Open Access Open Access  Restricted Access Subscription Access
Open Access Open Access Open Access  Restricted Access Restricted Access Subscription Access

Molecular Mechanisms Involved in Biosynthesis and Regulation of Carotenoids in Plants


Affiliations
1 Division of Biotechnology, ICAR-Indian Institute of Horticultural Research, Bengaluru 560 089, India
2 Division of Biotechnology, ICAR- Indian Institute of Horticultural Research, Bengaluru 560 089, India
3 Division of Plant Physiology and Biochemistry, ICAR- Indian Institute of Horticultural Research, Bengaluru 560 089, India
     

   Subscribe/Renew Journal


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.

Keywords

Carotenoid Biosynthesis, Regulation, Plastid, Fruit, Transcription Factor.
User
Subscription Login to verify subscription
Notifications
Font Size

  • 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 multigene engineering. Curr. Opin. Plant Biol., 19:111-117
  • Guil-Guerrero, J.L., Martinez-Guirado, C., Del Mar RebollosoFuentes, 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 postharvest temperature on the conversion of 14Cmevalonic 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 provides insight 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):1110211107
  • 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

Abstract Views: 34

PDF Views: 4




  • Molecular Mechanisms Involved in Biosynthesis and Regulation of Carotenoids in Plants

Abstract Views: 34  |  PDF Views: 4

Authors

P. Shilpa
Division of Biotechnology, ICAR-Indian Institute of Horticultural Research, Bengaluru 560 089, India
K. V. Ravishankar
Division of Biotechnology, ICAR- Indian Institute of Horticultural Research, Bengaluru 560 089, India
K. S. Shivashankara
Division of Plant Physiology and Biochemistry, ICAR- Indian Institute of Horticultural Research, Bengaluru 560 089, India
A. T. Sadashiva
Division of Plant Physiology and Biochemistry, ICAR- Indian Institute of Horticultural Research, Bengaluru 560 089, India
N. Sunil Kumar
Division of Biotechnology, ICAR- Indian Institute of Horticultural Research, Bengaluru 560 089, India

Abstract


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.

Keywords


Carotenoid Biosynthesis, Regulation, Plastid, Fruit, Transcription Factor.

References