1,957
Views
32
CrossRef citations to date
0
Altmetric
Original Articles

Biosynthesis and Engineering of Carotenoids and Apocarotenoids in Plants: State of the Art and Future Prospects

, &
Pages 139-162 | Published online: 15 Apr 2013

References

  • Al-Babili , S. and Beyer , P. 2005 . Golden Rice - five years on the road - five years to go? . Trends Plant Sci , 10 : 565 – 573 .
  • Al-Babili , S. , Hugueney , P. , Schledz , M. , Welsch , R. , Frohnmeyer , H. , Laule , O. and Beyer , P. 2000 . Identification of a novel gene coding for neoxanthin synthase from Solanum tuberosum . FEBS Lett , 485 : 168 – 172 .
  • Alba , R. , Fei , Z. , Payton , P. , Liu , Y. , Moore , S. L. , Debbie , P. , Cohn , J. , D'Ascenzo , M. , Gordon , J. S. , Rose , J. K. C. , Martin , G. , Tanksley , S. D. , Bouzayen , M. , Jahn , M. M. and Giovannoni , J. 2004 . ESTs, cDNA microarrays, and gene expression profiling: tools for dissecting plant physiology and development . Plant J , 39 : 697 – 714 .
  • Aluru , M. , Xu , Y. , Guo , R. , Wang , Z. , Li , S. , White , W. , Wang , K. and Rodermel , S. 2008 . Generation of transgenic maize with enhanced pro-vitamin A content . J Exp Bot , 59 : 3551 – 3562 .
  • Auldridge , M. E. , McCarty , D. R. and Klee , H. J. 2006 . Plant carotenoid cleavage oxygenases and their apocarotenoid products . Curr Opin Plant Biol , 9 : 1 – 7 .
  • Bird , C. R. , Ray , J. A. , Fletcher , J. D. , Boniwell , J. M. , Bird , A. S. , Teulieret , C. , Bramley , P. M. and Schuch , W. 1991 . Using antisense RNA to study gene function: inhibition of carotenoid biosynthesis in transgenic tomatoes . Bio/Technol , 7 : 635 – 639 .
  • Bouvier , F. , Hugueney , P. , D'Harlingue , A. , Kuntz , M. and Camara , B. 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 .
  • Bouvier , F. , D'harlingue , A. , Backhaus , R. A. , Kumagai , M. H. and Camara , B. 2000 . Identification of neoxanthin synthase as a carotenoid cyclase paralog . Eur J Biochem , 267 : 6346 – 6352 .
  • Bouvier , F. , Dogbo , O. and Camara , B. 2003a . Biosynthesis of the food and cosmetic plant pigment bixin (annatto) . Science , 300 : 2089 – 2091 .
  • Bouvier , F. , Suire , C. , Mutterer , J. and Camara , B. 2003b . 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 .
  • Breitenbach , J. and Sandmann , G. 2005 . ?-carotene cis isomers as products and substrates in the plant poly-cis carotenoid biosynthetic pathway to lycopene . Planta , 220 : 785 – 793 .
  • Britton , G. , Liaaen-Jensen , S. and Pfander , H. , eds. 2003 . Carotenoid Handbook , Basel : Birkhäuser .
  • Brown , C. R. 2005 . Antioxidants in potato . Am J Potato Res , 82 : 163 – 172 .
  • Bub , A. , Möseneder , J. , Wenzel , G. , Rechkemmer , G. and Briviba , K. 2008 . Zeaxanthin is bioavailable from genetically modified zeaxanthin-rich potatoes . Eur J Nutr , 47 : 99 – 103 .
  • Burkhardt , P. K. , Beyer , P. , Wünn , J. , Klöti , A. , Armstrong , G. A. , Schledz , M. , Von Lintig , J. and Potrykus , I. 1997 . Transgenic rice (Oryza sativa) endosperm expressing daffodil (Narcissus psuedonarcissus) phytoene synthase accumulates phytoene, a key intermediate of pro-vitamin A biosynthesis . Plant J , 11 : 1071 – 1078 .
