Molecular Mechanisms Involved in Biosynthesis and Regulation of Carotenoids in Plants
DOI:
https://doi.org/10.24154/jhs.v11i2.78Keywords:
Carotenoid Biosynthesis, Regulation, Plastid, Fruit, Transcription FactorAbstract
Carotenoids are coloured compounds beneficial to plants and humans. Some of the major health benefits carotenoids provide include Vitamin A precursors and, antioxidants besides being involved in several physiological functions. Even though several carotenoids are synthesised by plants, only a few like beta/ alpha carotenes and cryptoxanthin serve as Vitamin A precursors. The rest are useful as antioxidants. To draw maximum benefits from carotenoids, we need to incorporate these in crop improvement programmes for enhancing available Vitamin A precursor carotenoids. Therefore, it is essential to study biosynthesis of carotenoids, their genetics and their control. In this review, we focus on factors regulating carotenoid biosynthesis, metabolism and storage in plastids. Transcriptional and genetic control of carotenoid production in plants is discussed in the review using several mutants too. Further, environmental regulation of carotenoid biosynthesis is also highlighted. Carotenoid-rich fruits and vegetables have greater economic value owing to their health-promoting effects. Besides,carotenoids have several industrial applications. Therefore, knowledge of regulation mechanism in carotenoid production in plants can help develop crop varieties or technologies, thus generating carotene-rich fruits and vegetables.
Downloads
References
Alque-zar, B., Zacarias, L. and Rodrigo, M.J. 2009. Molecular and functional characterization of a novel chromoplast-specific lycopene b-cyclase from citrus and its relation to lycopene accumulation. J. Exptl. Bot., 60:1783-1797
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. Exptl. 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., 9:315-321
Beisel, K.G., Jahnke, S., Hofmann, D., Koppchen, S., Schurr, U. and Matsubara, S. 2010. Continuous turnover of carotenes and chlorophyll ‘a’ in mature leaves of Arabidopsis revealed by 14CO2 pulse-chase labeling. Plant Physiol., 152:2188-2199
Beyer, P., Al-Babili, S., Ye, X., Lucca, P., Schaub, P., Welsch, R. and Potrykus, I. 2002 . Golden rice: Introducing the ß-carotene biosynthesis pathway into rice endosperm by genetic engineering to defeat Vitamin A deficiency. J. Nutrition, 132:506S-510S
Bird, C.R., Ray, J.A., Fletcher, J.D., Boniwell, J.M., Bird, A.S., Teulieres, C., Blain, I., Bramley, P.M. and Schuch, W. 1991. Using antisense RNA to study gene function: inhibition of carotenoid biosynthesis in transgenic tomatoes. BioTechnology, 9:635-639
Bramley, P.M., Teulieres, C., Blain, I., Bird, C. and Schuch, W. 1992. Biochemical characterization of transgenic tomato plants in which carotenoid synthesis has been inhibited through expression of antisense RNA to pTOM5. The Plant J., 2:343-349
Brandt, S., Pék, Z., Barna, E., Lugasi, A. and Helyes, L. 2006. Lycopene content and colour of ripening tomatoes as affected by environmental conditions. J. Sci. Food Agri., 86(4):568-572
Carol, P. and Kuntz, M. 2001. A plastid terminal oxidase comes to light: implications for carotenoid biosynthesis and chloro-respiration. Trends Plant Sci., 6:31-36
Cazzonelli, C.I., Cuttriss, A.J., Cossetto, S.B., Pye, W., Crisp, P. and Whelan, J. 2009. Regulation of carotenoid composition and shoot branching in Arabidopsis by a chromatin modifying histone methyltransferase, SDG8. Plant Cell, 21:39-53
