Carotenoid Biosynthesis and Regulation in Plants

Carotenoids in Nutrition: Therapy, Spectroscopy and Technology

Volumn , Issue , 2016, Pages 159-189

  Baranski, Rafal ^a   Cazzonelli, Christopher I ^b  

^a UNIVERSITY OF AGRICULTURE IN KRAKOW   (Poland)

^b WESTERN SYDNEY UNIVERSITY   (Australia)

Author keywords

Biofortification; Carotenoid biosynthesis; Carotenoid degradation; Enzyme localization; Epigenetic regulatory mechanisms; MEP pathways; Metabolon compartmentalization; Photosynthesis; Plastid differentiation; Posttranscriptional regulatory mechanisms

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; ENZYMES; MOLECULES; PHOTOOXIDATION; PHOTOSYNTHESIS;

BIOFORTIFICATION; CAROTENOID BIOSYNTHESIS; MEP PATHWAYS; METABOLON; REGULATORY MECHANISM;

PIGMENTS;

EID: 84976897939     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781118622223.ch10     Document Type: Chapter

References (175)

1. C. I. Cazzonelli, "Carotenoids in nature: insights from plants and beyond," Funct. Plant Biol., 38, 833-47 (2011).
2. S. Takaichi, "Carotenoids in algae: distributions, biosyntheses and functions," Marine Drugs, 9, 1101-18 (2011).
3. N. A. Moran and T. Javik, "Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science, 328, 624-7 (2010).
4. E. Novakova and N. A. Moran, "Diversification of genes for carotenoid biosynthesis in aphids following an ancient transfer from a fungus," Mol. Biol. Evol., 29, 313-23 (2012).
5. M. Grbić, T. Van Leeuwen, R. M. Clark, S. Rombauts, P. Rouze, V. Grbić, et al., "The genome of Tetranychus urticae reveals herbivorous pest adaptations," Nature, 479, 487-92 (2011).
6. B. Altincicek, J. L. Kovacs, and N. M. Gerardo, "Horizonatally transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae," Biol. Lett., 8, 253-7 (2012).
7. C. Cobbs, J. Heath, J. O. Stireman III, and P. Abbot, "Carotenoids in unexpected places: Gall midges, lateral gene transfer, and carotenoid biosynthesis in animals," Mol. Phylogen. Evol., 68, 221-8 (2013).
8. L. Boto, "Horizontal gene transfer in the acquisition of novel traits by metazoans," Proc. Royal Soc. London B, 281, 2013-450 (2014).
9. K. Wang and S.-I. Ohnuma, "Chain-length determination mechanism of isoprenyl diphosphate synthases and implications for molecular evolution," Trends Biochem. Sci., 24, 445-51 (1999).
10. V. M. Ye and S. K. Bhatia, "Metabolic engineering strategies for the production of beneficial carotenoids in plants," Food Sci. Biotech., 21, 1511-7 (2012).
11. D. Kim, M. R. Filtz, and P. J. Proteau, "The methylerythritol phosphate pathway contributes to carotenoid but not phytol biosynthesis in Euglena gracilis," J. Nat. Products, 67, 1067-9 (2004).
12. IUPAC-IUB, "Nomenclature of carotenoids," 1974, http://www.chem.qmul.ac.uk/iupac/ carot/ (last accessed July 2, 2015).
13. S. Takaichi, K. Inoue, M. Akaike, M. Kobayashi, H. Oh-oka, and M. T. Madigan, "The major carotenoid in all known species of heliobacteria is the C30 carotenoid 4,4'-diaponeurosporene, not neurosporene," Arch. Microbiol., 168, 277-81 (1997).
14. F. Wang, J. G. Jiang, and Q. Chen, "Progress on molecular breeding and metabolic engineering of biosynthesis pathways of C30, C35, C40, C45, C50 carotenoids," Biotechnol. Adv., 25, 211-22 (2007).
15. D. Umeno, A. V. Tobias, and F. H. Arnold, "Diversifying carotenoid biosynthetic pathways by directed evolution," Microbiol. Mol. Biol. Rev., 69, 51-78 (2005).
16. P. M. Dewick, "The biosynthesis of C5-C25 terpenoid compounds," Nat. Prod. Rep., 19, 181-222 (2002).
17. M. Rodriguez-Concepción and A. Boronat, "Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics," Plant Physiol., 130, 1079-89 (2002).
18. A. R. Moise, S. Al-Babili, and E. T. Wurtzel, "Mechanistic aspects of carotenoid biosynthesis," Chem. Rev., 114, 164-93 (2014).
19. O. B. Weeks, A. G. Andrewes, B. O. Brown, et al., "Occurrence of C40 and C45 carotenoids in the C50 carotenoid system of Flavobacterium dehydrogenans," Nature, 224, 879-82 (1969).
20. P. Krubasik, M. Kobayashi, and G. Sandmann, "Expression and functional analysis of gene cluster involved in the synthesis of decaprenoxanthin reveals the mechanisms for C50 carotenoid formation," Euro. J. Biochem., 268, 3702-8 (2001).
21. L. Tao, H. Yao, and Q. Cheng, "Genes from a Dietzia sp. for synthesis of C40 and C50 betacyclic carotenoids," Gene, 386, 90-7 (2007).