  • Côté , F. , Cormier , F. , Dufresne , C. and Willemot , C. 2000 . Properties of a glucosyltransferase involved in crocin synthesis . Plant Sci , 153 : 55 – 63 .
  • Cunningham , F. X. Jr. and Gantt , E. 2001 . One ring or two? Determination of ring number in carotenoids by lycopene epsilon-cyclases . Proc Natl Acad Sci USA , 98 : 2905 – 2910 .
  • Cunningham , F. X. Jr. and Gantt , E. 2005 . A study in scarlet: enzymes of ketocarotenoid biosynthesis in the flowers of Adonis aestivalis . Plant J , 41 : 478 – 492 .
  • Cunningham , F. X. Jr. and Gantt , E. 2007 . A portfolio of plasmids for identification and analysis of carotenoid pathway enzymes: Adonis aestivalis as a case study . Photosynth Res , 92 : 245 – 259 .
  • D'ambrosio , C. , Giorio , G. , Marino , I. , Merendino , A. , Petrozza , A. , Salfi , L. , Stigliani , A. L. and Cellini , F. 2004 . Virtually complete conversion of lycopene into ?-carotene in fruits of tomato plants transformed with the tomato lycopene ?-cyclase (tlcy-b) cDNA . Plant Sci , 166 : 207 – 214 .
  • Datta , K. , Baisakh , N. , Oliva , N. , Torrizo , L. , Abrigo , E. , Tan , J. , Rai , M. , Rehana , S. , Al-Babili , S. , Beyer , P. , Potrykus , I. and Datta , S. K. 2000 . Bioengineered 'golden' indica rice cultivars with ?-carotene metabolism in the endosperm with hygromycin and mannose selection systems . Plant Biotechnol J , 1 : 81 – 90 .
  • Davidovich-Rikanati , R. , Sitrit , Y. , Tadmor , Y. , Iijima , Y. , Bilenko , N. , Bar , E. , Carmona , B. , Fallik , E. , Dudai , N. , Simon , J. E. , Pichersky , E. and Lewinsohn , E. 2007 . Enrichment of tomato flavor by diversion of the early plastidial terpenoid pathway . Nat Biotechnol , 25 : 899 – 901 .
  • Davison , P. A. , Hunter , C. N. and Horton , P. 2002 . Overexpression of ?-carotene hydroxylase enhances stress tolerance in Arabidopsis . Nature , 418 : 203 – 206 .
  • 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. 2005 . Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes . Nat Biotechnol , 23 : 890 – 895 .
  • Deli , J. , Molnár , P. , Matus , Z. and Tóth , G. 2001 . Carotenoid composition in the fruits of red paprika (Capsicum annuum var. lycopersiciforme rubrum) during ripening; biosynthesis of carotenoids in red paprika . J Agric Food Chem , 49 : 1517 – 1523 .
  • Dellapenna , D. and Pogson , B. J. 2006 . Vitamin synthesis in plants: tocopherols and carotenoids . Annu Rev Plant Biol , 57 : 711 – 738 .
  • Dharmapuri , S. , Rosati , C. , Pallara , P. , Aquilani , R. , Bouvier , F. , Camara , B. and Giuliano , G. 2002 . Metabolic engineering of xanthophyll content in tomato fruits . FEBS Lett , 519 : 30 – 34 .
  • Diretto , G. , Tavazza , R. , Welsch , R. , Pizzichini , D. , Mourgues , F. , Papacchioli , V. , Beyer , P. and Giuliano , G. 2006 . Metabolic engineering of potato tuber carotenoids through tuber-specific silencing of lycopene epsilon cyclase . BMC Plant Biol , 6 : 13
  • Diretto , G. , Al-Babili , S. , Tavazza , R. , Papacchioli , V. , Beyer , P. and Giuliano , G. 2007a . Metabolic engineering of potato carotenoid content through tuber-specific overexpression of a bacterial mini-pathway . PLoS ONE , 2 : e350
  • Diretto , G. , Welsch , R. , Tavazza , R. , Mourgues , F. , Pizzichini , D. , Beyer , P. and Giuliano , G. 2007b . Silencing of beta-carotene hydroxylase increases total carotenoid and beta-carotene levels in potato tubers . BMC Plant Biol , 7 : 11
  • Ducreux , L. J. , Morris , W. L. , Hedley , P. E. , Shepherd , T. , Davies , H. V. , Millam , S. and Taylor , M. A. 2005 . Metabolic engineering of high carotenoid potato tubers containing enhanced levels of beta-carotene and lutein . J Exp Bot , 56 : 81 – 89 .
