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Advances of CCD Subfamily in Higher Plants |
LIU Yu-Cheng1, 2, ZHANG Chao1, DONG Bin1, ZHAO Hong-Bo1, * |
1 School of Landscape Architecture, Zhejiang A & F University, Hangzhou 311300, China; 2 Research Institute of Forestry,Chinese Academy of Forestry, Beijing 100091, China |
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Abstract Carotenoids are one of the most important pigments in plants, apocarotenoids from carotenoids via carotenoids cleavage dioxygenases (CCDs) or non-enzyme pathway and their derivatives play an important role in plants as pigment, plant hormone, volatiles and signals. CCD family consists of two subfamilies: CCD and NCED. To date, five members in CCD subfamily including CCD1, CCD2, CCD4, CCD7 and CCD8 have been cloned from higher plants. It has been proved that CCD1 and CCD4 play important role in color and volatiles (eg, α-ionone and β-ionone) formation of flowers and fruits in plants. CCD2 was only found in Crocus plants, which was involved in the formation of aroma and pigments (eg, crocetin). CCD7 and CCD8 were involved in formation of strigolactone. In this paper, in order to provide references for the functional research and future application of CCD subfamily genes, the structure, expression patterns and functions of various members of CCD subfamily genes in higher plants are summarized, and further research directions and keynote are prospected.
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Received: 26 October 2018
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Corresponding Authors:
zhaohb@zafu.edu.cn
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1 吴转娣, 刘新龙, 刘家勇,等. 2016. 甘蔗独脚金内酯生物合成基因ScCCD8的克隆与表达分析[J]. 中国农业科学, 49: 2662-2674. (Wu Z T, Liu X L, Liu J Y, et al.2016. Cloing and expression analysis of strigolactones biosynthesis-related gene ScCCD8 in sugarcane[J]. Scientia Agriculture Sincia, 49: 2662-2674.) 2 Adami M, Franceshi P D, Brandi F, et al.2013. Identifying a carotenoid cleavage dioxygenase (ccd4) gene controlling yellow/white fruit flesh color of peach[J]. Plant Molecular Biology Reporter, 31: 1166-1175(1110). 3 Ahrazem O, Rubio-Moraga A, Argando A-Picazo J, et al.2016. Intron retention and rhythmic diel pattern regulation of carotenoid cleavage dioxygenase 2 during crocetin biosynthesis in saffron[J]. Plant Molecular Biology, 91: 1-20. 4 Ahrazem O, Rubio-Moraga A, Berman J, et al.2015a. The carotenoid cleavage dioxygenase CCD2 catalysing the synthesis of crocetin in spring crocuses and saffron is a plastidial enzyme[J]. New Phytologist, 209: 650-663. 5 Ahrazem O, Rubio-Moraga A, Jimeno M L, et al.2015b. Structural characterization of highly glucosylated crocins and regulation of their biosynthesis during flower development in Crocus[J]. Frontiers in Plant Science, 6: 53-85. 6 Alder A, Jamil M, Marzorati M, et al.2012. The path from β-carotene to carlactone, a strigolactone-like plant hormone[J]. Science, 335: 1348. 7 Angela R M A, Rambla J L, Fern N D C A, et al.2014. New target carotenoids for CCD4 enzymes are revealed with the characterization of a novel stress-induced carotenoid cleavage dioxygenase gene from Crocus sativus[J]. Plant Molecular Biology, 86: 555-569. 8 Auldridge M E, Block A, Vogel J T, et al.2006a. Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family[J]. Plant Journal, 45: 982-993. 9 Auldridge M E, Mccarty D R, Klee H J.2006b. Plant carotenoid cleavage oxygenases and their apocarotenoid products[J]. Current Opinion in Plant Biology, 9: 315-321. 