22. R. Netzer, M. H. Stafsnes, T. Andreassen, A. Goksøyr, P. Bruheim, and T. Brautaset, "Biosynthetic pathway for γ-cyclic sarcinaxanthin in Micrococcus luteus: heterologous expression and evidence for diverse and multiple catalytic functions of C(50) carotenoid cyclases," J. Bacteriol., 192, 5688-99 (2010).
23. D. Umeno and F. H. Arnold, "A C35 carotenoid biosynthetic pathway," Appl. Environ. Microbiol., 69, 3573-9 (2003).
24. V. S. Dubey, R. Bhalla, and R. Luthra, "An overview of the non-mevalonate pathway for terpenoid biosynthesis in plants," J. Biosci., 28, 637-46 (2003).
25. F. J. Cunningham and E. Gantt, "Genes and enzymes of carotenoid biosynthesis in plants," Ann. Rev. Plant Physiol. Plant Mol. Biol., 49, 557-83 (1998).
26. J. Hirschberg, "Carotenoid biosynthesis in flowering plants," Curr. Opin. Plant Biol., 4, 210-18 (2001).
27. P. D. Fraser and P. M. Bramley, "The biosynthesis and nutritional uses of carotenoids," Prog. Lipid Res., 43, 228-65 (2004).
28. C. Rosati, G. Diretto, and G. Giuliano, "Biosynthesis and engineering of carotenoids and apocarotenoids in plants: state of the art and future prospects," Biotech. Gen. Engin. Rev., 26, 151-74 (2009).
29. M. H. Walter and D. Strack, "Carotenoids and their cleavage products: Biosynthesis and functions," Nat. Products Rep., 28, 663-92 (2011).
30. M. A. Ruiz-Sola and M. Rodriguez-Concepcion, "Carotenoid biosynthesis in Arabidopsis:a colorful pathway," Arabidopsis Book, 10, e0158 (2012).
31. G. Giuliano, "Plant carotenoids: genomics meets multi-gene engineering," Curr. Opin. Plant Biol., 19, 111-7 (2014).
32. G. Giuliano, L. Giliberto, and C. Rosati, "Carotenoid isomerase: a tale of light and isomers," Trends Plant Sci., 7, 427-9 (2002).
33. T. Isaacson, G. Ronen, D. Zamir, and J. Hirschberg, "Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of beta-carotene and xanthophylls in plants," Plant Cell, 14, 333-42 (2002).
34. H. Park, S. S. Kreunen, A. J. Cuttriss, D. DellaPenna, and B. J. Pogson, "Identification of the carotenoid isomerase provides insight into carotenoid biosynthesis, prolamellar body formation, and photomorphogenesis," Plant Cell, 14, 321-32 (2002).
35. D. B. Rodriguez-Amaya, A guide to carotenoid analysis in foods, Washington, DC: ILSI (International Life Sciences Institute) Press, 2001.
36. R. F. Quinlan, M. Shumskaya, L. M. T. Bradbury, J. Beltrán, C. Ma, E. J. Kennelly, and E. T. Wurtzel, "Synergistic interactions between carotene ring hydroxylases drive lutein formation in plant carotenoid biosynthesis," Plant Physiol., 160, 204-14 (2012).
37. J. E. Kim, K. M. Cheng, N. E. Craft, B. Hamberger, and C. J. Douglas, "Overexpression of Arabidopsis thaliana carotenoid hydroxylases individually and in combination with a β-carotene ketolase provides insight into in vivo functions," Phytochemistry, 71, 168-78 (2010).
38. S. Bak, F. Beisson, G. Bishop, B. Hamberger, R. Höfer, S. Paquette, and D. Werck-Reichhart, "Cytochromes P450," Arabidopsis Book, 9, e0144 (2011).
39. L.-E. Yang, X.-Q. Huang, Y. Hang, Y.-Y. Deng, Q.-Q. Lu, and S. Lu, "The P450-type carotene hydroxylase PuCHY1 from Porphyra suggests the evolution of carotenoid metabolism in red algae," J. Integr. Plant Biol., 56, 902-15 (2014).
40. D. Siefermann-Harms, S. Hertzberg, G. Borch, and S. Liaaen-Jensen, "Lactucaxanthin, an ε,ε-carotene-3,3'-diol from Lactuca sativa," Phytochemistry, 20, 85-8 (1981).
41. J. Deli, P. Molnar, Z. Matus, and G. Toth, "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, 1517-23 (2001).
42. I. Guzman, S. Hamby, J. Romero, P. W. Bosland, and M. A. O'Connell, "Variability of carotenoid biosynthesis in orange colored Capsicum spp.," Plant Sci., 179, 49-59 (2010).
43. M. Yamagishi, S. Kishimoto, and M. Nakayama, "Carotenoid composition and changes in expression of carotenoid biosynthetic genes in tepals of Asiatic hybrid lily," Plant Breeding, 129, 100-7 (2010).
44. M. R. Gomez-García and N. Ochoa-Alejo, "Biochemistry and molecular biology of carotenoid biosynthesis in chili peppers (Capsicum spp.)," Intl. J. Mol. Sci., 14, 19025-53 (2013).
45. P. Hugueney, A. Badillo, H. Chen, A. Klein, J. Hirschberg, B. Camara, and M. Kuntz, "Metabolism of cyclic carotenoids: a model for the alteration of this biosynthetic pathway in Capsicum annuum chromoplasts," Plant J., 8, 417-24 (1995).