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 â-carotene in fruits of tomato plants transformed with the tomato lycopene â-cyclase (tlcy-b) cDNA. Plant Sci., 166:207-214
Dalal, M., Viswanathan, C. and Kailash C. Bansal. 2010. Isolation and functional characterization of lycopene â-cyclase (CYC-B) promoter from Solanum habrochaites. BMC Plant Biol., 10:61-75
Devitt, L.C., Fanning, K., Dietzgen, R.G. and Holton, T.A. 2010. Isolation and functional characterization of a lycopene b-cyclase gene that controls fruit colour of papaya (Carica papaya L.). J. Exptl. Bot., 61:33-39
Diretto, G., Al-Babili, S., Tavazz, R., Papacchioli, V., Beyer, P. and Giuliano, G. 2007. Metabolic engineering of potato carotenoid content through tuber-specific overexpression of a bacterial mini-pathway. PLoS ONE, 2:e350
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. Exptl. Bot., 56:81-89
Dumas, Y., Dadomo, M., Di Lucca, G. and Grolier, P. 2003. Effects of environmental factors and agricultural techniques on antioxidant content of tomatoes. J. Sci. Food Agri., 83(5):369-382
Eisenreich, W., Bacher, A., Arigoni, D. and Rohdich, F. 2004. Biosynthesis of isoprenoids via the non-mevalonate pathway. Cell. Mol. Life Sci., 61:1401-1426
Fantini, E., Falcone, G., Frusciante, S., Giliberto, L. and Giuliano, G. 2013. Dissection of tomato lycopene biosynthesis through virus induced gene silencing. Plant Physiol., 163:986-998
Farre, G., Bai, C., Twyman, R.M., Capell, T., Christou, P. and Zhu C. 2011. Nutritious crops producing multiple carotenoids - a metabolic balancing act. Trends Plant Sci.,16(10):532-540
Fiedor, J. and Burda, K. 2014. Potential role of carotenoids as antioxidants in human health and disease. Nutrients, 6:466-488
Fraser, P.D. and Bramley, P.M. 2004. The biosynthesis and nutritional uses of carotenoids. Prog. Lipid Res., 43:228-265
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., Kiano, J.W., Truesdale, M.R., Schuch, W. and Bramley, P.M. 1999. Phytoene synthase-2 enzyme activity in tomato does not contribute to carotenoid synthesis in ripening fruit. Plant Mol. Biol., 40:687-698
Fraser, P.D., Misawa, N., Linden, H., Shigeyuki, Y., Kobayashi, K. and Sandmann, G. 1992. Expression in E. coli, purification and reactivation of a recombinant Erwinia uredovora phytoene desaturase. J. Biol. Chem., 267:19891-19895
Fray, R.G. and Grierson, D. 1993. Identification and genetic analysis of normal and mutant phytoene synthase genes of tomato by sequencing, complementation and co-suppression. Plant Mol. Biol., 22:589-602
Gady, A.L., Vriezen, W.H., Van de Wal, M.H., Huang, P., Bovy, A.G., Visser, R.G. and Bachem, C.W.B. 2012. Induced point mutations in the phytoene synthase 1 gene cause differences in carotenoid content during tomato fruit ripening. Mol. Breed., 29:801-812
Galpaz, N., Wang, Q., Menda, N., Zamir, D. and Hirschberg, J. 2008. Abscisic acid deficiency in the tomato mutant high-pigment 3 leading to increased plastid number and higher fruit lycopene content. Plant J., 53:717-730
Giuliano, G. 2014. Plant carotenoids: genomics meets multi- gene engineering. Curr. Opin. Plant Biol., 19:111-117
Guil-Guerrero, J.L., Martinez-Guirado, C., Del Mar Rebolloso- Fuentes, M. and Carrique-Perez, A. 2006. Nutrient composition and antioxidant activity of 10 pepper (Capsicum annuum) varieties. Eur. Food Res. Technol., 224:1-9