  • Enfissi , E. M. A. , Fraser , P. D. , Lois , L. M. , Boronat , A. , Schuch , W. and Bramley , P. M. 2005 . Metabolic engineering of the mevalonate and nonmevalonate isopentenyl diphosphate-forming pathways for the production of health-promoting isoprenoids in tomato . Plant Biotechnol J , 3 : 17 – 27 .
  • Fraser , P. D. , Römer , S. , Shipton , C. A. , Mills , P. B. , Kiano , J. W. , Misawa , N. , Drake , R. G. , Schuch , W. and Bramley , P. M. 2002 . Evaluation of transgenic tomato plants expressing an additional phytoene synthase in a fruit-specific manner . Proc Natl Acad Sci USA , 99 : 1092 – 1097 .
  • Fraser , P. D. , Enfissi , E. M. , Halket , J. M. , Truesdale , M. R. , Yu , D. , Gerrish , C. and Bramley , P. M. 2007 . Manipulation of phytoene levels in tomato fruit: effects on isoprenoids, plastids, and intermediary metabolism . Plant Cell , 19 : 3194 – 3211 .
  • Fraser , P. D. , Enfissi , E. M. A. and Bramley , P. M. 2009 . Genetic engineering of carotenoid formation in tomato fruit and the potential application of systems and synthetic biology approaches . Arch Biochem Biophys , 483 : 196 – 204 .
  • Fray , R. G. , Wallace , A. , Fraser , P. D. , Valero , D. , Hedden , P. , Bramley , P. M. and Grierson , D. 1995 . Constitutive expression of a fruit phytoene synthase gene in transgenic tomatoes causes dwarfism by redirecting metabolites from the gibberellin pathway . Plant J , 8 : 693 – 701 .
  • Fujisawa , M. , Watanabe , M. , Choi , S. K. , Teramoto , M. , Ohyama , K. and Misawa , N. 2008 . Enrichment of carotenoids in flaxseed (Linum usitatissimum) by metabolic engineering with introduction of bacterial phytoene synthase gene crtB . J Biosci Bioeng , 105 : 636 – 641 .
  • Fujisawa , M. , Takita , E. , Harada , H. , Sakurai , N. , Suzuki , H. , Ohyama , K. , Shibata , D. and Misawa , N. 2009 . Pathway engineering of Brassica napus seeds using multiple key enzyme genes involved in ketocarotenoid formation . J Exp Bot , 60 : 1319 – 1332 .
  • Galpaz , N. , Ronen , G. , Khalfa , Z. , Zamir , D. and Hirschberg , J. 2006 . A chromoplast-specific carotenoid biosynthesis pathway is revealed by cloning of the tomato whiteflower locus . Plant Cell , 18 : 1947 – 1960 .
  • Gann , P. H. , Ma , J. , Giovannucci , E. , Willett , W. , Sacks , F. M. , Hennekens , C. H. and Stampfer , M. J. 1999 . Lower prostate cancer risk in men with elevated plasma lycopene levels: results of a prospective analysis . Cancer Res , 59 : 1225 – 1230 .
  • Garcia-Limones , C. , SchnÄbele , K. , Blanco-Portales , R. , Bellido , M. L. , Caballero , J. L. , Schwab , W. and MuÑoz-Blanco , J. 2008 . Functional characterization of FaCCD1: a carotenoid cleavage dioxygenase from strawberry involved in lutein degradation during fruit ripening . J. Agric. Food Chem , 56 : 9277 – 9285 .
  • Gerjets , T. and Sandmann , G. 2006 . Ketocarotenoid formation in transgenic potato . J Exp Bot , 57 : 3639 – 3645 .
