Abstract
Carotenoids, important lipid-soluble antioxidants in photosynthetic tissues, are known to be completely absent in rice endosperm. Many studies, involving transgenic manipulations of carotenoid biosynthesis genes, have been performed to get carotenoid-enriched rice grain. Study of genes involved in their biosynthesis can provide further information regarding the abundance/absence of carotenoids in different tissues. We have identified 16 and 34 carotenoid biosynthesis genes in rice and Populus genomes, respectively. A detailed analysis of the domain structure of carotenoid biosynthesis enzymes in rice, Populus and Arabidopsis has shown that highly conserved catalytic domains, along with other domains, are present in these proteins. Phylogenetic analysis of rice genes with Arabidopsis and other characterized carotenoid biosynthesis genes has revealed that homologous genes exist in these plants, and the duplicated gene copies probably adopt new functions. Expression of rice and Populus genes has been analyzed by full-length cDNA- and EST-based expression profiling. In rice, this analysis was complemented by real-time PCR, microarray and signature-based expression profiling, which reveal that carotenoid biosynthesis genes are highly expressed in light-grown tissues, have differential expression pattern during vegetative/reproductive development and are responsive to stress.
Similar content being viewed by others
References
Adams MD, Kerlavage AR, Fleischmann RD, Fuldner RA, Bult CJ, Lee NH, Kirkness EF, Weinstock KG, Gocayne JD, White O et al (1995) Initial assessment of human genome diversity and expression patterns based upon 83 million nucleotides of cDNA sequence. Nature 377:3–17
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815
Audran C, Liotenberg S, Gonneau M, North H, Frey A, Tap-Waksman K, Vartanian N, Marion-Poll A (2001) Localization and expression of zeaxanthin epoxidase mRNA in Arabidopsis in response to drought stress and during seed development. Aust J Plant Physiol 28:1161–1173
Bashton M, Chothia C (2007) The generation of new protein functions by the combination of domains. Structure 15:85–99
Beveridge CA, Gresshoff PM, Rameau C, Turnbull CGN (2003) Additional signaling compounds are required to orchestrate plant development. J Plant Growth Regul 22:15–24
Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1030
Bouvier F, Dogbo O, Camara B (2003a) Biosynthesis of the food and cosmetic plant pigment bixin (annatto). Science 300:2089–2091
Bouvier F, Suire C, Mutterer J, 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
Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unraveling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433–438
Britton G, Jensen SL, Pfander H (2004) Carotenoids handbook. Birkhäuser Verlag, Basel
Burkhardt P, Beyer P, Wunn J, Kloti A, Armstrong G, Schledz M, von Lintig J, Potrykus I (1997) Transgenic rice (Oryza sativa) endosperm expressing daffodil (Narcissus pseudonarcissus) phytoene synthase accumulates phytoene, a key intermediate of provitamin A biosynthesis. Plant J 11:1071–1078
Calucci L, Capocchi A, Galleschi L, Ghiringhelli S, Pinzino C, Saviozzi F, Zandomeneghi M (2004) Antioxidants, free radicals, storage proteins, puroindolines, and proteolytic activities in bread wheat (Tritium aestivum) seeds during accelerated aging. J Agric Food Chem 52:4274–4281
Chen J, Agrawal V, Rattray M, West MAL, St Clair DA, Michelmore RW, Coughlan SJ, Meyers BC (2007) A comparison of microarray and MPSS technology platforms for expression analysis of Arabidopsis. BMC Genomics 8:414
Dall’Osto L, Lico C, Alric J, Giuliano G, Havaux M, Bassi R (2006) Lutein is needed for efficient chlorophyll triplet quenching in the major LHCII antenna complex of higher plants and effective photoprotection in vivo under strong light. BMC Plant Biol 6:32