46. Z. Jeknić, J. T. Morré, S. Jeknić, S. Javremović, A. Subotić, and T. H. H. Chen "Cloning and functional characterization of a gene for capsanthin/capsorubin synthase from tiger lily (Lilium lancifolium Thunb 'Splendens')," Plant Cell Physiol., 53, 1899-912 (2012).
47. M. Yamagishi, "How genes paint lily flowers: Regulation of colouration and pigmentation patterning," Scienta Horticulturae, 163, 27-36 (2013).
48. T. Maoka, T. Etoh, S. Kishimoto, and S. Sakata, "Carotenoids and their fatty acid esters in the petals of Adonis aestivalis," J. Oleo Sci., 60, 47-52 (2011).
49. Y. Wang and T. Chen, "The biosynthetic pathway of carotenoids in the astaxanthin-producing green alga Chlorella zofingiensis," World J. Microbiol Biotech., 24, 2927-32 (2008).
50. D. Han, Y. Li, and Q. Hu, "Astaxanthin in microalgae: pathways, functions and biotechnological implications," Algae, 28, 131-47 (2013).
51. T. Matsuno, "Aquatic animal carotenoids," Fisheries Sci., 67, 771-83 (2001).
52. F. X. Cunningham and E. Gantt, "Elucidation of the pathway to astaxanthin in the flowers of Adonis aestivalis," Plant Cell, 23, 3055-69 (2011).
53. M. Bertrand, "Carotenoid biosynthesis in diatoms," Phytosynthesis Res., 106, 89-102 (2010).
54. M. Dambek, U. Eilers, J. Breitenbach, S. Steiger, C. Büchel, and G. Sandmann, "Biosynthesis of fucoxanthin and diadinoxanthin and function of initial pathway genes in Phaeodactylum tricornutum," J. Exper. Botany, 63, 5607-12 (2012).
55. P. Heydarizadeh, I. Poirer, D. Loizeau, L. Ulmann, V. Mimouni, B. Schoefs, and M. Bertrand, "Plastids of marine phytoplankton produce bioactive pigments and lipids," Marine Drugs, 11, 3425-71 (2013).
56. S. R. Kumar, M. Hosokawa, and K. Miyashita, "Fucoxanthin: a marine carotenoid exerting anti-cancer effects by affecting multiple mechanisms," Marine Drugs, 11, 5130-47 (2013).
57. E. Christaki, E. Bonos, I. Giannenas, and P. Flotou-Paneri, "Functional properties of carotenoids originating from algae," J. Sci. Food Agric., 93, 5-11 (2013).
58. K. Mikami and M. Hosokawa, "Biosynthetic pathway and health benefits of fucoxanthin, an algae-specific xanthophyll in brown seaweeds," Int. J. Mol. Sci., 14, 13763-81 (2013).
59. S. Römer, P. D. Fraser, J. W. Kiano, C. A. Shipton, N. Misawa, W. Schuch, and P. M. Bramley, "Elevation of the provitamin A content of transgenic tomato plants," Nature Biotechnol., 18, 666-9 (2000).
60. P. Beyer, S. Al-Babili, X. Ye, P. Lucca, P. Schaub, R. Welsch, and I. Potrykus, "Golden Rice:introducing the beta-carotene biosynthesis pathway into rice endosperm by genetic engineering to defeat vitamin A deficiency," J. Nutr., 132, 506S-10S (2002).
61. A. J. Cuttriss, A. Chubb, A. Alawady, B. Grimm, and B. Pogson, "Regulation of lutein biosynthesis and prolamellar body formation in Arabidopsis," Funct. Plant Biol., 34, 663-72 (2007).
62. G. Qin, H. Gu, L. Ma, Y. Peng, X. W. Deng, Z. Chen, and L. J. Qu, "Disruption of phytoene desaturase gene results in albino and dwarf phenotypes in Arabidopsis by impairing chlorophyll, carotenoid, and gibberellin biosynthesis," Cell Res., 17, 471-82 (2007).
63. F. Li, R. Vallabhaneni, and E. T. Wurtzel, "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, 1333-45 (2008a).
64. R. Welsch, F. Wust, C. Bar, S. Al-Babili, and P. Beyer, "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., 147, 367-80 (2008).
65. L. Bai, E. H. Kim, D. DellaPenna, and T. P. Brutnell, "Novel lycopene epsilon cyclase activities in maize revealed through perturbation of carotenoid biosynthesis," Plant J., 59, 588-99 (2009).
66. D. E. Kachanovsky, S. Filler, T. Isaacson, and J. Hirschberg, "Epistasis in tomato color mutations involves regulation of phytoene synthase 1 expression by cis-carotenoids," Proc. Natl. Acad. Sci. USA, 109, 19021-6 (2012).
67. E. Fantini, G. Falcone, S. Frusciante, L. Giliberto, and G. Giuliano, "Dissection of tomato lycopene biosynthesis through virus-induced gene silencing," Plant Physiol., 163, 986-98 (2013).
68. J. Arango, M. Jourdan, E. Geoffriau, P. Beyer, and R. Welsch, "Carotene hydroxylase activity determines the levels of both alpha-carotene and total carotenoids in orange carrots," Plant Cell, 26, 2223-33 (2014).
69. L. P. Wright, J. M. Rohwer, A. Ghirardo, A. Hammerbacher, M. Ortiz-Alcaide, B. Raguschke, J. P. Schnitzler, J. Gershenzon, and M. A. Phillips, "Deoxyxylulose 5-phosphate synthase controls flux through the methylerythritol 4-phosphate pathway in Arabidopsis," Plant Physiol., 165, 1488-504 (2014).