  • Gerjets , T. , Sandmann , M. , Zhu , C. and Sandmann , G. 2007 . Metabolic engineering of ketocarotenoid biosynthesis in leaves and flowers of tobacco species . Biotechnol J , 2 : 1263 – 1269 .
  • Giliberto , L. , Perrotta , G. , Pallara , P. , Weller , J. L. , Fraser , P. D. , Bramley , P. M. , Fiore , A. , Tavazza , M. and Giuliano , G. 2005 . Manipulation of the blue light photoreceptor cryptochrome 2 in tomato affects vegetative development, flowering time, and fruit antioxidant content . Plant Physiol , 137 : 199 – 208 .
  • Giuliano , G. , Giliberto , L. and Rosati , C. 2002 . Carotenoid isomerase: a tale of light and isomers . Trends Plant Sci , 7 : 513 – 516 .
  • Giuliano , G. , Rosati , C. and Bramley , P. M. 2003 . To dye or not to dye: biochemistry of annatto unveiled . Trends Biotechnol , 21 : 427 – 429 .
  • Giuliano , G. , Tavazza , R. , Diretto , G. , Beyer , P. and Taylor , M. A. 2008 . Metabolic engineering of carotenoid biosynthesis in plants . Trends Biotechnol , 26 : 139 – 145 .
  • Götz , T. , Sandmann , G. and Römer , S. 2002 . Expression of a bacterial carotene hydroxylase gene (crtZ) enhances UV tolerance in tobacco . Plant Mol Biol , 50 : 129 – 142 .
  • Guil-Guerrero , J. L. , Martínez-Guirado , C. , Del Mar Rebolloso-Fuentes , M. and Carrique-Pérez , A. 2006 . Nutrient composition and antioxidant activity of 10 pepper (Capsicum annuum) varieties . Eur Food Res Technol , 224 : 1 – 9 .
  • Ha , S. H. , Kim , J. B. , Park , J. S. , Lee , S. W. and Cho , K. J. 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 , 133 : 161 – 169 .
  • Harjes , C. E. , Rocheford , T. R. , Bai , L. , Brutnell , T. P. , Bermudez Kandianis , C. , Sowinski , S. G. , Stapleton , A. E. , Vallabhaneni , R. , Williams , M. , Wurtzel , E. T. , Yan , J. and Buckler , E. S. 2008 . Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification . Science , 319 : 330 – 333 .
  • Hasunuma , T. , Miyazawa , S. , Yoshimura , S. , Shinzaki , Y. , Tomizawa , K. , Shindo , K. , Choi , S. K. , Misawa , N. and Miyake , C. 2008 . Biosynthesis of astaxanthin in tobacco leaves by transplastomic engineering . Plant J , 55 : 857 – 868 .
  • Hirschberg , J. 2001 . Carotenoid biosynthesis in flowering plants . Curr Opin Plant Biol , 4 : 210 – 218 .
  • Hoa , T. T. C. , Al-Babili , S. , Schaub , P. , Potrykus , I. and Beyer , P. 2003 . Golden indica and japonica rice lines amenable to deregulation . Plant Physiol , 133 : 161 – 169 .
  • Hornero-Méndez , D. , De Guevara , R. G. L. and Mínguez-Mosquera , I. M. 2000 . Carotenoid biosynthesis changes in five red pepper (Capsicum annuum) cultivars during ripening. Cultivar selection for breeding . J Agric Food Chem , 48 : 3857 – 3864 .
  • Huang , F. C. , Horváth , G. , Molnár , P. , Turcsi , E. , Deli , J. , Schrader , J. , Sandmann , G. , Schmidt , H. and Schwab , W. 2009 . Substrate promiscuity of RdCCD1, a carotenoid cleavage oxygenase from Rosa damascena . Phytochem , 70 : 457 – 464 .
  • Ibdah , M. , Azulay , Y. , Portnoy , V. , Wasserman , B. , Bar , E. , Meir , A. , Burger , Y. , Hirschberg , J. , Schaffer , A. A. , Katzir , N. , Tadmor , Y. and Lewinsohn , E. 2006 . Functional characterization of CmCCD1, a carotenoid cleavage dioxygenase from melon . Phytochem , 67 : 1579 – 1589 .