Dall’Osto L, Fiore A, Cazzaniga S, Giuliano G, Bassi R (2007) Different roles of alpha- and beta-branch xanthophylls in photosystem assembly and photoprotection. J Biol Chem 282:35056–35068
Davidson PA, Hunter CN, Horton P (2002) Overexpression of beta-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418:203–206
Dellapenna D, Pogson BJ (2006) Vitamin synthesis in plants: tocopherols and carotenoids. Annu Rev Plant Biol 57:711–738
Durbin R, Eddy SR, Krogh A, Mitchison GJ (1998) Biological sequence analysis: probabilistic models of proteins and nucleic acids. Cambridge University Press, London
Fang J, Chu C (2008) Abscisic acid and the pre-harvest sprouting in cereals. Plant Signal Behav 3:1046–1048
Franco AC, Matsubara S, Orthen B (2007) Photoinhibition, carotenoid composition and the co-regulation of photochemical and non-photochemical quenching in neotropical savanna trees. Tree Physiol 27:717–725
Fraser PD, Kiano JW, Truesdale MR, Schuch W, Bramley PM (1999) Phytoene synthase-2 enzyme activity in tomato does not contribute to carotenoid synthesis in ripening fruit. Plant Mol Biol 40:687–698
Gallagher CE, Matthews PD, Li F, Wurtzel ET (2004) Gene duplication in the carotenoid biosynthetic pathway preceded evolution of grasses. Plant Physiol 135:1776–1783
Hable WE, Oishi KK, Schumaker KS (1998) Viviparous-5 encodes phytoene desaturase, an enzyme essential for abscisic acid (ABA) accumulation and seed development in maize. Mol Gen Genet 257:167–176
Harjes C, Rocheford TR, Bai L, Brutnell TP, Kandianis CB, Sowinski SG et al (2008) Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science 319:330–333
Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc Natl Acad Sci USA 96:8762–8767
Holt NE, Zigmantas D, Valkunas L, Li XP, Niyogi KK, Fleming GR (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307:433–436
Howitt CA, Pogson BJ (2006) Carotenoid accumulation and function in seeds and non-green tissues. Plant Cell Environ 29:435–445
International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800
Jeffery SW, Douce R, Benson AA (1974) Carotenoid transformations in the chloroplast envelope. Proc Natl Acad Sci USA 71:807–810
Jordan IK, Makarova KS, Spouge JL, Wolf YI, Koonin EV (2001) Lineage-specific gene expansions in bacterial and archaeal genomes. Genome Res 11:555–565
Kato M, Ikoma Y, Matsumoto H, Sugiura M, Hyodo H, Yano M (2004) Accumulation of carotenoids and expression of carotenoid biosynthetic genes during maturation in citrus fruit. Plant Physiol 134:824–837
Kulheim C, Agren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 308:267–269
Lespinet O, Wolf YI, Koonin EV, Aravind L (2002) The role of lineage-specific gene family expansion in the evolution of eukaryotes. Genome Res 12:1048–1059
Li L, Paolillo DJ, Parthasarathy MV, DiMuzio EM, Garvin DF (2001) A novel gene mutation that confers abnormal patterns of β-carotene accumulation in cauliflower (Brassica oleracea var. botrytis). Plant J 26:59–67
Li X, Duan X, Jiang H, Sun Y, Tang Y, Yuan Z, Guo J, Liang W, Chen L, Yin J, Ma H, Wang J, Zhang D (2006) Genome-wide analysis of basic/helix–loop–helix transcription factor family in rice and Arabidopsis. Plant Physiol 141:1167–1184
Li F, Vallabhaneni R, Wurtzel ET (2008a) PSY3, a new member of the phytoene synthase gene family conserved in the Poaceae and regulator of abiotic stress-induced carotenogenesis. Plant Physiol 146:1333–1345
Li F, Vallabhaneni R, Yu J, Rocheford T, Wurtzel ET (2008b) The maize phytoene synthase gene family: overlapping roles for carotenogenesis in endosperm, photomorphogenesis and thermal stress tolerance. Plant Physiol 147:1334–1346
Lokstein H, Tian L, Polle JEW, Dellapenna D (2002) Xanthophyll biosynthetic mutants of Arabidopsis thaliana: altered nonphotochemical quenching of chlorophyll fluorescence is due to changes in photosystem II antenna size and stability. Biochim Biophys Acta 1553:309–319
