New target carotenoids for CCD4 enzymes are revealed with the characterization of a novel stress-induced carotenoid cleavage dioxygenase gene from Crocus sativus

详细信息    查看全文

• 作者：Angela Rubio-Moraga ; José Luis Rambla ; Asun Fernández-de-Carmen…
• 关键词：Apocarotenoids ; Carotenoid cleavage dioxygenases ; Saffron ; Stigmas ; Stress
• 刊名：Plant Molecular Biology
• 出版年：2014
• 出版时间：November 2014
• 年：2014
• 卷：86
• 期：4-5
• 页码：555-569
• 全文大小：1,066 KB
• 参考文献：1. Ahrazem O, Rubio-Moraga A, Lopez RC, Gomez-Gomez L (2010a) The expression of a chromoplast-specific lycopene beta cyclase gene is involved in the high production of saffron’s apocarotenoid precursors. J Exp Bot 61:105-19 CrossRef
  2. Ahrazem O, Trapero A, Gomez MD, Rubio-Moraga A, Gomez-Gomez L (2010b) Genomic analysis and gene structure of the plant carotenoid dioxygenase 4 family: a deeper study in / Crocus sativus and its allies. Genomics 96:239-50 CrossRef
  3. Alder A, Holdermann I, Beyer P, Al-Babili S (2008) Carotenoid oxygenases involved in plant branching catalyse a highly specific conserved apocarotenoid cleavage reaction. Biochem J 416:289-96 CrossRef
  4. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL Workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:7 CrossRef
  5. Auldridge ME, McCarty DR, Klee HJ (2006) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9:315-21 CrossRef
  6. Baldermann S, Kato M, Kurosawa M, Kurobayashi Y, Fujita A, Fleischmann P, Watanabe N (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 Exp Bot 61:2967-977 CrossRef
  7. Bindon KA, Dry PR, Loveys BR (2007) Influence of plant water status on the production of C13-norisoprenoid precursors in / Vitis vinifera L. Cv. cabernet sauvignon grape berries. J Agric Food Chem 55:4493-500 CrossRef
  8. Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8:7 devcel.2005.01.009" target="_blank" title="It opens in new window">CrossRef
  9. Bouvier F, Suire C, Mutterer J, Camara B (2003) Oxidative remodeling of chromoplast carotenoids: identification of the carotenoid dioxygenase CsCCD and CsZCD genes involved in Crocus secondary metabolite biogenesis. Plant Cell 15:47-2 CrossRef
  10. Brandi F, Bar E, Mourgues F, Horvath 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 CrossRef
  11. Brehelin C, Kessler F, van Wijk KJ (2007) Plastoglobules: versatile lipoprotein particles in plastids. Trends Plant Sci 12:260-66 CrossRef
  12. Brilli F, Barta C, Fortunati A, Lerdau M, Loreto F, Centritto M (2007) Response of isoprene emission and carbon metabolism to drought in white poplar ( / Populus alba) saplings. New Phytol 175:244-54 CrossRef
  13. 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 154:656-64 CrossRef
  14. Castillo R, Fernandez JA, Gomez-Gomez L (2005) Implications of carotenoid biosynthetic genes in apocarotenoid formation during the stigma development of / Crocus sativus and its closer relatives. Plant Physiol 139:674-89 CrossRef
  15. Cunningham FX Jr, Pogson B, Sun Z, McDonald KA, DellaPenna D, Gantt E (1996) Functional analysis of the beta and epsilon lycopene cyclase enzymes of Arabidopsis reveals a mechanism for control of cyclic carotenoid formation. Plant Cell 8:1613-626
  16. Dun EA, Brewer PB, Beveridge CA (2009) Strigolactones: discovery of the elusive shoot branching hormone. Trends Plant Sci 14:364-72 CrossRef
  17. Falchi R, Vendramin E, Zanon L, Scalabrin S, Cipriani G, Verde I, Vizzotto G, Morgante M (2013) Three distinct mutational mechanisms acting on a single gene underpin the origin of yellow flesh in peach. Plant J 76:175-87
  18. Floss DS, Schliemann W, Schmidt J, Strack D, Walter MH (2008) RNA interference-mediated repression of MtCCD1 in mycorrhizal roots of Medicago truncatula causes accumulation of C27 apocarotenoids, shedding light on the functional role of CCD1. Plant Physiol 148:1267-282 CrossRef
  19. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531-545
  20. Galpaz N, Ronen G, Khalfa Z, Zamir D, Hirschberg J (2006) A chromoplast-specific carotenoid biosynthesis pathway is revealed by cloning of the tomato white-flower locus. Plant Cell 18:1947-960 CrossRef
  21. Gang DR (2005) Evolution of flavors and scents. Annu Rev Plant Biol 56:301-25 CrossRef
  22. Garcia-Limones C, Schnabele K, Blanco-Portales R, Luz Bellido M, Caballero JL, Schwab W, Munoz-Blanco J (2088) Functional characterization of FaCCD1: a carotenoid cleavage dioxygenase from strawberry involved in lutein degradation during fruit ripening. J Agric Food Chem 56:9277-285
  23. Glover BJ (2011) Pollinator attraction: the importance of looking good and smelling nice. Curr Biol 21:R307–R309 CrossRef