  • Ilg , A. , Beyer , P. and Al-Babili , S. 2009 . Characterization of the rice carotenoid cleavage dioxygenase 1 reveals a novel route for geranial biosynthesis . FEBS J , 276 : 736 – 747 .
  • Isaacson , T. , Ohad , I. , Beyer , P. and Hirschberg , J. 2004 . Analysis in vitro of the enzyme CRTISO establishes a poly-cis-carotenoid biosynthesis pathway in plants . Plant Physiol , 136 : 4246 – 55 .
  • Jayaraj , J. and Punja , Z. K. 2008 . Transgenic carrot plants accumulating ketocarotenoids show tolerance to UV and oxidative stress . Plant Physiol Biochem , 46 : 875 – 883 .
  • Jayaraj , J. , Devlin , R. and Punja , Z. K. 2008 . Metabolic engineering of novel ketocarotenoids production in carrot plants . Transgenic Res , 17 : 489 – 501 .
  • Just , B. J. , Santos , C. A. , Fonseca , M. E. , Boiteux , L. S. , Oloizia , B. B. and Simon , P. W. 2007 . Carotenoid biosynthesis structural genes in carrot (Daucus carota): isolation, sequence-characterization, single nucleotide polymorphism (SNP) markers and genome mapping . Theor Appl Genet , 114 : 693 – 704 .
  • Kumagai , M. H. , Keller , Y. , Bouvier , F. , Clary , D. and Camara , B. 1998 . Functional integration of non-native carotenoids into chloroplasts by viral-derived expression of capsanthin-capsorubin synthase in Nicotiana benthamiana . Plant J , 14 : 305 – 315 .
  • Lee , Y. H. , Jung , M. , Shin , S. H. , Lee , J. H. , Choi , S. H. , Her , N. H. , Lee , J. H. , Ryu , K. H. , Paek , K. Y. and Harn , C. H. 2009 . Transgenic peppers that are highly tolerant to a new CMV pathotype . Plant Cell Rep , 28 : 223 – 232 .
  • Lefebvre , V. , Kuntz , M. , Camara , B. and Palloix , A. 1998 . The capsanthin-capsorubin synthase gene: a candidate locus for the y locus controlling the red fruit colour in pepper . Plant Mol Biol , 36 : 785 – 789 .
  • Li , F. , Murillo , C. and Wurtzel , E. T. 2007 . Maize Y9 encodes a product essential for 15-cis-?-carotene isomerization . Plant Physiol , 144 : 1181 – 1189 .
  • Li , F. , Vallabhaneni , R. and Wurtzel , E. T. 2008 . PSY3, a new member of the phytoene synthase gene family conserved in the Poaceae and regulator of abiotic stress-induced root carotenogenesis . Plant Physiol , 146 : 1333 – 1345 .
  • Lindgren , L. O. , Stålberg , K. G. and Höglund , A. S. 2003 . 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 : 779 – 785 .
  • Liu , Y. , Roof , S. , Ye , Z. , Barry , C. , van Tuinen , A. , Vrebalov , J. , Bowler , C. and Giovannoni , J. 2004 . Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato . Proc Natl Acad Sci USA , 101 : 9897 – 9902 .
  • Lopez , A. B. , Van Eck , J. , Conlin , B. J. , Paolillo , D. J. , O'Neill , J. and Li , L. 2008 . Effect of the cauliflower Or transgene on carotenoid accumulation and chromoplast formation in transgenic potato tubers . J Exp Bot , 59 : 213 – 223 .
  • 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. , KÜpper , H. , Earle , E. D. , Cao , J. and Li , L. 2006 . The cauliflower Or gene encodes a DnaJ cysteine-rich domain-containing protein that mediates high-levels of ?-carotene accumulation . Plant Cell , 18 : 3594 – 3605 .
  • Mahjoub , A. , Hernould , M. , Joubes , J. , Decendit , A. , Mars , M. , Barrieu , F. , Hamdi , S. and Delrot , S. 2009 . Overexpression of a grapevine R2R3-MYB factor in tomato affects vegetative development, flower morphology and flavonoid and terpenoid metabolism . Plant Physiol Biochem , 47 : 551 – 561 .
