Differential expression of flavonoid 3'-hydroxylase during fruit development establishes the different B-ring hydroxylation patterns of flavonoids in Fragaria× ananassa and Fragaria vesca

Plant Physiology and Biochemistry

Volumn 72, Issue , 2013, Pages 72-78

  Thill, Jana ^a   Miosic, Silvija ^a   Gotame, Tek Prasad ^a   Mikulic Petkovsek, Maja ^b   Gosch, Christian ^a   Veberic, Robert ^b   Preuss, Anja ^c   Schwab, Wilfried ^c   Stampar, Franci ^b   Stich, Karl ^a   Halbwirth, Heidi ^a  

^a VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Anthocyanins; Flavonoid 3' hydroxylase (F3'H); Fruit color; Fruit ripening; Hydroxylation pattern; Pelargonidin; Strawberry (Fragaria sp.)

Indexed keywords

FRAGARIA; FRAGARIA VESCA; FRAGARIA X ANANASSA;

ANTHOCYANIN; CYTOCHROME P450; FLAVONOID; FLAVONOID 3' HYDROXYLASE; FLAVONOID 3'-HYDROXYLASE; PELARGONIDIN; VEGETABLE PROTEIN;

ARTICLE; ENZYMOLOGY; FLAVONOID 3′-HYDROXYLASE (F3′H); FRAGARIA; FRUIT; FRUIT COLOR; FRUIT RIPENING; GENETICS; HYDROXYLATION; HYDROXYLATION PATTERN; METABOLISM; STRAWBERRY (FRAGARIA SP.);

ANTHOCYANINS; FLAVONOID 3′-HYDROXYLASE (F3′H); FRUIT COLOR; FRUIT RIPENING; HYDROXYLATION PATTERN; PELARGONIDIN; STRAWBERRY (FRAGARIA SP.);

CYTOCHROME P-450 ENZYME SYSTEM; FLAVONOIDS; FRAGARIA; FRUIT; HYDROXYLATION; PLANT PROTEINS;

EID: 84886594920     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2013.03.019     Document Type: Article

References (41)