10 Avendaño-Vázquez O V, Cordoba E, Llamas, E.2014. An uncharacterized apocarotenoid-derived signal generated in ζ-carotene desaturase mutants regulates leaf development and the expression of chloroplast and nuclear genes in Arabidopsis[J]. Plant Cell, 26: 2524-2537. 11 Bai S, Tuan P A, Tatsuki M, et al.2015. Knockdown of carotenoid cleavage dioxygenase 4 (CCD4) via virus-induced gene silencing confers yellow coloration in peach fruit: Evaluation of gene function related to fruit traits[J]. Plant Molecular Biology Reporter: 1-8. 12 Baldermann S, Kato M, Fleischmann P, et al.2012. Biosynthesis of α-and β-ionone, prominent scent compounds, in flowers of Osmanthus fragrans[J]. Acta Biochimica Polonica, 59: 79-81. 13 Baldermann S, Kato M, Kurosawa M, et al.2010. Functional characterization of a carotenoid cleavage dioxygenase 1 and its relation to the carotenoid accumulation and volatile emission during the floral development of Osmanthus fragrans Lour[J]. Journal of Experimental Botany, 61: 2967-2977. 14 Booker J, Sieberer T, Wright W, et al.2005. MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone[J]. Developmental Cell, 8: 443-449. 15 Bruno M, Vermathen M, Alder A, et al.2017. Insights into the formation of carlactone from in-depth analysis of the CCD8-catalyzed reactions[J]. Febs Letters, 591: 792-800. 16 Cao Y, Guo X L, Zhang Q, et al.2005. Isolation and characterization of carotenoid cleavage dioxygenase genein halophyte Suaeda salsa[J]. Plant Growth Regulation, 46: 61-67. 17 Carmen G I, Kerstin S, Rosario B, et al.2008. Functional characterization of FaCCD1: A carotenoid cleavage dioxygenase from strawberry involved in lutein degradation during fruit ripening[J]. Journal of Agriculture & Food Chemistry, 56: 9277-9285. 18 Cazzonelli C I, Pogson B J.2010. Source to sink: Regulation of carotenoid biosynthesis in plants[J]. Trends Plant Science, 15: 266-274. 19 Floss D S, Walter M H.2009. Role of carotenoid cleavage dioxygenase 1 (CCD1) in apocarotenoid biogenesis revisited[J]. Plant Signaling &Behavior, 4: 172-175. 20 Frusciante S, Diretto G, Bruno M, et al.2014. Novel carotenoid cleavage dioxygenase catalyzes the first dedicated step in saffron crocin biosynthesis[J]. Proceedings of the National Academy of Sciences of the USA, 111: 12246-12251. 21 Fukamatsu Y, Tamura T, Hihara S, et al.2013. Mutations in the CCD4 carotenoid cleavage dioxygenase gene of yellow-flesh peaches[J]. Bioscience Biotechnology & Biochemistry, 77: 2514-2516. 22 Gao J, Zhang T, Xu B, et al.2018. CRISPR/Cas9-mediated mutagenesis of carotenoid cleavage dioxygenase 8 (CCD8) in tobacco affects shoot and root architecture[J]. International Journal of Molecular Sciences, 19: 1062. 23 Gonzalez-Verdejo C I, Obrero A, Roman B, et al.2015. Expression profile of carotenoid cleavage dioxygenase genes in summer squash (Cucurbita pepo L.)[J]. Plant Foods for Human Nutrition, 70: 200-206. 24 Hai N T L, Ji M, Ikuo M, et al.2012. Involvement of carotenoid cleavage dioxygenase 4 gene in tepal color change in Lilium brownii var. colchesteri[J]. Journal-Japanese Society for Horticultural Science, 81: 366-373. 25 Han Y, Wang X, Chen W, et al.2014. Differential expression of carotenoid-related genes determines diversified carotenoid coloration in flower petal of Osmanthus fragrans[J]. Tree Genetics & Genomes, 10: 329-338. 26 Hou X, Rivers J, Le N P, et al.2016. Synthesis and function of apocarotenoid signals in plants[J]. Trends in Plant Science, 21: 792-803. 