  • Mann , V. , Harker , M. , Pecker , I. and Hirschberg , J. 2000 . Metabolic engineering of astaxanthin production in tobacco flowers . Nat Biotechnol , 18 : 888 – 892 .
  • Mehta , R. A. , Cassol , T. , Li , N. , Ali , N. , Handa , A. K. and Mattoo , A. K. 2002 . Engineered polyamine accumulation in tomato enhances phytonutrient content, juice quality, and vine life . Nat Biotechnol , 20 : 613 – 618 .
  • Misawa , N. , Kazumori , M. , Hori , T. , Ohtani , T. , Böger , P. and Sandmann , G. 1994 . Expression of an Erwinia phytoene desaturase gene not only confers multiple resistance to herbicides interfering with carotenoid biosynthesis but also alters xanthophyll metabolism in transgenic plants . Plant J , 6 : 481 – 489 .
  • Moco , S. , Bino , R. J. , Vorst , O. , Verhoeven , H. A. , de Groot , J. , van Beek , T. A. , Vervoort , J. and de Vos , R. C. H. 2006 . A liquid chromatography-mass spectrometry-based metabolome database for tomato . Plant Physiol , 141 : 1205 – 1218 .
  • Morris , W. L. , Ducreux , L. , Griffiths , D. W. , Stewart , D. , Davies , H. V. and Taylor , M. A. 2004 . Carotenogenesis during tuber development and storage in potato . J Exp Bot , 55 : 975 – 982 .
  • Morris , W. L. , Ducreux , L. , Fraser , P. D. , Millam , S. and Taylor , M. A. 2006a . Engineering ketocarotenoid biosynthesis in potato tubers . Metab Eng , 8 : 253 – 63 .
  • Morris , W. L. , Ducreux , L. , Hedden , P. , Millam , S. and Taylor , M. A. 2006b . Overexpression of a bacterial 1-deoxy-d-xylulose 5-phosphate synthase gene in potato tubers perturbs the isoprenoid metabolic network: implications for the control of the tuber life cycle . J Exp Bot , 57 : 3007 – 3018 .
  • Naqvi , S. , Zhu , C. , Farre , G. , Ramessar , K. , Bassie , L. , Breitenbach , J. , Perez Conesa , D. , Ros , G. , Sandmann , G. , Capell , T. and Christou , P. 2009 . Transgenic multivitamin corn through biofortification of endosperm with three vitamins representing three distinct metabolic pathways . Proc Natl Acad Sci USA , 106 : 7762 – 7767 .
  • North , H. M. , De Almeida , A. , Boutin , J. P. , Frey , A. , To , A. , Botran , L. , Sotta , B. and Marion-Poll , A. 2007 . The Arabidopsis ABA-deficient mutant aba4 demonstrates that the major route for stress-induced ABA accumulation is via neoxanthin isomers . Plant J , 50 : 810 – 824 .
  • 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. 2005 . Improving the nutritional value of Golden Rice through increased pro-vitamin A content . Nat Biotechnol , 23 : 482 – 487 .
  • Popovsky , S. and Paran , I. 2000 . Molecular genetics of the y locus in pepper: its relation to capsanthin-capsorubin synthase and to fruit color . Theor Appl Genet , 101 : 86 – 89 .
  • Ralley , L. , Enfissi , E. M. , Misawa , N. , Schuch , W. , Bramley , P. M. and Fraser , P. D. 2004 . Metabolic engineering of ketocarotenoid formation in higher plants . Plant J , 39 : 477 – 486 .
  • Ravanello , M. P. , Ke , D. , Alvarez , J. , Huang , B. and Shewmaker , C. K. 2003 . Coordinate expression of multiple bacterial carotenoid genes in canola leading to altered carotenoid production . Metab Eng , 5 : 255 – 263 .
  • Renstrøm , B. , Berger , H. and Liaaen-Jensen , S. 1981 . Esterified, optical pure (3S, 3?S)-astaxanthin from flowers of Adonis annua . Biochem Syst Ecol , 9 : 249 – 250 .