  24. Ha CV, Leyva-Gonzalez MA, Osakabe Y, Tran UT, Nishiyama R, Watanabe Y, Tanaka M, Seki M, Yamaguchi S, Dong NV, Yamaguchi-Shinozaki K, Shinozaki K, Herrera-Estrella L, Tran LS (2014) Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci USA 111:851-56 CrossRef
  25. Huang FC, Horvath G, Molnar P, Turcsi E, Deli J, Schrader J, Sandmann G, Schmidt H, Schwab W (2009a) Substrate promiscuity of RdCCD1, a carotenoid cleavage oxygenase from / Rosa damascena. Phytochemistry 70:457-64 CrossRef
  26. Huang FC, Molnar P, Schwab W (2009b) Cloning and functional characterization of carotenoid cleavage dioxygenase 4 genes. J Exp Bot 60:3011-022 CrossRef
  27. Ibdah M, Azulay Y, Portnoy V, Wasserman B, Bar E, Meir A, Burger Y, Hirschberg J, Schaffer AA, Katzir N, Tadmor Y, Lewinsohn E (2006) Functional characterization of CmCCD1, a carotenoid cleavage dioxygenase from melon. Phytochemistry 67:1579-589 CrossRef
  28. 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 276:736-47 CrossRef
  29. 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 232:691-99 CrossRef
  30. Kato M, Matsumoto H, Ikoma Y, Okuda H, Yano M (2006) The role of carotenoid cleavage dioxygenases in the regulation of carotenoid profiles during maturation in citrus fruit. J Exp Bot 57:2153-164 CrossRef
  31. Kishimoto S, Sumitomo K, Nakayama M, Ohmiya A (2007) Three routes to orange petal color via carotenoid components in 9 composite species. J Jpn Soc Hortic Sci 76:8 CrossRef
  32. Klingner A, Bothe H, Wray V, Marner FJ (1995) Identification of a yellow pigment formed in maize roots upon mycorrhizal colonization. Phytochemistry 38:3 CrossRef
  33. Kloer DP, Schulz GE (2006) Structural and biological aspects of carotenoid cleavage. Cell Mol Life Sci 63:2291-303 CrossRef
  34. Lamikanra O, Richard OA, Parker A (2002) Ultraviolet induced stress response in fresh cut cantaloupe. Phytochemistry 60:27-2 CrossRef
  35. 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 CrossRef
  36. Lewinsohn E, Sitrit Y, Bar E, Azulay Y, Meir A, Zamir D, Tadmor Y (2005) Carotenoid pigmentation affects the volatile composition of tomato and watermelon fruits, as revealed by comparative genetic analyses. J Agric Food Chem 53:3142-148 CrossRef
  37. Lynch M, Conery JS (2003) The origins of genome complexity. Science 302:1401-404 CrossRef
  38. Ma G, Zhang L, Matsuta A, Matsutani K, Yamawaki K, Yahata M, Wahyudi A, Motohashi R, Kato M (2013) Enzymatic formation of beta-citraurin from beta-cryptoxanthin and zeaxanthin by carotenoid cleavage dioxygenase4 in the flavedo of citrus fruit. Plant Physiol 163:682-95 CrossRef
  39. Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M, Kuiper M, Van de Peer Y (2005) Modeling gene and genome duplications in eukaryotes. Proc Natl Acad Sci USA 102:5454-459 CrossRef
  40. Maier W, Peipp H, Schmidt J, Wray V, Strack D (1995) Levels of a terpenoid glycoside (blumenin) and cell wall-bound phenolics in some cereal mycorrhizas. Plant Physiol 109:465-70 CrossRef
  41. Mathieu S, Terrier N, Procureur J, Bigey F, Gunata Z (2005) A carotenoid cleavage dioxygenase from / Vitis vinifera L.: functional characterization and expression during grape berry development in relation to C13-norisoprenoid accumulation. J Exp Bot 56:2721-731 CrossRef
  42. Messing SA, Gabelli SB, Echeverria I, Vogel JT, Guan JC, Tan BC, Klee HJ, McCarty DR, Amzel LM (2010) Structural insights into maize viviparous14, a key enzyme in the biosynthesis of the phytohormone abscisic acid. Plant Cell 22:2970-980 CrossRef
  43. Moraga AR, Rambla JL, Ahrazem O, Granell A, Gomez-Gomez L (2009) Metabolite and target transcript analyses during / Crocus sativus stigma development. Phytochemistry 70:1009-016 CrossRef
  44. Nakagawa T, Suzuki T, Murata S, Nakamura S, Hino T, Maeo K, Tabata R, Kawai T, Tanaka K, Niwa Y, Watanabe Y, Nakamura K, Kimura T, Ishiguro S (2007) Improved gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci Biotechnol Biochem 71:2095-100 CrossRef
  45. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:9
  46. Ohmiya A, Kishimoto S, Yoshioka S, Sumitomo K (2005) Cloning of a carotenoid cleavage dioxygenase gene (CmCCD1) differentially expressed in white petals of chrysanthemum. Plant Cell Physiol 46:1 CrossRef
  47. 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 142:1193-201 CrossRef
  48. Ohmiya A, Sumitomo K, Aida A (2009) ”Yellow Jimba- supression of carotenoid cleavage dioxygenase ( / CmCCD4a) expression turns white chrysanthemum petals yellow. J Jpn Soc Hortic Sci 78:6 CrossRef
  49. Osborn TC, Pires JC, Birchler JA, Auger DL, Chen ZJ, Lee HS, Comai L, Madlung A, Doerge RW, Colot V, Martienssen RA (2003) Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19:141-47 CrossRef
  50. Pfander H, Schurtenberger H (1982) Biosynthesis of C20-Carotenoids in / Crocus sativus. Phytochemistry 21:4 CrossRef