1. Shulaev V., Sargent D.J., Crowhurst R.N., Mockler T.C., Folkerts O., Delcher A.L., Jaiswal P., Mockaitis K., Liston A., Mane S.P. The genome of woodland strawberry (Fragaria vesca). Nature Genetics 2010, 43:109-116.
2. Velasco R., Zharkikh A., Affourtit J., Dhingra A., Cestaro A., Kalyanaraman A., Fontana P., Bhatnagar S.K., Troggio M., Pruss D. The genome of the domesticated apple (Malus x domestica Borkh.). Nature Genetics 2010, 42:833-839.
3. Treutter D., Feucht W., Christ E. Flavan-3-ols and their relation to resistance to fungi in strawberries. Mitteilungen Klosterneuburg 1991, 41:79-83.
4. Yamamoto M., Nakatsuka S., Otani H., Kohmoto K., Nishimura S. (+)-Catechin acts as an infection-inhibiting factor in strawberry leaf. Phytopathology 2000, 90:595-600.
5. Schlösser E. Preformed phenols as resistance factors. International Symposium on Natural Phenols in Plant Resistance 1993, 615-630. 381.
6. Aharoni A., Ric de Vos C., Verhoeven H.A., Maliepaard C.A., Kruppa G., Bino R., Goodenowe D.B. Nontargeted metabolome analysis by use of Fourier transform ion cyclotron mass spectrometry. Omics: A Journal of Integrative Biology 2002, 6:217-234.
7. Carbone F., Preuss A., De Vos R.C.H., D'Amico E., Perrotta G., Bovy A.G., Martens S., Rosati C. Developmental, genetic and environmental factors affect the expression of flavonoid genes, enzymes and metabolites in strawberry fruits*. Plant, Cell & Environment 2009, 32:1117-1131.
8. Kyle J., Duthie G. Flavonoids in food. Flavonoids: Chemistry, Biochemistry and Applications 2006, 219-262. CRC Press, Boca Raton, pp. hlm. O.D. Andersen, K.R. Markham (Eds.).
9. Harborne J.B. Introduction to Ecological Biochemistry 1993, Academic Pr.
10. Rice-Evans C.A., Miller N.J., Paganga G. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radical Biology and Medicine 1996, 20:933-956.
11. Scalbert A., Morand C., Manach C., Rémésy C. Absorption and metabolism of polyphenols in the gut and impact on health. Biomedicine & Pharmacotherapy 2002, 56:276-282.
12. Yao L.H., Jiang Y., Shi J., Tomas-Barberan F., Datta N., Singanusong R., Chen S. Flavonoids in food and their health benefits. Plant Foods for Human Nutrition (Formerly Qualitas Plantarum) 2004, 59:113-122.
13. Aharoni A., O'Connell A.P. Gene expression analysis of strawberry achene and receptacle maturation using DNA microarrays. Journal of Experimental Botany 2002, 53:2073-2087.
14. Griesser M., Hoffmann T., Bellido M.L., Rosati C., Fink B., Kurtzer R., Aharoni A., Muñoz-Blanco J., Schwab W. Redirection of flavonoid biosynthesis through the down-regulation of an anthocyanidin glucosyltransferase in ripening strawberry fruit. Plant Physiology 2008, 146:1528-1539.
15. Halbwirth H., Puhl I., Haas U., Jezik K., Treutter D., Stich K. Two-phase flavonoid formation in developing strawberry (Fragaria×ananassa) fruit. Journal of Agricultural and Food Chemistry 2006, 54:1479-1485.
16. Almeida J.R.M., D'Amico E., Preuss A., Carbone F., De Vos C., Deiml B., Mourgues F., Perrotta G., Fischer T.C., Bovy A.G. Characterization of major enzymes and genes involved in flavonoid and proanthocyanidin biosynthesis during fruit development in strawberry (Fragaria× ananassa). Archives of Biochemistry and Biophysics 2007, 465:61-71.
17. Miyawaki K., Fukuoka S., Kadomura Y., Hamaoka H., Mito T., Ohuchi H., Schwab W., Noji S. Establishment of a novel system to elucidate the mechanisms underlying light-induced ripening of strawberry fruit with an Agrobacterium-mediated RNAi technique. Plant Biotechnology 2012, 29:271-277.
18. Muñoz C., Sánchez-Sevilla J.F., Botella M.A., Hoffmann T., Schwab W., Valpuesta V. Polyphenol composition in the ripe fruits of Fragaria species and transcriptional analyses of key genes in the pathway. Journal of Agricultural and Food Chemistry 2011, 59:12598-12604.
19. Wang S.Y., Lewers K.S. Antioxidant capacity and flavonoid content in wild strawberries. Journal of the American Society for Horticultural Science 2007, 132:629-637.
20. Moyano E., Portero-Robles I., Medina-Escobar N., Valpuesta V., Muñoz-Blanco J., Caballero J.L. Afruit-specific putative dihydroflavonol 4-reductase gene is differentially expressed in strawberry during the ripening process. Plant Physiology 1998, 117:711-716.