  • Rey , P. , Gillet , B. , Römer , S. , Eymery , F. , Massimino , J. , Peltier , G. and Kuntz , M. 2000 . Over-expression of a pepper plastid lipid-associated protein in tobacco leads to changes in plastid ultrastructure and plant development upon stress . Plant J , 21 : 483 – 494 .
  • Rocco , M. , D'Ambrosio , C. , Arena , S. , Faurobert , M. , Scaloni , A. and Marra , M. 2006 . Proteomic analysis of tomato fruits from two ecotypes during ripening . Proteomics , 6 : 3781 – 3791 .
  • Römer , S. , Fraser , P. D. , Kiano , J. W. , Shipton , C. A. , Misawa , N. , Schuch , W. and Bramley , P. M. 2000 . Elevation of the pro-vitamin A content of transgenic tomato plants . Nat Biotechnol , 18 : 666 – 669 .
  • Römer , S. , Lubeck , J. , Kauder , F. , Steiger , S. , Adomat , C. and Sandmann , G. 2002 . Genetic engineering of a zeaxanthin-rich potato by antisense inactivation and cosuppression of carotenoid epoxidation . Metab Eng , 4 : 263 – 272 .
  • Ronen , G. , Carmel-Goren , L. , Zamir , D. and Hirschberg , J. 2000 . An alternative pathway to ?-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 .
  • Rosati , C. , Aquilani , R. , Dharmapuri , S. , Pallara , P. , Marusic , C. , Tavazza , R. , Bouvier , F. , Camara , B. and Giuliano , G. 2000 . Metabolic engineering of beta-carotene and lycopene content in tomato fruit . Plant J , 24 : 413 – 420 .
  • Rubio , A. , Rambla , J. L. , Santaella , M. , Gomez , M. D. , Orzaez , D. , Granell , A. and Gómez-Gómez , L. 2008 . Cytosolic and plastoglobule-targeted carotenoid dioxygenases from Crocus sativus are both involved in beta-ionone release . J Biol Chem , 283 : 24816 – 24825 .
  • Rubio Moraga , A. , Fernández Nohales , P. , Fernández Pérez , J. A. and Gómez-Gómez , L. 2004 . Cytosolic and plastoglobule-targeted carotenoid dioxygenases from Crocus sativus are both involved in beta-ionone release . Planta , 219 : 955 – 966 .
  • Schaub , P. , Al-Babili , S. , Drake , R. and Beyer , P. 2005 . Why is golden rice golden (yellow) and not red? . Plant Physiol , 138 : 441 – 450 .
  • Schwartz , S. H. , Tan , B. C. , Gage , D. A. , Zeevart , J. A. and McCarty , D. R. 1997 . Specific oxidative cleavage of carotenoids by VP14 of maize . Science , 276 : 1872 – 1874 .
  • Schwartz , S. H. , Qin , X. and Loewen , M. C. 2004 . The biochemical characterization of two carotenoid cleavage enzymes from Arabidopsis indicates that a carotenoidderived compound inhibits lateral branching . J Biol Chem , 279 : 46940 – 46945 .
  • Sergeant , M. J. , Li , J. J. , Fox , C. , Brookbank , N. , Rea , D. , Bugg , T. D. H. and Thompson , A. J. 2009 . Selective inhibition of carotenoid cleavage dioxygenases: phenotypic effects on shoot branching . J Biol Chem , 284 : 5257 – 5264 .
  • Shewmaker , C. K. , Sheehy , J. A. , Daley , M. , Colburn , S. and Ke , D. Y . 1999 . Seed-specific overexpression of phytoene synthase: increase in carotenoids and other metabolic effects . Plant J , 20 : 401 – 412 .
  • Simkin , A. J. , Schwartz , S. H. , Auldridge , M. , Taylor , M. G. and Klee , H. J. 2004a . The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles ?-ionone, pseudoionone, and geranylacetone . Plant J , 40 : 882 – 892 .
