Abstract
Carotenoid cleavage dioxygenases (CCDs) in plant species is one of the most important enzymes in the carotenoid metabolism. In this study, we performed a comprehensive analysis for the CCDs family in Solanum lycopersicum based on the whole tomato genome sequences and explored their expression pattern. At least seven CCD genes were discovered in the tomato genome sequence. Two pairs of them were arranged in tandem. The tandem duplication events could be dating to approximately 14 and 21 Mya, and the tandem duplication genes experienced a purifying selection during the course of evolution after diversification. Additionally, subcellular localization revealed that four members were predicted to be cytoplasm-localized and the three remaining members plastids-localized. Subsequently, a number of cis-regulatory elements, which were involved in light responsiveness, hormone regulation, and abiotic and biotic stresses, were identified in the promoter sequences of SlCCD genes. Phylogenetic tree revealed that the CCDs from Solanaceae crops have a closer genetic relationship. The difference in abundance and distinct expression patterns during the vegetative and reproductive development suggests different functions for these seven SlCCDs. Our findings suggest that SlCCDs family play important roles throughout the whole life course and will lay the foundation for further elaborating the regulatory mechanism of each member in tomato.
Similar content being viewed by others
References
Adami M, De Franceschi P, Brandi F, Liverani A, Giovannini D, Rosati C, Dondini L, Tartarini S (2013) Identifying a carotenoid cleavage dioxygenase (CCD4) gene controlling yellow/white fruit flesh color of peach. Plant Mol Biol Rep 31:1166–1175
Ahrazem O, Trapero A, Gómez MD, Rubio-Moraga A, Gómez-Gómez L (2010) Genomic analysis and gene structure of the plant carotenoid dioxygenase 4 family: a deeper study in Crocus sativus and its allies. Genomics 96:239–250
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Auldridge ME, Block A, Vogel JT, Dabney-Smith C, Mila I, Bouzayen M, Magallanes-Lundback M, DellaPenna D, McCarty DR, Klee HJ (2006a) Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. Plant J 45:982–993
Auldridge ME, McCarty DR, Klee HJ (2006b) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9:315–321
Bailey TL, Elkan C (1995) The value of prior knowledge in discovering motifs with MEME. Proc Int Conf Intell Syst Mol Biol 3:21–29
Benson G, Dong L (1999) Reconstructing the duplication history of a tandem repeat. Proc Int Conf Intell Syst Mol Biol 44–53
Blanc G, Wolfe KH (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16:1667–1678
Booker J, Auldridge M, Wills S, McCarty D, Klee H, Leyser O (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr Biol 14:1232–1238
Bouvier F, Isner J-C, Dogbo O, Camara B (2005) Oxidative tailoring of carotenoids: a prospect towards novel functions in plants. Trends Plant Sci 10:187–194
Brandi F, Bar E, Mourgues F, Horváth G, Turcsi E, Giuliano G, Liverani A, Tartarini S, Lewinsohn E, Rosati C (2011) Study of' ‘Redhaven' peach and its white-fleshed mutant suggests a key role of CCD4 carotenoid dioxygenase in carotenoid and norisoprenoid volatile metabolism. BMC Plant Biol 11:24
Britton G, Liaaen-Jensen S, Pfander HP (2004) Carotenoids: handbook. Springer
Campbell R, Ducreux LJ, Morris WL, Morris JA, Suttle JC, Ramsay G, Bryan GJ, Hedley PE, Taylor MA (2010) The metabolic and developmental roles of carotenoid cleavage dioxygenase4 from potato. Plant Physiol 154:656–664
Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10
Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, Klingenhoff A, Frisch M, Bayerlein M, Werner T (2005) MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 21:2933–2942
Expósito-Rodríguez M, Borges AA, Borges-Pérez A, Pérez JA (2008) Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biol 8:131
Freeling M (2009) Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60:433–453
Giuliano G, Al-Babili S, von Lintig J (2003) Carotenoid oxygenases: cleave it or leave it. Trend Plant Sci 8:145–149
Heo J, Kim SH, Lee PC (2013) New Insight into the Cleavage Reaction of Nostoc sp. Strain PCC 7120 Carotenoid Cleavage Dioxygenase in Natural and Nonnatural Carotenoids. Appl Environ Microb 79:3336–3345