Hamauzu, Y., Chachin, K. and Ueda, Y. 1998. Effects of post- harvest temperature on the conversion of 14C- mevalonic acid to carotenes in tomato fruit. J. Jpn. Soc. Hortl. Sci., 67:549-555
Harjes, C.E., Rocheford, T.R., Bai, L., Brutnell, T.P., Kandianis, C.B. and Sowinski, S.G. 2008. Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science, 319:330-333
Howitt, C.A. and Pogson, B.J. 2006. Carotenoid accumulation and function in seeds and non-green tissues. Plant Cell Environ., 29:435-445
Ilg, A., Brunoa, M., Beyera, P. and Al-Babili, S. 2014. Tomato carotenoid cleavage dioxygenases 1A and 1B: relaxed double bond specificity leads to a plenitude of dialdehydes, mono-apocarotenoids and isoprenoid volatiles. FEBS Open Biol., 4:584-593
Isaacson, T., Ronen, G., Zamir, D. and Hirschberg, J. 2002. Cloning of tangerine from tomato reveals a carotenoid
isomerase essential for the production of â-carotene and xanthophylls in plants. Plant Cell, 14:333-342
Jayaraj, J., Devlin, R. and Punja, Z. 2008. Metabolic engineering of novel keto carotenoid production in carrot plants. Transgenic Res., 17(4):489-501
Karlova, R., Rosin, F.M., Busscher-Lange, J., Parapunova, V., Do, P.T., Fernie, A.R., Fraser, P.D., Baxter, C., Angenent, G.C. and de Maagd, R.A. 2011. Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening. Plant Cell, 23:923-941
Lanahan, M.B., Yen, H.C., Giovannoni, J.J. and Klee, H.J. 1994. The never-ripe mutation blocks ethylene perception in tomato. Plant Cell, 6:521-530
Lee, J.M., Joung, J.G., McQuinn, R., Chung, M.Y., Fei, Z., Tieman, D., Klee, H. and Giovannoni, J. 2012. Combined transcriptome, genetic diversity and metabolite profiling in tomato fruit reveals that the ethylene response factor SlERF6 plays an important role in ripening and carotenoid accumulation. Plant J., 70:191-204
Leivar, P., Tepperman, J.M., Monte, E., Calderon, R.H., Liu, T.L. and Quail, P.H. 2009. Definition of early transcriptional circuitry involved in light-induced reversal of PIF imposed repression of photomorphogenesis in young Arabidopsis seedlings. Plant Cell, 21:3535-3553
Levin, I., Ric de Vos, C.H., Tadmor,Y., Bovy, A., Lieberman, M., Oren-Shamir, M., Segev, O., Kolotilin, I., Keller, M., Ovadia , R., Meir, A. and Bino, R.J. 2006. High pigment tomato mutants more than just lycopene (a review). Isr. J. Plant Sci., 54:179-190
Li, F.Q., Murillo, C. and Wurtzel, E.T. 2007. Maize Y9 encodes a product essential for 15- cis-zeta-carotene isomerization. Plant Physiol., 144:1181-1189
Li, F.Q., Vallabhaneni, R. and Wurtzel, E.T. 2008a. 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
Li, F.Q., Vallabhaneni, R., Yu, J., Rocheford, T. and Wurtzel, E.T. 2008b. The maize phytoene synthase gene family: Overlapping roles for carotenogenesis in endosperm, photomorphogenesis and thermal stress tolerance. Plant Physiol., 147:1334-1346
Lin, Z., Hong, Y., Yin, M., Li, C., Zhang, K. and Grierson, D. 2008. A tomato HD-Zip homeobox protein, LeHB-1, plays an important role in floral organogenesis and ripening. Plant J., 55:301-310
Liu, L., Shao, Z., Zhang, M. and Wang Q. 2015. Regulation of carotenoid metabolism in tomato. Mol. Plant., 8:28-39
Liu, Y.S., Roof, S., Ye, Z.B., Barry, C., Van Tuinen, A. and Vrebalov, J. 2004. Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc. Nat’l. Acad. Sci., 101:9897- 9902
Lois, L.M., Campos, N., Putra, S.R., Danielsen, K., Rohmer, M. and Boronat, A. 2000. Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-D-xylulose 5-phosphatesynthase. Plant J., 22:503–513