  • Simkin , A. J. , Underwood , B. A. , Auldridge , M. , Loucas , H. M. , Shibuya , K. , Schmelz , E. , Clark , D. G. and Klee , H. J. 2004b . Circadian regulation of the PhCCD1 carotenoid cleavage dioxygenase controls emission of ?-ionone, a fragrance volatile of petunia flowers . Plant Physiol , 136 : 3504 – 3514 .
  • Simkin , A. J. , Gaffe , J. , Alcaraz , J. P. , Carde , J. P. , Bramley , P. M. , Fraser , P. D. and Kuntz , M. 2007 . Fibrillin influence on plastid ultrastructure and pigment content in tomato fruit . Phytochem , 68 : 1545 – 1556 .
  • Singh , A. , Reimer , S. , Pozniak , C. J. , Clarke , F. R. , Clarke , J. M. , Knox , R. E. and Singh , A. K. 2009 . Allelic variation at Psy1-A1 and association with yellow pigment in durum wheat grain . Theor Appl Genet , 118 : 1539 – 1548 .
  • Snowden , K. C. , Simkin , A. J. , Janssen , B. J. , Templeton , K. R. , Loucas , H. M. , Simons , J. L. , Karunairetnam , S. , Gleave , A. P. , Clark , D. G. and Klee , H. J. 2005 . The Decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development . Plant Cell , 17 : 746 – 759 .
  • Stålberg , K. , Lindgren , O. , Ek , B. and Höglund , A. S. 2003 . Synthesis of ketocarotenoids in the seed of Arabidopsis thaliana . Plant J , 36 : 771 – 779 .
  • Surles , R. L. , Weng , N. , Simon , P. W. and Tanumihardjo , S. A. 2004 . Carotenoid profiles and consumer sensory evaluation of specialty carrots (Daucus carota L.) of various colors . J Agric Food Chem , 52 : 3417 – 3421 .
  • Tan , B. C. , Joseph , L. M. , Deng , W. T. , Liu , L. , Li , Q. B. , Cline , K. and McCarty , D. R. 2003 . Molecular characterization of the Arabidopsis 9-cis-epoxycarotenoid dioxygenase gene family . Plant J , 35 : 44 – 56 .
  • Vallabhaneni , R. and Wurtzel , E. T. 2009 . Timing and biosynthetic potential for carotenoid accumulation in genetically diverse germplasm of maize . Plant Physiol , 150 : 562 – 572 .
  • Winterhalter , P. and Rouseff , R. L. , eds. 2001 . Carotenoid-derived aroma compounds , Washington DC : American Chemical Society .
  • Wurbs , D. , Ruf , S. and Bock , R. 2007 . Contained metabolic engineering in tomatoes by expression of carotenoid biosynthesis genes from the plastid genome . Plant J , 49 : 276 – 288 .
  • Ye , X. , Al-Babili , S. , Zhang , J. , Lucca , P. , Beyer , P. and Potrykus , I. 2000 . Engineering the pro-vitamin A (?-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm . Science , 287 : 303 – 305 .
  • Yu , B. , Lydiate , D. J. , Young , L. W. , SchÄfer , U. A. and Hannoufa , A. 2008 . Enhancing the carotenoid content of Brassica napus seeds by downregulating lycopene epsilon cyclase . Transgenic Res , 17 : 573 – 585 .
  • Zhu , C. , Gerjets , T. and Sandmann , G. 2007a . Nicotiana glauca engineered for the production of ketocarotenoids in flowers and leaves by expressing the cyanobacterial crtO ketolase gene . Transgenic Res , 16 : 813 – 821 .
  • Zhu , C. F. , Kauder , F. , Römer , S. and Sandmann , G. 2007b . Cloning of two individual cDNAS encoding 9-cis-epoxycarotenoid dioxygenase from Gentiana lutea, their tissue-specific expression and physiological effect in transgenic tobacco . J Plant Physiol , 164 : 195 – 204 .
  • Zhu , C. , Naqvi , S. , Breitenbach , J. , Sandmann , G. , Christou , P. and Capell , T. 2008 . Combinatorial genetic transformation generates a library of metabolic phenotypes for the carotenoid pathway in maize . Proc Natl Acad Sci USA , 105 : 18232 – 18237 .

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.