70. A. Rodriguez-Villalon, E. Gas, and M. Rodriguez-Concepcion, "Colors in the dark: a model for the regulation of carotenoid biosynthesis in etioplasts," Plant Sign. Behav., 4, 965-7 (2009a).
71. C. I. Cazzonelli and B. J. Pogson, "Source to sink: regulation of carotenoid biosynthesis in plants," Trends Plant Sci., 15, 266-74 (2010).
72. A. J. Thompson, B. J. Mulholland, A. C. Jackson, J. M. McKee, H. W. Hilton, R. C. Symonds, T. Sonneveld, A. Burbidge, P. Stevenson, and I. B. Taylor, "Regulation and manipulation of ABA biosynthesis in roots," Plant Cell Environ., 30, 67-78 (2007).
73. F. Li, R. Vallabhaneni, J. Yu, T. Rocheford, and E. T. Wurtzel, "The maize phytoene synthase gene family: overlapping roles for carotenogenesis in endosperm, photomorphogenesis, and thermal stress tolerance," Plant Physiol., 147, 1334-46 (2008b).
74. M. L. Perez-Bueno and P. Horton, "The role of lutein in the acclimation of higher plant chloroplast membranes to suboptimal conditions," Physiol. Plant., 134, 227-36 (2008).
75. A. L. Fanciullino, L. P. Bidel, and L. Urban, "Carotenoid responses to environmental stimuli: integrating redox and carbon controls into a fruit model," Plant Cell Environ., 37, 273-89 (2014).
76. L. Liu, Z. Shao, M. Zhang, and Q. Wang, "Regulation of carotenoid metabolism in tomato," Mol. Plant (2014), DOI: 10.1093/mp/ssu121.
77. M. A. Ruiz-Sola, V. Arbona, A. Gomez-Cadenas, M. Rodriguez-Concepcion, and A. Rodriguez-Villalon, "A root specific induction of carotenoid biosynthesis contributes to ABA production upon salt stress in arabidopsis," PLoS ONE, 9, e90765 (2014).
78. Z. Zhang, L. Liu, M. Zhang, Zhang Y., and Q. Wang, "Effect of carbon dioxide enrichment on health-promoting compounds and organoleptic properties of tomato fruits grown in greenhouse," Food Chem., 153, 157-63 (2014b).
79. C. A. Howitt and B. J. Pogson, "Carotenoid accumulation and function in seeds and nongreen tissues," Plant Cell Environ., 29, 435-45 (2006).
80. M. Ghassemian, J. Lutes, J. M. Tepperman, H. S. Chang, T. Zhu, X. Wang, P. H. Quail, and B. M. Lange, "Integrative analysis of transcript and metabolite profiling data sets to evaluate the regulation of biochemical pathways during photomorphogenesis," Arch. Biochem. Biophys., 448, 45-59 (2006).
81. A. Castillon, H. Shen, and E. Huq, "Phytochrome Interacting Factors: central players in phytochrome-mediated light signaling networks," Trends Plant Sci., 12, 514-21 (2007).
82. C. Stange and C. Flores, "Carotenoids and photosynthesis: regulation of carotenoid biosyntesis by photoreceptors," in M. Najafpour (ed.), Advances in photosynthesis: fundamental aspects, Zagreb, Croatia: InTech, 2012.
83. S. Römer and P. D. Fraser, Recent advances in carotenoid biosynthesis, regulation and manipulation," Planta, 221, 305-8 (2005).
84. A. Rodriguez-Villalon, E. Gas, and M. Rodriguez-Concepcion, "Phytoene synthase activity controls the biosynthesis of carotenoids and the supply of their metabolic precursors in dark-grown Arabidopsis seedlings," Plant J., 60, 424-35 (2009b).
85. J. von Lintig, R. Welsch, M. Bonk, G. Giuliano, A. Batschauer, and H. Kleinig, "Lightdependent 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, 625-34 (1997).
86. P. Botella-Pavia, O. Besumbes, M. A. Phillips, L. Carretero-Paulet, A. Boronat, and M. Rodriguez-Concepcion, "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, 188-99 (2004).
87. G. Toledo-Ortiz, E. Huq, and M. Rodriguez-Concepcion, "Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors," Proc. Natl. Acad. Sci. USA, 107, 11626-31 (2010).
88. S. Meier, O. Tzfadia, R. Vallabhaneni, C. Gehring, and E. T. Wurtzel, "A transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thaliana," BMC Systems Biol., 5, 77 (2011).
89. S. Woitsch and S. Romer, "Expression of xanthophyll biosynthetic genes during lightdependent chloroplast differentiation," Plant Physiol., 132, 1508-17 (2003).
90. P. Leivar and P. H. Quail, "PIFs: pivotal components in a cellular signaling hub," Trends Plant Sci., 16, 19-28 (2011).
91. P. M. Bramley, "Regulation of carotenoid formation during tomato fruit ripening and development," J. Exper. Botany, 53, 2107-13 (2002).
92. G. Giuliano and G. Diretto, "Of chromoplasts and chaperones," Trends Plant Sci., 12, 529-31 (2007).
93. I. Pecker, D. Chamovitz, H. Linden, G. Sandmann, and J. Hirschberg, "A single polypeptide catalyzing the conversion of phytoene to zeta-carotene is transcriptionally regulated during tomato fruit ripening," Proc. Natl. Acad. Sci. USA, 89, 4962-6 (1992).