Huang F-C, Molnár P, Schwab W (2009) Cloning and functional characterization of carotenoid cleavage dioxygenase 4 genes. J Exp Bot 60:3011–3022
Huang S, Gao Y, Liu J, Peng X, Niu X, Fei Z, Cao S, Liu Y (2012) Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. Mol Genet Genomics 287:495–513
Ibdah M, Azulay Y, Portnoy V, Wasserman B, Bar E, Meir A, Burger Y, Hirschberg J, Schaffer AA, Katzir N (2006) Functional characterization of CmCCD1, a carotenoid cleavage dioxygenase from melon. Phytochemistry 67:1579–1589
Ilg A, Beyer P, Al-Babili S (2009) Characterization of the rice carotenoid cleavage dioxygenase 1 reveals a novel route for geranial biosynthesis. FEBS J 276:736–747
Ilg A, Yu Q, Schaub P, Beyer P, Al-Babili S (2010) Overexpression of the rice carotenoid cleavage dioxygenase 1 gene in Golden Rice endosperm suggests apocarotenoids as substrates in planta. Planta 232:691–699
Jabeen R, Bhat SV, Wani AA (2013) Functions and stability of lycopene: a review. Indian J Horticul 3:57–63
Jarquín-Enríquez L, Mercado-Silva E, Maldonado J, Lopez-Baltazar J (2013) Lycopene content and color index of tomatoes are affected by the greenhouse cover. Sci Hortic-Amsterdam 155:43–48
Kloer D, Schulz G (2006) Structural and biological aspects of carotenoid cleavage. Cell Mol Life Sci 63:2291–2303
Kohlen W, Charnikhova T, Lammers M, Pollina T, Tóth P, Haider I, Pozo MJ, Maagd RA, Ruyter-Spira C, Bouwmeester HJ (2012) The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol 196:535–547
Lashbrooke JG, Young PR, Dockrall SJ, Vasanth K, Vivier MA (2013) Functional characterisation of three members of the Vitis vinifera L. carotenoid cleavage dioxygenase gene family. BMC Plant Biol 13:156
Ledger SE, Janssen BJ, Karunairetnam S, Wang T, Snowden KC (2010) Modified CAROTENOID CLEAVAGE DIOXYGENASE8 expression correlates with altered branching in kiwifruit (Actinidia chinensis). New Phytol 188:803–813
Li X, Cheng Y, Ma W, Zhao Y, Jiang H, Zhang M (2010) Identification and characterization of NBS-encoding disease resistance genes in Lotus japonicus. Plant Syst Evol 289:101–110
Liang YS, Jeon Y-A, Lim S-H, Kim JK, Lee J-Y, Kim Y-M, Lee Y-H, Ha S-H (2011) Vascular-specific activity of the Arabidopsis carotenoid cleavage dioxygenase 7 gene promoter. Plant Cell Rep 30:973–980
Liu J, Novero M, Charnikhova T, Ferrandino A, Schubert A, Ruyter-Spira C, Bonfante P, Lovisolo C, Bouwmeester HJ, Cardinale F (2013) CAROTENOID CLEAVAGE DIOXYGENASE 7 modulates plant growth, reproduction, senescence, and determinate nodulation in the model legume Lotus japonicus. J Exp Bot 64:1967–1981
Nagal S, Kaur C, Choudhary H, Singh J, Bhushan Singh B, Singh K (2012) Lycopene content, antioxidant capacity and colour attributes of selected watermelon (Citrullus lanatus (Thunb.) Mansfeld) cultivars grown in India. Int J Food Sci Nutr 63:996–1000
Ohmiya A, Kishimoto S, Aida R, Yoshioka S, Sumitomo K (2006) Carotenoid cleavage dioxygenase (CmCCD4a) contributes to white color formation in chrysanthemum petals. Plant Physiol 142:1193–1201
Ohmiya A, Sumitomo K, Aida R (2009) “Yellow Jimba”: suppression of carotenoid cleavage dioxygenase (CmCCD4a) expression turns white chrysanthemum petals yellow. J Jpn Soc Hortic Sci 78:450–455
Pasare SA, Ducreux LJ, Morris WL, Campbell R, Sharma SK, Roumeliotis E, Kohlen W, van der Krol S, Bramley PM, Roberts AG, Fraser PD, Taylor MA (2013) The role of the potato (Solanum tuberosum) CCD8 gene in stolon and tuber development. New Phytol 198:1108–1120
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29:e45–e45
Rubio A, Rambla JL, Santaella M, Gómez MD, Orzaez D, Granell A, Gómez-Gómez L (2008) Cytosolic and plastoglobule-targeted carotenoid dioxygenases from Crocus sativus are both involved in β-ionone release. J Biol Chem 283:24816–24825
Sato S, Tabata S, Hirakawa H, Asamizu E, Shirasawa K, Isobe S et al (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641
Schwartz SH, Qin X, Loewen MC (2004) The biochemical characterization of two carotenoid cleavage enzymes from Arabidopsis indicates that a carotenoid-derived compound inhibits lateral branching. J Biol Chem 279:46940–46945
Sharp P, Li W-H (1987) The rate of synonymous substitution in enterobacterial genes is inversely related to codon usage bias. Mol Biol Evol 4:222–230