21. Cheng G.W., Breen P.J. Activity of phenylalanine ammonia-lyase (PAL) and concentrations of anthocyanins and phenolics in developing strawberry fruit. Journal of the American Society for Horticultural Science 1991, 116:865-869.
22. Han Y., Vimolmangkang S., Soria-Guerra R.E., Rosales-Mendoza S., Zheng D., Lygin A.V., Korban S.S. Ectopic expression of apple F3' H genes contributes to anthocyanin accumulation in the Arabidopsis tt7 mutant grown under nitrogen stress. Plant Physiology 2010, 153:806-820.
23. Gotoh O. Substrate recognition sites in cytochrome P450 family 2 (CYP2) proteins inferred from comparative analyses of amino acid and coding nucleotide sequences. Journal of Biological Chemistry 1992, 267:83-90.
24. Kemper B. Structural basis for the role in protein folding of conserved proline-rich regions in cytochromes P450. Toxicology and Applied Pharmacology 2004, 199:305-315.
25. Ravichandran K.G., Boddupalli S.S., Hasermann C., Peterson J.A., Deisenhofer J. Crystal structure of hemoprotein domain of P450BM-3, a prototype for microsomal P450's. Science (New York, NY) 1993, 261:731.
26. Schlangen K., Miosic S., Halbwirth H. Allelic variants from Dahlia variabilis encode flavonoid 3'-hydroxylases with functional differences in chalcone 3-hydroxylase activity. Archives of Biochemistry and Biophysics 2010, 494:40-45.
27. Schlangen K., Miosic S., Topuz F., Muster G., Marosits T., Seitz C., Halbwirth H. Chalcone 3-hydroxylation is not a general property of flavonoid 3'-hydroxylase. Plant Science 2009, 177:97-102.
28. Schlangen K., Miosic S., Thill J., Halbwirth H. Cloning, functional expression, and characterization of a chalcone 3-hydroxylase from Cosmos sulphureus. Journal of Experimental Botany 2010, 61:3451-3459.
29. Roudeillac P., Trajkovski K. Breeding for fruit quality and nutrition in strawberries. Euro Berry Symposium-COST-Action 836 Final Workshop 649 2003, 55-60.
30. Hoffmann T., Kurtzer R., Skowranek K., Kießling P., Fridman E., Pichersky E., Schwab W. Metabolic engineering in strawberry fruit uncovers a dormant biosynthetic pathway. Metabolic Engineering 2011, 13:527-531.
31. Mahoney L.B. Investigation of Cyanidin and Pelargonidin Contents in the Genus Fragaria L. (Fragaria, Cyanidin, Anthocyanidins, Pelargonidin, Supercore Collection) 2008, Dissertation, University of New Hampshire.
32. Cheel J., Theoduloz C., Rodríguez J.A., Caligari P.D.S., Schmeda-Hirschmann G. Free radical scavenging activity and phenolic content in achenes and thalamus from Fragaria chiloensis ssp. chiloensis, F. vesca and F.× ananassa cv. Chandler. Food Chemistry 2007, 102:36-44.
33. Sondheimer E., Karash C.B. The major anthocyanin pigments of the wild strawberry (Fragaria vesca) 1956, 178:648-649.
34. Mikulic-Petkovsek M., Slatnar A., Stampar F., Veberic R. The influence of organic/integrated production on the content of phenolic compounds in apple leaves and fruits in four different varieties over a 2-year period. Journal of the Science of Food and Agriculture 2010, 90:2366-2378.
35. Thill J., Miosic S., Ahmed R., Schlangen K., Muster G., Stich K., Halbwirth H. 'Le Rouge et le Noir': a decline in flavone formation correlates with the rare colorof black dahlia (Dahlia variabilis hort.) flowers. BMC Plant Biology 2012, 12:225.
36. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 1994, 22:4673-4680.
37. Thompson J.D., Gibson T., Higgins D.G. Multiple sequence alignment usingClustalW and ClustalX. Current Protocols in Bioinformatics 2002, 2.3. 1-2.3. 22.
38. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 2011, 28:2731-2739.
39. Pompon D., Louerat B., Bronine A., Urban P. Yeast expression of animal and plant P450s in optimized redox environments. Methods in Enzymology 1996, 272:51-64. [6].
40. Sandermann H., Strominger J.L. Purification and properties of C55-isoprenoid alcohol phosphokinase from Staphylococcus aureus. Journal of Biological Chemistry 1972, 247:5123.
41. Hulo N., Bairoch A., Bulliard V., Cerutti L., De Castro E., Langendijk-Genevaux P.S., Pagni M., Sigrist C.J.A. The PROSITE database. Nucleic Acids Research 2006, 34:D227-D230.