94. V. Corona, B. Aracri, G. Kosturkova, G. E. Bartley, L. Pitto, L. Giorgetti, P. A. Scolnik, and G. Giuliano, "Regulation of a carotenoid biosynthesis gene promoter during plant development," Plant J., 9, 505-12 (1996).
95. L. M. Lois, M. Rodriguez-Concepcion, F. Gallego, N. Campos, and A. Boronat, "Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-D-xylulose 5-phosphate synthase," Plant J., 22, 503-13 (2000).
96. J. Giovannoni, "Molecular biology of fruit maturation and ripening," Ann. Rev. Plant Physiol. Plant Mol. Biol., 52, 725-49 (2001).
97. C. P. Moehs, L. Tian, K. W. Osteryoung, and D. DellaPenna, "Analysis of carotenoid biosynthetic gene expression during marigold petal development," Plant Mol. Biol., 45, 281-93 (2001).
98. G. Ronen, M. Cohen, D. Zamir, and J. Hirschberg, "Regulation of carotenoid biosynthesis during tomato fruit development: expression of the gene for lycopene epsilon-cyclase is down-regulated during ripening and is elevated in the mutant Delta," Plant J., 17, 341-51 (1999).
99. G. Giuliano, G. E. Bartley, and P. A. Scolnik, "Regulation of carotenoid biosynthesis during tomato development," Plant Cell, 5, 379-87 (1993).
100. P. D. Fraser, M. R. Truesdale, C. R. Bird, W. Schuch, and P. M. Bramley, "Carotenoid biosynthesis during tomato fruit development (evidence for tissue-specific gene expression)," Plant Physiol., 105, 405-13 (1994).
101. I. Pecker, R. Gabbay, F. X. Cunningham, and J. Hirschberg, "Cloning and characterization of the cDNA for lycopene β-cyclase from tomato reveals decrease in its expression during fruit ripening," Plant Mol. Biol., 30, 807-19 (1996).
102. M. Dalal, V. Chinnusamy, and K. C. Bansal, "Isolation and functional characterization of lycopene beta-cyclase (CYC-B) promoter from Solanum habrochaites," BMC Plant Biol., 10, 61 (2010).
103. C. I. Cazzonelli, K. Yin, and B. J. Pogson, "Potential implications for epigenetic regulation of carotenoid biosynthesis during root and shoot development," Plant Signal Behav., 4, 339-41 (2009a).
104. C. I. Cazzonelli, A. J. Cuttriss, S. B. Cossetto, W. Pye, P. Crisp, J. Whelan, E. J. Finnegan, C. Turnbull, and B. J. Pogson, "Regulation of carotenoid composition and shoot branching in Arabidopsis by a chromatin modifying histone methyltransferase, SDG8," Plant Cell, 21, 39-53 (2009b).
105. C. I. Cazzonelli, T. Millar, E. J. Finnegan, and B. J. Pogson, "Promoting gene expression in plants by permissive histone lysine methylation," Plant Signal Behav., 4, 484-8 (2009c).
106. C. I. Cazzonelli, A. C. Roberts, M. E. Carmody, and B. J. Pogson, "Transcriptional control of set domain group8 and carotenoid isomerase during Arabidopsis development," Molecular Plant, 3, 174-91 (2010).
107. S. Wei, B. Yu, M. Y. Gruber, G. G. Khachatourians, D. D. Hegedus, and A. Hannoufa, "Enhanced seed carotenoid levels and branching in transgenic Brassica napus expressing the Arabidopsis miR156b gene," J. Agric. Food Chem., 58, 9572-8 (2010).
108. S. Wei, M. Y. Gruber, B. Yu, M. J. Gao, G. G. Khachatourians, D. D. Hegedus, I. A. Parkin, and A. Hannoufa, "Arabidopsis mutant sk156 reveals complex regulation of SPL15 in a miR156-controlled gene network," BMC Plant Biol., 12, 169 (2012).
109. G. Dong and J. Li, "MicroRNAs profiling reveals a potential link between the SDG8 methyltransferase and brassinosteroid-regulated gene expression in Arabidopsis," Data Mining Genom. Proteom., 4, e110 (2013).
110. L. L. Lin, C. C. Wu, H. C. Huang, H. J. Chen, Hsieh H. L., and H. F. Juan, "(2013) Identification of MicroRNA 395a in 24-epibrassinolide-regulated root growth of Arabidopsis thaliana using MicroRNA arrays," Intl. J. Mol. Sci., 14, 14270-86 (2013).
111. A. Berr, E. J. McCallum, A. Alioua, D. Heintz, T. Heitz, and W. H. Shen, "Arabidopsis histone methyltransferase Set Domain Group8 mediates induction of the jasmonate/ ethylene pathway genes in plant defense response to necrotrophic fungi," Plant Physiol., 154, 1403-14 (2010).
112. C. I. Cazzonelli, N. Nisar, A. C. Roberts, K. D. Murray, J. O. Borevitz, and B. J. Pogson, "A chromatin modifying enzyme, SDG8, is involved in morphological, gene expression, and epigenetic responses to mechanical stimulation," Frontiers Plant Sci., 5, 533 (2014).
