchi S., Kobayashi M., Yamaguchi-Shinozaki K., and Shinozaki K. A stress-inducible gene for 9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. Plant Physiol 123 (2000) 553-562
37. Bouvier F., Suire C., Mutterer J., and Camara B. Oxidative remodeling of chromoplast carotenoids: identification of the carotenoid dioxygenase CsCCD and CsZCD genes involved in crocus secondary metabolite biogenesis. Plant Cell 15 (2003) 47-62
38. Bouvier F., Dogbo O., and Camara B. Biosynthesis of the food and cosmetic plant pigment bixin (annatto). Science 300 (2003) 2089-2091
39. Tan B.C., Schwartz S.H., Zeevaart J.A., and McCarty D.R. Genetic control of abscisic acid biosynthesis in maize. Proc Natl Acad Sci USA 94 (1997) 12235-12240
40. Simkin A.J., Underwood B.A., Auldridge M., Loucas H.M., Shibuya K., Schmelz E., Clark D.G., and Klee H.J. Circadian regulation of the PhCCD1 carotenoid cleavage dioxygenase controls emission of β-ionone, a fragrance volatile of petunia flowers. Plant Physiol 136 (2004) 3504-3514
41. Marano M.R., Serra E.C., Orellano E.G., and Carrillo N. The path of chromoplast development in fruits and flowers. Plant Sci 94 (1993) 1-17
42. Vishnevetsky M., Ovadis M., and Vainstein A. Carotenoid sequestration in plants: the role of carotenoid-associated proteins. Trends Plant Sci 4 (1999) 232-235
43. Kessler F., Schnell D., and Blobel G. Identification of proteins associated with plastoglobules isolated from pea (Pisum sativum L) chloroplasts. Planta 208 (1999) 107-113
44. Deruere J., Romer S., d'Harlingue A., Backhaus R.A., Kuntz M., and Camara B. Fibril assembly and carotenoid overaccumulation in chromoplasts: a model for supramolecular lipoprotein structures. Plant Cell 6 (1994) 119-133
45. Vishnevetsky M., Ovadis M., Itzhaki H., Levy M., Libal-Weksler Y., Adam Z., and Vainstein A. Molecular cloning of a carotenoid-associated protein from Cucumis sativus corollas: homologous genes involved in carotenoid sequestration in chromoplasts. Plant J 10 (1996) 1111-1118
46. Kim H.U., Wu S.S.H., Ratnayake C., and Huang A.H.C. Brassica rapa has three genes that encode proteins associated with different neutral lipids in plastids of specific tissues. Plant Physiol 126 (2001) 330-341
47. Simkin A.J., Gaffé J., Alcaraz J.P., Carde J.P., Bramley P.M., Fraser P.D., and Kuntz M. Fibrillin influence on plastid ultrastructure and pigment content in tomato fruit. Phytochem 68 (2007) 1545-1556
48. Leitner-Dagan Y., Ovadis M., Shklarman E., Elad Y., Rav David D., and Vainstein A. Expression and functional analyses of the plastid lipid-associated protein CHRC suggest its role in chromoplastogenesis and stress. Plant Physiol 142 (2006) 233-244
49. Fraser P.D., Romer S., Shipton C.A., Mills P.B., Kiano J.W., Misawa N., Drake R.G., Schuch W., and Bramley P.M. Evaluation of transgenic tomato plants expressing an additional phytoene synthase in a fruit-specific manner. Proc Natl Acad Sci USA 99 (2002) 1092-1097
50. Ducreux L.J., Morris W.L., Hedley P.E., Shepherd T., Davies H.V., Millam S., and Taylor M.A. Metabolic engineering of high carotenoid potato tubers containing enhanced levels of beta-carotene and lutein. J Exp Bot 56 (2005) 81-89
51. Shewmaker C.K., Sheehy J.A., Daley M., Colburn S., and Ke D.Y. Seed-specific overexpression of phytoene synthase: increase in carotenoids and other metabolic effects. Plant J 20 (1999) 401-412
52. Ye X., Al-Babili S., Klöti A., Zhang J., Lucca P., Beyer P., and Potrykus I. Engineering the provitamin A (β-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287 (2000) 303-305
53. Diretto G., Al-Babili S., Tavazza R., Papacchioli V., Beyer P., and Giuliano G. Metabolic engineering of potato carotenoid content through tuber-specific overexpression of a bacterial mini-pathway. PLoS ONE 2 (2007) e350
54. Dharmapuri S., Rosati C., Pallara P., Aquilani R., Bouvier F., Camara B., and Giuliano G. Metabolic engineering of xanthophyll content in tomato fruits. FEBS Lett 519 (2002) 30-34
55. Römer S., Lübeck J., Kauder F., Steiger S., Adomat C., and Sandmann G. Genetic engineering of a zeaxanthin-rich potato by antisense inactivation and co-suppression of carotenoid epoxidation. Metab Eng 4 (2002) 263-272
56. Diretto G., Welsch R., Tavazza R., Mourgues F., Pizzichini D., Beyer P., and Giuliano G. Silencing of beta-carotene hydroxylase increases total carotenoid and beta-carotene levels in potato tubers. BMC Plant Biol 7 (2007) 11
57. Van Eck J., Conlin B., Garvin D.F., Mason H., Navarre D.A., and Brown C.R. Enhancing beta-carotene content in potato by RNAi-mediated silencing of the b-carotene hydroxylase gene. Am J Potato Res 84 (2007) 331-342