Lopez AB, Van Eck J, Conlin BJ, Paolillo DJ, O’Neill J, 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
López-Ráez JA, Charnikhova T, Gómez-Roldán V, Matusova R, Kohlen W, De Vos R, Verstappen F, Puech-Pages V, Bécard G, Mulder P, Bouwmeester H (2008) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178:863–874
Lu S, Li L (2008) Carotenoid metabolism: biosynthesis, regulation and beyond. J Integr Plant Biol 50:778–785
McNulty HP, Byun J, Lockwood SF, Jacob RF, Mason RP (2007) Differential effects of carotenoids on lipid peroxidation due to membrane interactions: X-ray diffraction analysis. BBA Biomembranes 1768:167–174
McSteen P, Leyser O (2005) Shoot branching. Annu Rev Plant Biol 56:353–374
Miyao A, Tanaka K, Murata K, Sawaki H, Takeda S, Abe K, Shinozuka Y, Onosato K, Hirochika H (2003) Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome. Plant Cell 15:1771–1780
Nakano M, Nobuta K, Vemaraju K, Tej SS, Skogen JW, Meyers BC (2006) Plant MPSS databases: signature-based transcriptional resources for analyses of mRNA and small RNA. Nucleic Acids Res 34:D731–D735
Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185
Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Biol 56:165–185
Nobuta K, Venu RC, Lu C, Beló A, Vemaraju K, Kulkarni K, Wang W, Pillay M, Green PJ, Wang G, Meyers BC (2007) An expression atlas of rice mRNAs and small RNAs. Nat Biotechnol 25:473–477
Oudes AJ, Roach JC, Walashek LS, Eichner LJ, True LD, Vessella RL, Liu AY (2005) Application of Affymetrix array and massively parallel signature sequencing for identification of genes involved in prostate cancer progression. BMC Cancer 5:86
Paine JA, Shipton CA, Chaggar S, Howells RM, Kennedy MJ, Vernon G, Wright SY, Hinchliffe E, Adams JL, Silverstone AL, Drake R (2005) A new version of golden rice with increased pro-vitamin A content. Nat Biotechnol 23:482–487
Park H, Kreunen SS, Cuttriss AJ, Dellapenna D, Pogson BJ (2002) Identification of the carotenoid isomerase provides insight into carotenoid biosynthesis, prolamellar body formation, and photomorphogenesis. Plant Cell 14:321–332
Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556
Pogson BJ, Niyogi KK, Bjorkman O, Dellapenna D (1998) Altered xanthophylls compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. Proc Natl Acad Sci USA 95:13324–13329
Quinlan RF, Jaradat TT, Wurtzel ET (2007) Escherichia coli as a platform for functional expression of plant P450 carotene hydroxylases. Arch Biochem Biophys 458:146–157
Raes J, Rohde A, Christensen JH, van de Peer Y, Boerjan W (2003) Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol 133:1051–1071
Rivier L, Léonard JF, Cottier JP (1983) Rapid effect of osmotic stress on the content and exodiffusion of abscisic acid in Zea mays roots. Plant Sci Lett 83:133–137
Rossel JB, Wilson IW, Pogson BJ (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol 130:1109–1120
Rouze P, Pavy N, Rombauts S (1999) Genome annotation: which tools do we have for it? Curr Opin Plant Biol 2:90–95
Segerman B, Jansson S, Karlsson J (2007) Characterization of genes with narrow expression patterns in Populus. Tree Genet Genomes 3:351–362
Shan H, Zhang N, Liu C, Xu G, Zhang J, Chen Z et al (2007) Patterns of gene duplication and functional diversification during the evolution of the AP1/SQUA subfamily of plant MADS-box genes. Mol Phylogenet Evol 44:26–41
Siefermann-Harms D, Joyard J, Douce R (1978) Light-induced changes of the carotenoid levels in chloroplast envelopes. Plant Physiol 61:530–533
Simkin AJ, Schwartz SH, Auldridge M, Taylor MG, Jee HJ (2004a) The tomato carotenoid cleavage dioxygenase I gene contributes to the formation of the flavor volatiles beta-ionone, pseudo ionone, and geranylacetone. Plant J 40:882–892