  51. Rodrigo MJ, Alquézar B, Alós E, Medina V, Carmona L, Bruno M, Al-Babili S, Zacarias L (2013) A novel carotenoid cleavage activity involved in the biosynthesis of Citrus fruit-specific apocarotenoid pigments. J Exp Bot 64(14):4461-478
  52. Ronen G, Carmel-Goren L, Zamir D, Hirschberg J (2000) An alternative pathway to beta-carotene formation in plant chromoplasts discovered by map-based cloning of beta and old-gold color mutations in tomato. Proc Natl Acad Sci USA 97:11102-1107 CrossRef
  53. Rosati C, Diretto G, Giuliano G (2010) Biosynthesis and engineering of carotenoids and apocarotenoids in plants: state of the art and future prospects. Biotechnol Genet Eng Rev 26:139-62 CrossRef
  54. Rubio A, Rambla JL, Santaella M, Gomez MD, Orzaez D, Granell A, Gomez-Gomez L (2008) Cytosolic and plastoglobule-targeted carotenoid dioxygenases from / Crocus sativus are both involved in beta-ionone release. J Biol Chem 283:24816-4825 CrossRef
  55. Rubio-Moraga A, Ahrazem O, Perez-Clemente RM, Gomez-Cadenas A, Yoneyama K, Lopez-Raez JA, Molina RV, Gomez-Gomez L (2014) Apical dominance in saffron and the involvement of the branching enzymes CCD7 and CCD8 in the control of bud sprouting. BMC Plant Biol 14:171 CrossRef
  56. Ryle MJ, Hausinger RP (2002) Non-heme iron oxygenases. Curr Opin Chem Biol 6:193-01 CrossRef
  57. Sainsbury F, Thuenemann EC, Lomonossoff GP (2009) pEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants. Plant Biotechnol J 7:682-93 CrossRef
  58. Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872-874 CrossRef
  59. Schwartz SH, Qin X, Zeevaart JA (2001) Characterization of a novel carotenoid cleavage dioxygenase from plants. J Biol Chem 276:25208-5211 CrossRef
  60. 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 279:46940-6945 CrossRef
  61. Sharkey TD, Chen X, Yeh S (2001) Isoprene increases thermotolerance of fosmidomycin-fed leaves. Plant Physiol 125:2001-006 CrossRef
  62. 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 beta-ionone, pseudoionone, and geranylacetone. Plant J 40:882-92 CrossRef
  63. 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 beta-ionone, a fragrance volatile of petunia flowers. Plant Physiol 136:3504-514 CrossRef
  64. Simkin AJ, Moreau H, Kuntz M, Pagny G, Lin C, Tanksley S, McCarthy J (2008) An investigation of carotenoid biosynthesis in / Coffea canephora and / Coffea arabica. J Plant Physiol 165:1087-106 CrossRef
  65. Soares VL, Rodrigues SM, de Oliveira TM, de Queiroz TO, Lima LS, Hora-Junior BT, Gramacho KP, Micheli F, Cascardo JC, Otoni WC, Gesteira AS, Costa MG (2011) Unraveling new genes associated with seed development and metabolism in / Bixa orellana L. by expressed sequence tag (EST) analysis. Mol Biol Rep 38:1329-340 CrossRef
  66. Sun Z, Hans J, Walter MH, Matusova R, Beekwilder J, Verstappen FW, Ming Z, van Echtelt E, Strack D, Bisseling T, Bouwmeester HJ (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 228:789-01 CrossRef
  67. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:4 CrossRef
  68. Taylor IB, Burbidge A, Thompson AJ (2000) Control of abscisic acid synthesis. J Exp Bot 51:1563-574 CrossRef
  69. Vallabhaneni R, Bradbury LM, Wurtzel ET (2010) The carotenoid dioxygenase gene family in maize, sorghum, and rice. Arch Biochem Biophys 504:104-11 CrossRef
  70. Van Norman JM, Zhang J, Cazzonelli CI, Pogson BJ, Harrison PJ, Bugg TD, Chan KX, Thompson AJ, Benfey PN (2014) Periodic root branching in Arabidopsis requires synthesis of an uncharacterized carotenoid derivative. Proc Natl Acad Sci USA 111:E1300–E1309 CrossRef
  71. Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5:283-91 CrossRef
  72. Vogel JT, Tan BC, 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 283:11364-1373 CrossRef
  73. Voinnet O, Rivas S, Mestre P, Baulcombe D (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33:949-56 CrossRef
  74. Wahlberg I (2002) Carotenoid-derived aroma compounds in tobacco. In: Winterhalter P, Ruseff R (eds) Carotenoid-derived aroma compounds. American Chemical Society, Washington, pp 131-44
  75. Walsh JB (1995) How often do duplicated genes evolve new functions? Genetics 139:421-28
  76. Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28(4):663-69
  77. Welsch R, Wust F, Bar 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 147:367-80 CrossRef
  78. Yamamizo C, Kishimoto S, Ohmiya A (2010) Carotenoid composition and carotenogenic gene expression during Ipomoea petal development. J Exp Bot 61:709-19 CrossRef
  79. Ytterberg AJ, Peltier JB, van Wijk KJ (2006) Protein profiling of plastoglobules in chloroplasts and chromoplasts. A surprising site for differential accumulation of metabolic enzymes. Plant Physiol 140:984-97 CrossRef
  