113. X. Wang, J. Chen, Z. Xie, S. Liu, T. Nolan, H. Ye, M. Zhang, H. Guo, P. S. Schnable, Z. Li, and Y. Yin, "Histone lysine methyltransferase SDG8 is involved in brassinosteroid-regulated gene expression in Arabidopsis thaliana," Molecular Plant, 7, 1303-15 (2014).
114. D. Maass, J. Arango, F. Wust, P. Beyer, and R. Welsch, "Carotenoid crystal formation in Arabidopsis and carrot roots caused by increased phytoene synthase protein levels," PLoS ONE, 4, e6373 (2009).
115. M. Vishnevetsky, M. Ovadis, and A. Vainstein, "Carotenoid sequestration in plants: the role of carotenoid-associated proteins," Trends Plant Sci., 4, 232-5 (1999).
116. D. J. Paolillo, Jr., D. F. Garvin, and M. V. Parthasarathy, "The chromoplasts of Or mutants of cauliflower (Brassica oleracea L. var. botrytis)," Protoplasma, 224, 245-53 (2004).
117. S. Lu, J. V. 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. Küpper, E. D. Earle, J. Cao, and L. Li, "The cauliflower Or gene encodes a DnaJ cysteine-rich domain-containing protein that mediates high levels of β-carotene accumulation," Plant Cell, 18, 3594-605 (2006).
118. I. Neta-Sharir, T. Isaacson, S. Lurie, and D. Weiss, "Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation," Plant Cell, 17, 1829-38 (2005).
119. Y. S. Liu, S. Roof, Z. B. Ye, C. Barry, A. van Tuinen, J. Vrebalov, C. Bowler, and J. Giovannoni, "Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato," Proc. Natl. Acad. Sci. USA, 101, 9897-902 (2004).
120. G. R. Davuluri, van A. Tuinen, P. D. Fraser, A. Manfredonia, R. Newman, D. Burgess, D. A. Brummell, S. R. King, J. Palys, J. Uhlig, P. M. Bramley, H. M. Pennings, and C. Bowler, "Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes," Nature Biotechnol., 23, 890-5 (2005).
121. I. Kolotilin, H. Koltai, Y. Tadmor, C. Bar-Or, M. Reuveni, A. Meir, S. Nahon, H. Shlomo, L. Chen, and I. Levin, "Transcriptional profiling of high pigment-2dg tomato mutant links early fruit plastid biogenesis with its overproduction of phytonutrients," Plant Physiol., 145, 389-401 (2007).
122. R. Azari, M. Reuveni, D. Evenor, S. Nahon, H. Shlomo, L. Chen, and I. Levin, "Overexpression of UV-Damaged DNA Binding Protein 1 links plant development and phytonutrient accumulation in high pigment-1 tomato," J. Exper. Botany, 61, 3627-37 (2010).
123. N. Galpaz, Q. Wang, N. Menda, D. Zamir, and J. Hirschberg, "Abscisic acid deficiency in the tomato mutant high-pigment 3 leading to increased plastid number and higher fruit lycopene content," Plant J., 53, 717-30 (2008).
124. B. J. Pogson, N. S. Woo, B. Forster, and I. D. Small, "Plastid signalling to the nucleus and beyond," Trends Plant Sci., 13, 602-9 (2008).
125. A. O. Avendano-Vazquez, E. Cordoba, E. Llamas, C. San Roman, N. Nisar, S. De la Torre, M. Ramos-Vega, M. D. Gutierrez-Nava, C. I. Cazzonelli, B. J. Pogson, and P. Leon, "An uncharacterized apocarotenoid-derived signal generated in zeta-carotene desaturase mutants regulates leaf development and the expression of chloroplast and nuclear genes in Arabidopsis," Plant Cell, 26, 2524-37 (2014).
126. K. Jorgensen, A. V. Rasmussen, M. Morant, A. H. Nielsen, N. Bjarnholt, M. Zagrobelny, S. Bak, and B. L. Moller, "Metabolon formation and metabolic channeling in the biosynthesis of plant natural products," Curr. Opin. Plant Biol., 8, 280-91 (2005).
127. M. Shumskaya and E. T. Wurtzel, "The carotenoid biosynthetic pathway: thinking in all dimensions," Plant Sci., 208, 58-63 (2013).
128. S. Al-Babili, J. von Lintig, H. Haubruck, and P. Beyer, "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, 601-12 (1996).
129. M. Bonk, B. Hoffmann, J. Von Lintig, M. Schledz, S. Al-Babili, E. Hobeika, H. Kleinig, and P. Beyer, "Chloroplast import of four carotenoid biosynthetic enzymes in vitro reveals differential fates prior to membrane binding and oligomeric assembly," Euro. J. Biochem., 247, 942-50 (1997).
130. A. B. Lopez, Y. Yang, T. W. Thannhauser, and L. Li, "Phytoene desaturase is present in a large protein complex in the plastid membrane," Physiol. Plant., 133, 190-8 (2008).
131. A. Kostecka-Gugała, D. Latowski, and K. Strzałka, "Thermotropic phase behaviour of α-dipalmitoylphosphatidylcholine multibilayers is influenced to various extents by carotenoids containing different structural features: evidence from differential scanning calorimetry," Biochim. Biophys. Acta Biomemb., 1609, 193-202 (2003).
132. W. I. Gruszecki and K. Strzalka, "Carotenoids as modulators of lipid membrane physical properties," Biochim Biophys Acta, 1740, 108-15 (2005).