27 Huang F C, Horvath G, Molnar P, et al.2009a. Substrate promiscuity of RdCCD1, a carotenoid cleavage oxygenase from Rosa damascena[J]. Phytochemistry, 70: 457-464. 28 Huang F C, Molnar P, Schwab W.2009b. Cloning and functional characterization of carotenoid cleavage dioxygenase 4 genes[J]. Journal of Experimental Botony, 60: 3011-3022. 29 Ibdah M, Azulay Y, Portnoy V, et al.2006. Functional characterization of CmCCD1, a carotenoid cleavage dioxygenase from melon[J]. Phytochemistry, 67: 1579-1589. 30 Ilg A, Beter P, Al-Babili S.2009. Characterization of the rice carotenoid cleavage dioxygenase 1 reveals a novel route for geranial biosynthesis[J]. FEBS Journal, 276: 736-747. 31 Ilg A, Bruno M, Beyer P, et al.2014. Tomato carotenoid cleavage dioxygenases 1A and 1B: Relaxed double bond specificity leads to a plenitude of dialdehydes, mono-apocarotenoids and isoprenoid volatiles[J]. FEBS Open Bio, 4: 584-593. 32 Ilg A, Yu Q, Schaub P, et al.2010. Overexpression of the rice carotenoid cleavage dioxygenase 1 gene in Golden Rice endosperm suggests apocarotenoids as substrates in planta[J]. Planta, 232: 691-699. 33 Ji A, Jia J, Xu Z, et al.2017. Transcriptome-guided mining of genes involved in crocin biosynthesis[J]. Frontiers in Plant Science, 8: 518. 34 Jo Y D, Kim Y S, Ryu J, et al.2016. Deletion of carotenoid cleavage dioxygenase 4a (CmCCD4a) and global up-regulation of plastid protein-coding genes in a mutant chrysanthemum cultivar producing yellow petals[J]. Scientia Horticulturae, 212: 49-59. 35 Johnson J D.2009. Do carotenoids serve as transmembrane radical channels?[J]. Free Radical Biology & Medicine, 47: 321-323. 36 Karppinen K, Zoratti L, Sarala M, et al.2016. Carotenoid metabolism during bilberry (Vaccinium myrtillus L.) fruit development under different light conditions is regulated by biosynthesis and degradation[J]. BMC Plant Biology, 16: 1-16. 37 Kato M, Matsumoto H, Ikoma Y, et al.2006. The role of carotenoid cleavage dioxygenases in the regulation of carotenoid profiles during maturation in citrus fruit[J]. Journal of Experimental Botony, 57: 2153-2164. 38 Kulkarni K P, Vishwakarma C, Sahoo S P, et al.2014. A substitution mutation in OsCCD7 cosegregates with dwarf and increased tillering phenotype in rice[J]. Journal of Genetics, 93: 389-401. 39 Lashbrooke J G, Young P R, Dockrall S J, et al.2013. Functional characterisation of three members of the Vitis vinifera L. carotenoid cleavage dioxygenase gene family[J]. BMC Plant Biology, 13: 156-173. 40 Ledger S E, Janssen B J, Karunairetnam S, et al.2010. Modified CAROTENOID CLEAVAGE DIOXYGENASE8 expression correlates with altered branching in kiwifruit (Actinidia chinensis)[J]. New Phytologist, 188: 803-813. 41 Liu H, Kishimoto S, Yamamizo C, et al.2013. Carotenoid accumulations and carotenogenic gene expressions in the petals of Eustoma grandiflorum[J]. Plant Breeding, 132: 417-422. 42 Liu J, Novero M, Charnikhova T, et al.2013. CAROTENOID CLEAVAGE DIOXYGENASE 7 modulates plant growth, reproduction, senescence, and determinate nodulation in the model legume Lotus japonicus[J]. Journal of Experimental Botony, 64: 1967-1981. 43 Liu S Q, Tian N, Liu Z H, et al.2011. Cloning and characterization of a carotenoid cleavage dioxygenase from Artemisia annua L[J]. Applied Mechanics and Materials, 108: 274-281. 44 Lpez J, Essus K, Kim I K, et al.2015. Production of β-ionone by combined expression of carotenogenic and plant CCD1 genes in Saccharomyces cerevisiae[J]. Microbial Cell Factories, 14: 84-97. 