58. D'Ambrosio C., Giorio G., Marino I., Merendino A., Petrozza A., Salfi L., Stigliani A.L., and Cellini F. Virtually complete conversion of lycopene into β-carotene in fruits of tomato plants transformed with the tomato lycopene β-cyclase (tlcy-b) cDNA. Plant Sci 166 (2004) 207-214
59. Gerjets T., and Sandmann G. Ketocarotenoid formation in transgenic potato. J Exp Bot 57 (2006) 3639-3645
60. Mann V., Harker M., Pecker I., and Hirschberg J. Metabolic engineering of astaxanthin production in tobacco flowers. Nat Biotechnol 18 (2000) 888-892
61. Ralley L., Enfissi E.M.A., Misawa N., Schuch W., Bramley P.M., and Fraser P.D. Metabolic engineering of ketocarotenoid formation in higher plants. Plant J 39 (2004) 477-486
62. Stålberg K., Lindgren O., Ek B., and Höglund A.S. Synthesis of ketocarotenoids in the seed of Arabidopsis thaliana. Plant J 36 (2003) 771-779
63. Giliberto L., Perrotta G., Pallara P., Weller J.L., Fraser P.D., Bramley P.M., Fiore A., Tavazza M., and Giuliano G. Manipulation of the blue light photoreceptor cryptochrome 2 in tomato affects vegetative development, flowering time, and fruit antioxidant content. Plant Physiol 137 (2005) 199-208
64. Davuluri G.R., van Tuinen A., Fraser P.D., Manfredonia A., Newman R., Burgess D., Brummell D.A., King S.R., Palys J., Uhlig J., Bramley P.M., Pennings H.M.J., and Bowler C. Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes. Nat Biotechnol 23 (2005) 890-895
65. Lindgren L.O., Stalberg K.G., and Hoglund A.S. Seed-specific overexpression of an endogenous Arabidopsis phytoene synthase gene results in delayed germination and increased levels of carotenoids, chlorophyll, and abscisic acid. Plant Physiol 132 (2003) 779-785
66. Frey-Wyssling A., and Schwegler F. Ultrastructure of chromoplasts in the carrot root. J Ultrastruct Res 13 (1965) 543-559
67. Paolillo D.J., Garvin D.F., and Parthasarathy M.V. The chromoplasts of Or mutants of cauliflower (Brassica oleracea L. var. botrytis). Protoplasma 224 (2004) 245-253
68. Li L., Lu S., Cosman K.M., Earle E.D., Garvin D.F., and O'Neill J. β-Carotene accumulation induced by the cauliflower Or gene is not due to an increased capacity of biosynthesis. Phytochem 67 (2006) 1177-1184
69. Li L., and Garvin D.F. Molecular mapping of Or, a gene inducing β-carotene accumulation in cauliflower (Brassica oleracea var. botrytis). Genome 47 (2003) 588-594
70. Li L., Lu S., O'Halloran D.M., Garvin D.F., and Vrebalov J. High-resolution genetic and physical mapping of the cauliflower high β-carotene gene Or (Orange). Mol Genet Genomics 270 (2003) 132-138
71. Cheetham M.E., and Caplan A.J. Structure, function and evolution of DnaJ: conservation and adaptation of chaperone function. Cell Stress Chaperones 3 (1998) 28-36
72. Hartl F.U., and Hayer-Hartl M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295 (2002) 1852-1858
73. Hugueney P., Bouvier F., Badillo A., d'Harlingue A., Kuntz M., and Camara B. Identification of a plastid protein involved in vesicle fusion and/or membrane protein translocation. Proc Natl Acad Sci USA 92 (1995) 5630-5634
74. Morris W.L., Ducreux L., Griffiths D.W., Stewart D., Davies H.V., and Taylor M.A. Carotenogenesis during tuber development and storage in potato. J Exp Bot 55 (2004) 975-982
75. Griffiths D.W., Dale M.F., Morris W.L., and Ramsay G. Effects of season and postharvest storage on the carotenoid content of Solanum phureja potato tubers. J Agric Food Chem 55 (2007) 379-385
76. Fishwick M.J., and Wright A.J. Isolation and characterization of amyloplast envelope membranes from Solanum tuberosum. Phytochem 19 (1980) 55-59
77. Camara B., Hugueney P., Bouvier F., Kuntz M., and Moneger R. Biochemistry and molecular biology of chromoplast development. Int Rev Cytol 163 (1995) 175-247
78. Bartley G.E., and Scolnik P.A. Plant carotenoids: pigments for photoprotection, visual attraction, and human health. Plant Cell 7 (1995) 1027-1038
79. Rabbani S., Beyer P., Lintig J., Hugueney P., and Kleinig H. Induced beta-carotene synthesis driven by triacylglycerol deposition in the unicellular alga Dunaliella bardawil. Plant Physiol 116 (1998) 1239-1248
80. Cookson P.J., Kiano J.W., Shipton C.A., Fraser P.D., Romer S., Schuch W., Bramley P.M., and Pyke K.A. Increases in cell elongation, plastid compartment size and phytoene synthase activity underlie the phenotype of the high pigment-1 mutant of tomato. Planta 217 (2003) 896-903
81. Liu Y., Roof S., Ye Z., Barry C., van Tuinen A., Vrebalov J., Bowler C., and Giovannoni J. Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc Natl Acad Sci USA 101 (2004) 9897-9902
82. Li L., and Van Eck J. Metabolic engineering of carotenoid accumulation by creating a metabolic sink. Transgenic Res 16 (2007) 581-585