Tyrosine hydroxylation in betalain pigment biosynthesis is performed by cytochrome P450 enzymes in beets (Beta vulgaris)

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Sunnadeniya, Rasika ^a   Bean, Alexander ^a   Brown, Matthew ^a   Akhavan, Neda ^a   Hatlestad, Gregory ^a   Gonzalez, Antonio ^a   Symonds, V Vaughan ^b   Lloyd, Alan ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b MASSEY UNIVERSITY   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

BETACYANIN; BETALAIN; CYTOCHROME P450; CYTOCHROME P450 76AD1; CYTOCHROME P450 76AD5; CYTOCHROME P450 76AD6; LEVODOPA; TYROSINE; UNCLASSIFIED DRUG; OXYGENASE;

ARABIDOPSIS THALIANA; ARTICLE; BEET; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENE LOCUS; HAIRY ROOT CULTURE; HYDROXYLATION; NONHUMAN; PLESIOMORPHY; YEAST; AMINO ACID SEQUENCE; ARABIDOPSIS; BIOSYNTHESIS; CHEMISTRY; CLASSIFICATION; CONSERVED SEQUENCE; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; PHENOTYPE; PHYLOGENY; POSITION WEIGHT MATRIX;

AMINO ACID SEQUENCE; ARABIDOPSIS; BETA VULGARIS; BETACYANINS; BETALAINS; CONSERVED SEQUENCE; CYTOCHROME P-450 ENZYME SYSTEM; GENE EXPRESSION; GENE EXPRESSION PROFILING; HYDROXYLATION; LEVODOPA; OXYGENASES; PHENOTYPE; PHYLOGENY; POSITION-SPECIFIC SCORING MATRICES; TYROSINE;

EID: 84960510274     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0149417     Document Type: Article

References (38)