133. G. Britton, "Structure and properties of carotenoids in relation to function," FASEB J., 9, 1551-8 (1995).
134. W. W. Fish, "Interaction of sodium dodecyl sulfate with watermelon chromoplasts and examination of the organization of lycopene within the chromoplasts," J. Agric. Food Chem., 54, 8294-300 (2006).
135. M. Shumskaya, L. M. Bradbury, R. R. Monaco, and E. T. Wurtzel, "Plastid localization of the key carotenoid enzyme phytoene synthase is altered by isozyme, allelic variation, and activity," Plant Cell, 24, 3725-41 (2012).
136. K. G. Beisel, S. Jahnke, D. Hofmann, S. Koppchen, U. Schurr, and S. Matsubara, "Continuous turnover of carotenes and chlorophyll a in mature leaves of Arabidopsis revealed by 14CO2 pulse-chase labeling," Plant Physiol., 152, 2188-99 (2010).
137. S. Gonzalez-Perez, J. Gutierrez, F. Garcia-Garcia, D. Osuna, J. Dopazo, O. Lorenzo, J. L. Revuelta, and J. B. Arellano, "Early transcriptional defense responses in Arabidopsis cell suspension culture under high-light conditions," Plant Physiol., 156, 1439-56 (2011).
138. F. Leenhardt, B. Lyan, E. Rock, A. Boussard, J. Potus, E. Chanliaud, and C. Remesy, "Genetic variability of carotenoid concentration, and lipoxygenase and peroxidase activities among cultivated wheat species and bread wheat varieties," Euro. J. Agron., 25, 170-6 (2006).
139. A. J. Simkin, S. H. Schwartz, M. Auldridge, M. G. Taylor, and H. J. Klee, "The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles beta-ionone, pseudoionone, and geranylacetone," Plant J., 40, 882-92 (2004).
140. L. M. Bradbury, M. Shumskaya, O. Tzfadia, S. B. Wu, E. J. Kennelly, and E. T. Wurtzel, "Lycopene cyclase paralog CruP protects against reactive oxygen species in oxygenic photosynthetic organisms," Proc. Natl. Acad. Sci. USA, 109, E1888-97 (2012).
141. F. Ramel, S. Birtic, C. Ginies, L. Soubigou-Taconnat, C. Triantaphylides, and M. Havaux, "Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants," Proc. Natl. Acad. Sci. USA, 109, 5535-40 (2012).
142. M. Havaux, "Carotenoid oxidation products as stress signals in plants," Plant J., 79, 597-606 (2014).
143. F. Bouvier, J. C. Isner, O. Dogbo, and B. Camara, "Oxidative tailoring of carotenoids: a prospect towards novel functions in plants," Trends Plant Sci., 10, 187-94 (2005).
144. E. Lewinsohn, Y. Sitrit, E. Bar, Y. Azulay, M. Ibdah, A. Meir, E. Yosef, D. Zamir, and Y. Tadmor, "Not just colors: carotenoid degradation as a link between pigmentation and aroma in tomato and watermelon fruit," Trends Food Sci. Tech., 16, 407-15 (2005).
145. P. J. Harrison and T. D. H. Bugg, "Enzymology of the carotenoid cleavage dioxygenases:reaction mechanisms, inhibition and biochemical roles," Arch. Biochem. Biophys., 544, 105-11 (2014).
146. R. Campbell, L. J. Ducreux, W. L. Morris, J. A. Morris, J. C. Suttle, G. Ramsay, G. J. Bryan, P. E. Hedley, and M. A. Taylor, "The metabolic and developmental roles of carotenoid cleavage dioxygenase4 from potato," Plant Physiol., 154, 656-64 (2010).
147. R. Vallabhaneni, L. M. Bradbury, and E. T. Wurtzel, "The carotenoid dioxygenase gene family in maize, sorghum, and rice," Arch. Biochem. Biophys., 504, 104-11 (2010).
148. R. Finkelstein, "Abscisic acid synthesis and response," Arabidopsis Book, 11, e0166 (2013).
149. M. Seo and T. Koshiba, "Complex regulation of ABA biosynthesis in plants," Trends Plant Sci., 7, 41-48 (2002).
150. E. Nambara and A. Marion-Poll, "Abscisic acid biosynthesis and catabolism," Ann. Rev. Plant Biol., 56, 165-85 (2005).
151. H. Du, N. Wang, F. Cui, X. Li, J. Xiao, and L. Xiong, "Characterization of the beta-carotene hydroxylase gene DSM2 conferring drought and oxidative stress resistance by increasing xanthophylls and abscisic acid synthesis in rice," Plant Physiol., 154, 1304-18 (2010).
152. J. Fang, C. Chai, Q. Qian, et al., "Mutations of genes in synthesis of the carotenoid precursors of ABA lead to pre-harvest sprouting and photo-oxidation in rice," Plant J., 54, 177-89 (2008).
153. V. Gomez-Roldan, S. Fermas, P. B. Brewer, et al., "Strigolactone inhibition of shoot branching," Nature, 455, 189-94 (2008).
154. M. Umehara, A. Hanada, S. Yoshida, et al., "Inhibition of shoot branching by new terpenoid plant hormones," Nature, 455, 195-200 (2008).
155. K. Akiyama, K. Matsuzaki, and H. Hayashi, "Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi," Nature, 435, 824-7 (2005).