Simkin AJ, Schwartz SH, Auldridge M, Taylor MG, Klee HJ (2004a) The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles β-ionone, pseudoionone, and geranylacetone. Plant J 40:882–892
Simkin AJ, Underwood BA, Auldridge M, Loucas HM, Shibuya K, Schmelz E, Clark DG, Klee HJ (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
Snowden KC, Simkin AJ, Janssen BJ, Templeton KR, Loucas HM, Simons JL, Karunairetnam S, Gleave AP, Clark DG, Klee HJ (2005) The Decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 17:746–759
Sui X, Kiser PD, von Lintig J, Palczewski K (2013) Structural basis of carotenoid cleavage: from bacteria to mammals. Arch Biochem Biophys 539:203–213
Sun Z, Hans J, Walter MH, Matusova R, Beekwilder J, Verstappen FW, Ming Z, van Echtelt E, Strack D, Bisseling T (2008) Cloning and characterisation of a maize carotenoid cleavage dioxygenase (ZmCCD1) and its involvement in the biosynthesis of apocarotenoids with various roles in mutualistic and parasitic interactions. Planta 228:789–801
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tan BC, Schwartz SH, Zeevaart JA, McCarty DR (1997) Genetic control of abscisic acid biosynthesis in maize. Proc Natl Acad Sci U S A 94:12235–12240
Tan BC, Joseph LM, Deng WT, Liu L, Li QB, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis- epoxycarotenoid dioxygenase gene family. Plant J 35:44–56
Thompson AJ, Jackson AC, Symonds RC, Mulholland BJ, Dadswell AR, Blake PS, Burbidge A, Taylor IB (2000) Ectopic expression of a tomato 9-cis-epoxycarotenoid dioxygenase gene causes over-production of abscisic acid. Plant J 23:363–374
Vallabhaneni R, Bradbury LM, Wurtzel ET (2010) The carotenoid dioxygenase gene family in maize, sorghum, and rice. Arch Biochem Biophys 504:104–111
Vogel JT, Tan B-C, McCarty DR, Klee HJ (2008) The carotenoid cleavage dioxygenase 1 enzyme has broad substrate specificity, cleaving multiple carotenoids at two different bond positions. J Biol Chem 283:11364–11373
Vogel JT, Walter MH, Giavalisco P, Lytovchenko A, Kohlen W, Charnikhova T, Simkin AJ, Goulet C, Strack D, Bouwmeester HJ (2010) SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. Plant J 61:300–311
Walter MH, Floss DS, Strack D (2010) Apocarotenoids: hormones, mycorrhizal metabolites and aroma volatiles. Planta 232:1–17
Woffelman C (1994) DNAMAN for windows, version 2.6. Lynon Biosoft, Institute of Molecular Plant Sciences, Leiden University, the Netherlands
Woitsch S, Römer S (2003) Expression of xanthophyll biosynthetic genes during light-dependent chloroplast differentiation. Plant Physiol 132:1508–1517
Zhang M, Leng P, Zhang G, Li X (2009a) Cloning and functional analysis of 9-cis-epoxycarotenoid dioxygenase (NCED) genes encoding a key enzyme during abscisic acid biosynthesis from peach and grape fruits. J Plant Physiol 166:1241–1252
Zhang M, Yuan B, Leng P (2009b) Cloning of 9-cis-epoxycarotenoid dioxygenase (NCED) gene and the role of ABA on fruit ripening. Plant Signal Behav 4:460–463
Zhang M, Yuan B, Leng P (2009c) The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. J Exp Bot 60:1579–1588
Acknowledgments
This study was partially supported by the State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control (No. 2010DS700124-KF1518), the Young Talent Training Program of Zhejiang Academy of Agricultural Sciences (2015R23R08E09), the Zhejiang Provincial Natural Science Foundation of China (LQ12C150020), General Program from the National Natural Science Foundation of China (31301774, 31272156, and 31071800), Public Agricultural Technology Application Research Project for Zhejiang Province (2013C32G4010256), Breeding of Vegetable Varieties in Zhejiang Province (2009C02006-1), Technological System of Ordinary Vegetable Industry (CARS-25-G-16), Zhejiang Provincial Vegetable Industry Innovation Team (2009R50026), Zhejiang Provincial major Agricultural Science and Technology Projects of New Varieties Breeding (2012C12903), and Molecular Breeding of Major Vegetable and Functional Genomics Research (2012AA1001).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wei, Y., Wan, H., Wu, Z. et al. A Comprehensive Analysis of Carotenoid Cleavage Dioxygenases Genes in Solanum Lycopersicum . Plant Mol Biol Rep 34, 512–523 (2016). https://doi.org/10.1007/s11105-015-0943-1
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-015-0943-1