1. Christinet L, Burdet FX, Zaiko M, Hinz U, Zryd JP. Characterization and functional identification of a novel plant 4,5-extradiol dioxygenase involved in betalain pigment biosynthesis in Portulaca grandiflora. Plant Physiol. 2004: 134: 265-274. PMID: 14730069
2. Sasaki N, Abe Y, Goda Y, Adachi T, Kasahara K, Ozeki Y. Detection of DOPA 4,5-dioxygenase (DOD) activity using recombinant protein prepared from Escherichia coli cells harboring cDNA encoding DOD from Mirabilis jalapa. Plant Cell Physiol. 2009: 50: 1012-1016. doi: 10.1093/pcp/pcp053 PMID: 19366710
3. Gandía-Herrero F, García-Carmona F. Characterization of recombinant Beta vulgaris 4,5-extradiol dioxygenase active in the biosynthesis of betalains. Planta 2012: 236: 91-100. doi: 10.1007/s00425-012-1593-2 PMID: 22270561
4. Hatlestad GJ, Sunnadeniya RM, Akhavan NA, Gonzalez A, Goldman IL, McGrath JM, et al. The beet R locus encodes a new cytochrome P450 required for red betalain production. Nature Genetics 2012: 44: 816-820. doi: 10.1038/ng.2297 PMID: 22660548
5. DeLoache WC, Russ ZN, Narcross L, Gonzales AM, Martin VJJ, Dueber JE. An enzyme-coupled biosensor enables (S)-reticuline production in yeast from glucose. Nature Chemical Biology 2015: 11: 465-471. doi: 10.1038/nchembio.1816 PMID: 25984720
6. Schliemann W, Kobayashi N, Strack D. The decisive step in betaxanthin biosynthesis is a spontaneous reaction. Plant Physiology 1999: 119: 1217-1232. PMID: 10198080
7. Steiner U, Schliemann W, Böhm H, Strack D. Tyrosinase involved in betalain biosynthesis of higher plants. Planta 1999: 208: 114-124.
8. Strack D. Schliemann W. Bifunctional Polyphenol Oxidases: novel functions in plant pigment biosynthesis. Angew. Chem. Int. Ed. 2001: 40: 3791-3794.
9. Joy RWIV, Sugiyama M, Fukuda H Komamine A. Cloning and characterization of polyphenol oxidase cDNAs of Phytolacca americana. Plant Physiol. 1995: 107: 1083-1089. PMID: 7539531
10. Gandía-Herrero F, García-Carmona F, Escribano J. Purification and characterization of a latent polyphenol oxidase from beet root (Beta vulgaris L). J. Agric. Food Chem. 2004: 52: 609-15. PMID: 14759157
11. Gao Z.-J, Han X-H, Xiao X-G. Purification and characterization of polyphenol oxidase from red Swiss chard (Beta vulgaris subspecies cicla) leaves. Food Chem. 2009: 117: 342-348.
12. Yamamoto K, Kobayashi N, Yoshitama K, Teramoto S, Komamine A. Isolation and purification of tyrosine hydroxylase from callus cultures of Portulaca grandiflora. Plant Cell Physiol. 2001: 42: 969-975. PMID: 11577191
13. Nakatsuka T, Yamada E, Takahashi H, Imamura T, Suzuki M, Ozeki Y, et al. Genetic engineering of yellow betalain pigments beyond the species barrier. Scientific Reports 2013: 3: 1970. doi: 10.1038/srep01970 PMID: 23760173
14. Mayer AM Polyphenol oxidases in plants and fungi: Going places? A review. Phytochemistry 2006: 67, 2318-231. PMID: 16973188
15. Sullivan M. Beyond brown: polyphenol oxidases as enzymes of plant specialized metabolism. Front. Plant Sci. 2015: 5: 783. doi: 10.3389/fpls.2014.00783 PMID: 25642234
16. Polturak G, Breitel D, Grossman N, Sarrion-Perdigones A, Weithorn E, Pliner M, et al. Elucidation of the first committed step in betalain biosynthesis enables the heterologous engineering of betalain pigments in plants. New Phytologist 2015: doi: 10.1111/nph.13796
17. Brockington SF, Yang Y, Gandia-Herrero F, Covshoff S, Hibberd JM, Sage RF, et al. Lineage-specific gene radiations underlie the evolution of novel betalain pigmentation in Caryophyllales. New Phytologist 2015: 207: 1170-1180. doi: 10.1111/nph.13441 PMID: 25966996
18. Keller W. Inheritance of some major color types in beets. J. Agric. Res. 1936: 52: 27-38.
19. Karimi M, Inze D, Depicker A. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 2002: 7: 193-195. PMID: 11992820
20. Quandt HJ, Pühler A, Broer I. Transgenic root nodules of Vicia hirsuta: a fast and efficient system for the study of gene expression in indeterminate-type nodules. Molecular Plant-Microbe Interactions 1993: 6: 699-706.
21. Koncz C, Schell J. The promoterTl-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium vector. Mol. Gen. Genet. 1986: 204: 383-396.
22. Van Mullem V, Wery M, De Bolle X, Vandenhaute J. Construction of a set of Saccharomyces cerevisiae vectors designed for recombinational cloning. Yeast 2003: 20: 739-746. PMID: 12794935
23. Zhao M, Morohashi K, Hatlestad G, Grotewold E, Lloyd AM. The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci. Development 2008: 135: 1991-1999. doi: 10.1242/dev.016873 PMID: 18434419
24. Urban P, Mignotte C, Kazmaier M, Delorme F, Pompon D. Cloning, yeast expression, and characterization of the coupling of two distantly related Arabidopsis thaliana NADPH-cytochrome P450 reductases with P450CYP73A5. J. Biol. Chem. 1997: 272: 19176-19186. PMID: 9235908
25. Bilyk A. Thin layer chromatographic separation of beet pigments. J. Food Sci. 1981: 46: 298-299.
26. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012: 28: 1647-1649. doi: 10.1093/bioinformatics/bts199 PMID: 22543367
27. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 2012: 9: 772.
28. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012: 61: 539-542. doi: 10.1093/sysbio/sys029 PMID: 22357727
29. Xu B, Yang Z. PAMLX: a graphical user interface for PAML. Mol. Biol. EVol. 2013: 30: 2723-2724. doi: 10.1093/molbev/mst179 PMID: 24105918
30. Hatlestad G, Akhavan NA, Sunnadeniya RM, Elam L, Cargile S, Hembd A, et al. The beet Y locus encodes an anthocyanin-MYB-like protein that activates the betalain red pigment pathway. Nature Genetics 2015: 47: 92-96 doi: 10.1038/ng.3163 PMID: 25436858
31. Dohm JC, Minoche AE, Holtgrawe D, Capella-Gutierrez S, Zakrzewski F, Tafer H, et al. The genome of the recently domesticated crop plant sugar beet (Beta vulgaris). Nature 2014: 505: 546-549 doi: 10.1038/nature12817 PMID: 24352233
32. Harris NN, Javellana J, Davies KM, Lewis DH, Jameson PE, Deroles SC, et al. Betalain production is possible in anthocyanin-producing plant species given the presence of DOPA-dioxygenase and L-DOPA. BMC Plant Biology 2012: 12: 34. doi: 10.1186/1471-2229-12-34 PMID: 22409631
33. Gandía-Herrero F, García-Carmona F, Escribano J. Botany: Floral fluorescence effect. Nature 2005: 437: 334. PMID: 16163341
34. Kapadia GJ, Azuine MA, Sridhar R, Okuda Y, Tsuruta A, Ichiishi E, et al. Chemoprevention of DMBA-induced UV-B promoted, NOR-1-induced TPA promoted skin carcinogenesis, and DEN-induced phenobarbital promoted livertumors in mice by extract of beetroot. Pharmacol. Res. 2003: 47: 141-148. PMID: 12543062
35. Stintzing FC, Carle R. Functional properties of anthocyanins and betalains in plants, food, and in human nutrition. Trends in Food Science & Technology 2004: 15: 19-38.
36. Khan MI, Harsha PSCS, Giridhar P, Ravishankar GA. Pigment identification, nutritional composition, bioactivity, and in vitro cancer cell cytotoxicity of Rivina humilis L. berries, potential source of betalains. LWT-Food Sci. Technol. 2012: 47: 315-323.
37. Gandia-Herrero F, Cabanes J, Escribano J, Garcia-Carmona F, Jimenez-Atienzar M. Encapsulation of the most potent antioxidant betalains in edible matrixes as powders of different colors. J. Agric. Food Chem. 2013: 61: 4294-4302. doi: 10.1021/jf400337g PMID: 23521423
38. Brockington SF, Walker RH, Glover BJ, Soltis PS, Soltis DE. Complex pigment evolution in the Caryophyllales. New Phytologist 2011: 190: 854-864. PMID: 21714182