45 Ma G, Zhang L, Matsuta A, et al.2013. Enzymatic formation of β-citraurin from β-cryptoxanthin and Zeaxanthin by carotenoid cleavage dioxygenase 4 in the flavedo of citrus fruit[J]. Plant Physiology, 163: 682-695. 46 Mark B, Peter B, Salim A B.2015. The potato carotenoid cleavage dioxygenase 4 catalyzes a single cleavage of β-ionone ring-containing carotenes and non-epoxidated xanthophylls[J]. Archives of Biochemistry and Biophysics, 572: 126-133. 47 Mathieu S, Terrier N, Procureur J, et al.2005. A carotenoid cleavage dioxygenase from Vitis vinifera L.: Functional characterization and expression during grape berry development in relation to C13-norisoprenoid accumulation[J]. Journal of Experimental Botony[J], 56: 2721-2731. 48 Mikihisa U, Atsushi H, Satoko Y, et al.2008. Inhibition of shoot branching by new terpenoid plant hormones[J]. Nature, 455: 195-200. 49 Ohmiya A.2009. Carotenoid cleavage dioxygenases and their apocarotenoid products in plants[J]. Plant Biotechnology, 26: 351-358. 50 Pan X, Zheng H, Zhao J, et al.2016. ZmCCD7/ZpCCD7 encodes a carotenoid cleavage dioxygenase mediating shoot branching[J]. Planta, 243: 1407-1418. 51 Pasare S A, Ducreux L J M, Morris W L, et al.2013. The role of the potato (Solanum tuberosum) CCD8 gene in stolon and tuber development[J]. New Phytologist, 198: 1108-1120. 52 Rodrigo M A J, Alqu Z B A E, Vctor M, et al.2013. A novel carotenoid cleavage activity involved in the biosynthesis of Citrus fruit-specific apocarotenoid pigments[J]. Journal of Experimental Botony, 64: 4461. 53 Rottet S, Devillers J, Glauser G, et al.2016. Identification of plastoglobules as a site of carotenoid cleavage[J]. Frontiers in Plant Science, 7: 1855. 54 Rubio A, Rambla J L, Santaella M, et al.2008. Cytosolic and plastoglobule-targeted carotenoid dioxygenases from Crocus sativus are both involved in beta-ionone release[J]. Journal of Biological Chemistry, 283: 24816-24825. 55 Rubiomoraga A, Ahrazem O, Pérez-Clemente R M, et al.2014. Apical dominance in saffron and the involvement of the branching enzymes CCD7 and CCD8 in the control of bud sprouting[J]. BMC Plant Biology, 14: 171-186. 56 Sabrina G J, Sun-Hwa H, Maria M L, et al.2013. Carotenoid cleavage dioxygenase4 is a negative regulator of β-carotene content in Arabidopsis seeds[J]. Plant Cell, 25: 4812-4826. 57 Sankari M, Hemachandram H, Anantharaman A, et al.2016. Identifying a carotenoid cleavage dioxygenase 4a gene and its efficient Agrobacterium -mediated genetic transformation in Bixa orellana L[J]. Applied Biochemistry & Biotechnology, 179: 1-18. 58 Schmidt H, Kurtzer R, Eisenreich W, et al.2006. The carotenase AtCCD1 from Arabidopsis thaliana is a dioxygenase[J]. Journal of Biological Chemistry, 281: 9845-9851. 59 Schwartz S H, Qin X, Loewen M C.2004. The biochemical characterization of two carotenoid cleavage enzymes from Arabidopsis indicates that a carotenoid-derived compound inhibits lateral branching[J]. Journal of Biological Chemistry, 279: 46940-46945. 60 Schwartz S H, Tan B C, Gage D A, et al.1997. Specific oxidative cleavage of carotenoids by VP14 of maize[J]. Science, 276: 1872-1874. 61 Simkin A J, Schwartz S H, Auldridge M, et al.2004a. The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles beta-ionone, pseudoionone, and geranylacetone[J]. Plant Journal, 40: 882-892. 62 Simkin A J, Underwood B A, Auldridge M, et al.2004b. Circadian regulation of the PhCCD1 carotenoid cleavage dioxygenase controls emission of beta-ionone, a fragrance volatile of petunia flowers[J]. Plant Physiology, 136: 3504-3514. 