Luo, Z., Zhang, J., Li, J., Yang, C., Wang, T., Ouyang, B., Li, H., Giovannoni, J. and Ye, Z. 2013. A STAYGREEN protein SlSGR1 regulates lycopene and b-carotene accumulation by interacting directly with SlPSY1 during ripening processes in tomato. New Phytol., 198:442-452
Manning, K., Tor, M., Poole, M., Hong, Y., Thompson, A.J., King, G.J., Giovannoni, J.J. and Seymour, G.B. 2006. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nature Genet., 38:948-952
Martel, C., Vrebalov, J., Tafelmeyer, P. and Giovannoni, J.J. 2011. The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiol., 157:1568-1579
Marty, I., Bureau, S., Sarkissian, G., Gouble, B., Audergon, J.M. and Albagnac, G. 2005. Ethylene regulation of carotenoid accumulation and carotenogenic gene expression in colour-contrasted apricot varieties (Prunus armeniaca). J. Exptl. Bot., 56:1877-1886
Mayer, M.P., Nievelstein, V. and Beyer, P. 1992. Purification and characterization of an NADPH-dependent oxidoreductase from chloroplasts of Narcissus- redox mediator possibly involved in carotene desaturation. Plant Physiol Biochem., 30:389-398
Mohan, V., Pandey, A., Sreelakshmi, Y. and Sharma, R. 2016. Neofunctionalization of chromoplast specific lycopene beta cyclase gene (CYC-B) in tomato clade. PLoS ONE, 11(4):1-22
Nisar, N., Li, L., Lu, S., Khin, N.C. and Pogson, B.J. 2015. Carotenoid metabolism in plants. Mol. Plant, 8(1):68- 82
Norris, R., Barrette, T.R. and DellaPenna, D. 1995. Genetic dissection of carotenoid synthesis in Arabidopsis defines plastoquinone as an essential component of phytoene desaturase. Plant Cell, 7:2139-2149
North, H.M., De Almeida, A., Boutin, J.P., Frey, A., To, A. and Botran, L. 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
Pandurangaiah, S., Ravishankar, K.V., Shivashankar, K.S., Sadashiva, A.T., Pillakenchappa, K. and Narayanan, S.K. 2016. Differential expression of carotenoid biosynthetic pathway genes in two contrasting tomato genotypes for lycopene content. J. Biosci., 41(2):169-324
Park, H., Kreunen, S.S., Cuttriss, A.J., DellaPenna, D. and Pogson, B.J. 2002. Identification of the carotenoid isomerase provi des insi ght into carotenoid biosynthesis, prolamellar body formation, and photomorphogenesis. Plant Cell, 14:321-332
Pecker, I., Gabbay, R., Cunningham, F.X.J. and Hirschberg, J. 1996. Cloning and characterization of the cDNA for lycopene b-cyclase from tomato reveals decrease in its expression during fruit ripening. Plant Mol. Biol., 30:807-819
Pizarro, L. and Stange. C. 2009. Light-dependent regulation of carotenoid biosynthesis in plants. Cien. Inv. Agri., 36(2):143-162
Rodriguez-Concepcion, M. and Boronat, A. 2002. Elucidation of the methyl erythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastid: A metabolic milestone achieved through genomics. Plant Physiol., 130:1079-1089
Ronen, G., Carmel-Goren, L., Zamir, D. and Hirschberg, J. 2000. An alternative pathway to â-carotene formation in plant chromoplasts discovered by map-based cloning of Beta and old-gold colour mutations in tomato. Proc. Nat’l. Acad. Sci., U.S.A., 97(20):11102-11107
Ronen, G., Cohen, M., Zamir, D. and Hirschberg, J. 1999. 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., 17:341-351
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. The Plant J., 24:413-420
Rosati, C., Diretto, G. and Giuliano, G. 2010. Biosynthesis and engineering of carotenoids and apo-carotenoids in plants: state of the art and future prospects. Biotechnol. Genet. Engg. Rev., 26:139-162