• 作者单位：Angela Rubio-Moraga (1)
  José Luis Rambla (2)
  Asun Fernández-de-Carmen (2)
  Almudena Trapero-Mozos (1)
  Oussama Ahrazem (1) (3)
  Diego Orzáez (2)
  Antonio Granell (2)
  Lourdes Gómez-Gómez (1)
  
  1. Departamento de Ciencia y Tecnología Agroforestal y Genética, Facultad de Farmacia, Instituto Botánico, Universidad de Castilla-La Mancha, Campus Universitario s/n, 02071, Albacete, Spain
  2. Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas, Universidad Politécnica de Valencia, Camino de Vera s/n, 46022, Valencia, Spain
  3. Fundación Parque Científico y Tecnológico de Albacete, Albacete, Spain
  
• ISSN：1573-5028

文摘

Apocarotenoid compounds play diverse communication functions in plants, some of them being as hormones, pigments and volatiles. Apocarotenoids are the result of enzymatic cleavage of carotenoids catalyzed by carotenoid cleavage dioxygenase (CCD). The CCD4 family is the largest family of plant CCDs, only present in flowering plants, suggesting a functional diversification associated to the adaptation for specific physiological capacities unique to them. In saffron, two CCD4 genes have been previously isolated from the stigma tissue and related with the generation of specific volatiles involved in the attraction of pollinators. The aim of this study was to identify additional CCD4 members associated with the generation of other carotenoid-derived volatiles during the development of the stigma. The expression of CsCCD4c appears to be restricted to the stigma tissue in saffron and other Crocus species and was correlated with the generation of megastigma-4,6,8-triene. Further, CsCCD4c was up-regulated by wounding, heat, and osmotic stress, suggesting an involvement of its apocarotenoid products in the adaptation of saffron to environmental stresses. The enzymatic activity of CsCCD4c was determined in vivo in Escherichia coli and subsequently in Nicotiana benthamiana by analyzing carotenoids by HPLC–DAD and the volatile products by GC/MS. β-Carotene was shown to be the preferred substrate, being cleaved at the 9,10 (9-10- bonds and generating β-ionone, although β-cyclocitral resulting from a 7,8 (7-8- cleavage activity was also detected at lower levels. Lutein, neoxanthin and violaxanthin levels in Nicotiana leaves were markedly reduced when CsCCD4c is over expressed, suggesting that CsCCD4c recognizes these carotenoids as substrates.