63 Snowden K C, Simkin A J, Janssen B J, et al.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[J]. Plant Cell, 17: 746-759. 64 Song M H, Lim S H, Kim J K, et al.2016. In planta cleavage of carotenoids by Arabidopsis carotenoid cleavage dioxygenase 4 in transgenic rice plants[J]. Plant Biotechnology Report, 10: 291-300. 65 Sun Z, Hans J, Walter M H, et al.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[J]. Planta, 228: 789-801. 66 Tian X, Ji J, Gang W, et al.2015. Molecular cloning and characterization of a novel carotenoid cleavage dioxygenase 1 from Lycium chinense[J]. Biotechnology and Applied Biochemistry, 62: 772-779. 67 Tuan P A, Park S U.2013. Molecular cloning and characterization of cDNAs encoding carotenoid cleavage dioxygenase in bitter melon (Momordica charantia)[J]. Journal of Plant Physiology, 170: 115-120. 68 Ureshino K, Nakayama M, Miyajima I.2016. Contribution made by the carotenoid cleavage dioxygenase 4 gene to yellow colour fade in azalea petals[J]. Euphytica, 207: 401-417. 69 Vogel J T, Tan B C, Mccrty D R, et al.2008. The Carotenoid cleavage dioxygenase 1 enzyme has broad substrate specificity, cleaving multiple carotenoids at two different bond positions[J]. Journal of Biological Chemistry, 283: 11364-11373. 70 Vogel J T, Walter M H, Giavalisco P, et al.2009. SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato[J]. The Plant Journal, 61: 300-311. 71 Walter M H, Strack D2011. Carotenoids and their cleavage products: Biosynthesis and functions[J]. Natural Product Reports, 28: 663-692. 72 Wang R K, Wang C E, Fei Y Y, et al.2013. Genome-wide identification and transcription analysis of soybean carotenoid oxygenase genes during abiotic stress treatments[J]. Molecular Biology Reports, 40: 4737-4745. 73 Wang Y, Zhang C, Dong B, et al.2018. Carotenoid accumulation and its contribution to flower coloration of Osmanthus fragrans[J]. Frontiers in Plant Science, 9: 1499. 74 Wei Y, Wan H, Wu Z, et al.2015. A comprehensive analysis of carotenoid cleavage dioxygenases genes in Solanum Lycopersicum[J]. Plant Molecular Biology Reporter, 34: 512-523. 75 Yahyaa M, Bar E, Dubey N K, et al.2013. Formation of norisoprenoid flavor compounds in carrot (Daucus carota L.) roots: Characterization of a cyclic-specific carotenoid cleavage dioxygenase 1 gene[J]. Journal of Agricultural & Food Chemistry, 61: 12244-12252. 76 Yahyaa M, Berim A, Isaacson T, et al.2015. Isolation and functional characterization of carotenoid cleavage dioxygenase-1 from Laurus nobilis L. (Bay Laurel) fruits[J]. Journal of Agricultural & Food Chemistry, 63: 8275-8282. 77 Yoshioka S, Aida R, Yamamizo C, et al.2012. The carotenoid cleavage dioxygenase 4 (CmCCD4a) gene family encodes a key regulator of petal color mutation in chrysanthemum[J]. Euphytica, 184: 377-387. 78 Zhang B, Liu C, Wang Y, et al.2015. Disruption of a CAROTENOID CLEAVAGE DIOXYGENASE 4 gene converts flower colour from white to yellow in Brassica species[J]. New Phytologist, 206(4): 1513-1526. 79 Zhang Y, Dijk A D J V, Scaffidi A, et al.2014. Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis[J]. Nature Chemical Biology, 10: 1028-1033. 80 Zheng X, Xie Z, Zhu K, et al.2015. Isolation and characterization of carotenoid cleavage dioxygenase 4 genes from different Citrus species[J]. Molecular Genetics and Genomics, 290: 1-15. |
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