Schofield, A. and Paliyath, G. 2005. Modulation of carotenoid biosynthesis during tomato fruit ripening through phytochrome regulation of phytoene synthase activity. Plant Physiol. Biochem., 43:1052-1060
Sun, L., Yuan, B., Zhang, M., Wang, L., Cui, M., Wang, Q. and Leng, P. 2012. Fruit-specific RNAi-mediated suppression of SlNCED1 increases both lycopene and beta-carotene contents in tomato fruit. J. Exptl. Bot., 63:3097-3108
Tadmor, Y., King, S., Levi, A., Davis, A., Meir, A., Wasserman, B., Hirschberg, J. and Lewinsohn, E. 2005. Comparative fruit colouration in watermelon and tomato. Food Res. Int’l., 38:837-841
Vishnevetsky, M., Ovadis, M., Zuker, A. and Vainstein, A. 1999. Molecular mechanisms underlying carotenogenesis in the chromoplast: multilevel regulation of carotenoid-associated genes. Plant J., 20:423-431
Von Lintig, J., Welsch, R., Bonk, M., Giuliano, G., Batschauer, A. and Kleinig, H. 1997. Light-dependent regulation of carotenoid biosynthesis occurs at the level of phytoene synthase expression and is mediated by phytochrome in Sinapsis alba and Arabidopsis thaliana seedlings. Plant J., 12:625-634
Vrebalov, J., Pan, I.L., Arroyo, A.J., McQuinn, R., Chung, M., Poole, M., Rose, J., Seymour, G., Grandillo, S. and Giovannoni, J. 2009. Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene TAGL1. Plant Cell, 21:3041-3062
Vrebalov, J., Ruezinsky, D., Padmanabhan, V., White, R., Medrano, D., Drake, R., Schuch, W. and Giovannoni, J. 2002. A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (Rin) locus. Science, 296:343-346
Walter, M.H. and Strack, D. 2011. Carotenoids and their cleavage products: biosynthesis and functions. Nat. Prod. Rep., 28:663-692
Welsch, R., Beyer, P., Hugueney, P., Kleinig, H. and Von Lintig, J. 2000. Regulation and activation of phytoene synthase, a key enzyme in carotenoid biosynthesis, during photomorphogenesis. Planta, 211:846-854
Welsch, R., Maass, D., Voegel, T., Della Penna, D. and Beyer, P. 2007. Transcription factor RAP2.2 and its interacting partner SINAT2: Stable elements in the carotenogenesis of Arabidopsis leaves. Plant Physiol., 145:1073-1085
Welsch, R., Wust, F., Bar, C., Al-babili, S. and Beyer, P. 2008. 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., 147:367-380
Yuan, H., Zhang , J., Divyashree, N. and Li, L. 2015. Carotenoid metabolism and regulation in horticultural crops. Hort. Res., 2: Article number 15036
Zhu, M., Chen, G., Zhou, S., Tu, Y., Wang, Y., Dong, T. and Hu, Z. 2013. A new tomato NAC (NAM/ATAF1/2/CUC2) transcription factor, SlNAC4, functions as a positive regulator of fruit ripening and carotenoid accumulation. Plant Cell Physiol., 55(1):119-135
Downloads
Published
Issue
Section
License
Copyright (c) 2016 P Shilpa, K V Ravishankar, K S Shivashankara, A T Sadashiva, N Sunil Kumar (Author)
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
Authors retain copyright. Articles published are made available as open access articles, distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License, which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited. 
This journal permits and encourages authors to share their submitted versions (preprints), accepted versions (postprints) and/or published versions (publisher versions) freely under the CC BY-NC-SA 4.0 license while providing bibliographic details that credit, if applicable.
How to Cite
. 