Simkin AJ, Underwood BA, Auldridge M, Loucas HM, Shibuya K, Schmelz E et al (2004b) Circadian regulation of the PhCCD1 carotenoid cleavage dioxygenase controls emission of β-ionone, a fragrance volatile of petunia flowers. Plant Physiol 136:3504–3514
Singh G, Kumar S, Singh P (2003) A quick method to isolate RNA from wheat and other carbohydrate-rich seeds. PMB Report 21:93a-f
Sun ZR, Gantt E, Cunningham FX (1996) Cloning and functional analysis of the beta-carotene hydroxylase of Arabidopsis thaliana. J Biol Chem 271:24349–24352
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTALX Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Thompson AJ, Jackson AC, Parker RA, Morpeth DR, Burbidge A, Taylor IB (2000a) Abscisic acid biosynthesis in tomato: regulation of zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase mRNAs by light/dark cycles, water stress and abscisic acid. Plant Mol Biol 42:833–845
Thompson AJ, Jackson AC, Symonds RC, Mulholland BJ, Dadswell AR, Blake PS, Burbidge A, Taylor IB (2000b) Ectopic expression of a tomato 9-cis-epoxycarotenoid dioxygenase gene causes over-production of abscisic acid. Plant J 23:363–374
Thompson AJ, Mulholland BJ, Jackson AC, McKee JM, Hilton HW, Symonds RC, Sonneveld T, Burbidge A, Stevenson P, Taylor IB (2007) Regulation and manipulation of ABA biosynthesis in roots. Plant Cell Environ 30:67–78
Tian L, DellaPenna D (2001) Characterization of a second carotenoid β-hydroxylase gene from Arabidopsis and its relationship to the LUT1 locus. Plant Mol Biol 47:379–388
Tian L, Musetti V, Kim J, Magallanes-Lundback M, Dellapenna D (2004) The Arabidopsis LUT1 locus encodes a member of the cytochrome P450 family that is required for carotenoid epsilon-ring hydroxylation activity. Proc Natl Acad Sci USA 101:402–407
Tuskan GA et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604
Tuteja N (2007) Abscisic acid and abiotic stress signaling. Plant Signal Behav 2:135–138
van Norman, Jaimie M, Sieburth, Leslie E (2007) Dissecting the biosynthetic pathway for the bypass1 root-derived signal. Plant J 49:619–628
Vishnevetsky M, Ovadis M, Zuker A, 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, Kleinig H (1997) Light-stimulated carotenoid biosynthesis occurs at the level of phytoene synthase expression and is mediated by phytochrome in Sinapis alba and Arabidopsis thaliana seedlings. Plant J 12:625–634
Welsch R, Beyer P, Hugueney P, Kleinig H, von Lintig J (2000) Regulation and activation of phytoene synthase, a key enzyme in carotenoid biosynthesis, during photomorphogenesis. Planta 211:846–854
Welsch R, Wüst F, Bär C, Al-Babili S, 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
Woitsch S, Römer S (2003) Expression of xanthophyll biosynthetic genes during light-dependent chloroplast differentiation. Plant Physiol 132:1508–1517
Ye XD, Al-Babili S, Kloti A, Zhang J, Lucca P, Beyer P, Potrykus I (2000) Engineering the provitamin A (β-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287:303–305
Acknowledgments
This work was financially supported by the Department of Biotechnology, Government of India, the University Grants Commission and the Council of Scientific and Industrial Research, New Delhi (research fellowship to N. C. and A. N.). The TIGR, KOME, TAIR, NCBI and Populus database resources are gratefully acknowledged for the detailed sequence information.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Y. Van de Peer.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chaudhary, N., Nijhawan, A., Khurana, J.P. et al. Carotenoid biosynthesis genes in rice: structural analysis, genome-wide expression profiling and phylogenetic analysis. Mol Genet Genomics 283, 13–33 (2010). https://doi.org/10.1007/s00438-009-0495-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-009-0495-x