156. R. Matusova, K. Rani, F. W. Verstappen, M. C. Franssen, M. H. Beale, and H. J. Bouwmeester "The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway," Plant Physiol., 139, 920-34 (2005).
157. S. H. Schwartz, X. Qin, and M. C. Loewen, "The biochemical characterization of two carotenoid cleavage enzymes from Arabidopsis indicates that a carotenoid-derived compound inhibits lateral branching," J. Biol. Chem., 279, 46940-5 (2004).
158. A. Alder, M. Jamil, M. Marzorati, M. Bruno, M. Vermathen, P. Bigler, S. Ghisla, H. Bouwmeester, P. Beyer, and S. Al-Babili, "The path from beta-carotene to carlactone, a strigolactone-like plant hormone," Science, 335, 1348-51 (2012).
159. Y. Zhang, A. D. van Dijk, A. Scaffidi, et al., "Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis," Nature Chem. Biol., 10, 1028-33 (2014a).
160. M. Ibdah, Y. Azulay, V. Portnoy, et al. "Functional characterization of CmCCD1, a carotenoid cleavage dioxygenase from melon," Phytochemistry, 67, 1579-89 (2006).
161. F. C. Huang, G. Horvath, P. Molnar, E. Turcsi, J. Deli, J. Schrader, G. Sandmann, H. Schmidt, and W. Schwab, "Substrate promiscuity of RdCCD1, a carotenoid cleavage oxygenase from Rosa damascena," Phytochemistry, 70, 457-64 (2009).
162. M. E. Auldridge, D. R. McCarty, and H. J. Klee, "Plant carotenoid cleavage oxygenases and their apocarotenoid products," Curr. Opin. Plant Biol., 9, 315-21 (2006).
163. G. Ma, L. Zhang, A. Matsuta, K. Matsutani, K. Yamawaki, M. Yahata, A. Wahyudi, R. Motohashi, and M. Kato, "Enzymatic formation of beta-citraurin from beta-cryptoxanthin and zeaxanthin by carotenoid cleavage dioxygenase4 in the flavedo of citrus fruit," Plant Physiol., 163, 682-95 (2013).
164. S. Gonzalez-Jorge, S. H. Ha, M. Magallanes-Lundback, L. U. Gilliland, A. Zhou, A. E. Lipka, Y. N. Nguyen, R. Angelovici, H. Lin, J. Cepela, H. Little, C. R. Buell, M. A. Gore, and D. Dellapenna, "Carotenoid cleavage dioxygenase4 is a negative regulator of beta-carotene content in Arabidopsis seeds," Plant Cell, 25, 4812-26 (2013).
165. P. K. Lundquist, A. Poliakov, N. H. Bhuiyan, B. Zybailov, Q. Sun, and K. J. van Wijk, "The functional network of the Arabidopsis plastoglobule proteome based on quantitative proteomics and genome-wide coexpression analysis," Plant Physiol., 158, 1172-92 (2012).
166. G. Giuliano, S. Al-Babili, and J. von Lintig, "Carotenoid oxygenases: cleave it or leave it," Trends Plant Sci., 8, 145-9 (2003).
167. D. S. Floss, W. Schliemann, J. Schmidt, D. Strack, and M. H. Walter, "RNA interferencemediated repression of MtCCD1 in mycorrhizal roots of Medicago truncatula causes accumulation of C27 apocarotenoids, shedding light on the functional role of CCD1," Plant Physiol., 148, 1267-82 (2008).
168. M. H. Walter, D. S. Floss, and D. Strack, "Apocarotenoids: hormones, mycorrhizal metabolites and aroma volatiles," Planta, 232, 1-17 (2010).
169. J. M. Van Norman, R. L. Frederick, and L. E. Sieburth, "BYPASS1 negatively regulates a root-derived signal that controls plant architecture," Curr. Biol., 14, 1739-46 (2004).
170. J. M. Van Norman and L. E. Sieburth, "Dissecting the biosynthetic pathway for the bypass1 root-derived signal," Plant J., 49, 619-28 (2007).
171. J. M. Van Norman, J. Zhang, C. I. Cazzonelli, B. J. Pogson, P. J. Harrison, T. D. Bugg, K. X. Chan, A. J. Thompson, and P. N. Benfey, "Periodic root branching in Arabidopsis requires synthesis of an uncharacterized carotenoid derivative," Proc. Natl. Acad. Sci. USA, 111, E1300-9 (2014).
172. M. J. Sergeant, J. J. Li, C. Fox, N. Brookbank, D. Rea, T. D. Bugg, and A. J. Thompson, "Selective inhibition of carotenoid cleavage dioxygenases: phenotypic effects on shoot branching," J. Biol. Chem., 284, 5257-64 (2009).
173. G. Farré, G. Sanahuja, S. Naqvi, C. Bai, T. Capell, C. Zhu, and P. Christou, "Travel advice on the road to carotenoids in plants," Plant Sci., 179, 28-48 (2010).
174. J. A. Paine, C. A. Shipton, S. Chaggar, R. M. Howells, M. J. Kennedy, G. Vernon, S. Y. Wright, E. Hinchliffe, J. L. Adams, A. L. Silverstone, and R. Drake, "Improving the nutritional value of Golden Rice through increased pro-vitamin A content," Nature Biotechnol., 23, 482-7 (2005).
175. Y. Jayaraj, R. Devlin, and Z. Punja, "Metabolic engineering of novel ketocarotenoid production in carrot plants," Transgenic Res., 17, 489-501 (2008).