Polyphenol oxidases in Physcomitrella: Functional PPO1 knockout modulates cytokinin-dependent developmentin the moss Physcomitrella patens

Journal of Experimental Botany

Volumn 63, Issue 14, 2012, Pages 5121-5135

  Richter, Hanna ^a,b   Lieberei, Reinhard ^a   Strnad, Miroslav ^c,d   Novák, Ondrej ^c   Gruz, Jiri ^c,d   Rensing, Stefan A ^e   Von Schwartzenberg, Klaus ^a  

^a UNIVERSITY OF HAMBURG   (Germany)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c INSTITUTE OF EXPERIMENTAL BOTANY   (Czech Republic)

^d PALACKÝ UNIVERSITY   (Czech Republic)

^e UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Cytokinins; gene family; gene replacement; knockout; phylogeny; Physcomitrella patens; polyphenol oxidase; PPO

Indexed keywords

CATECHOL OXIDASE; CYTOKININ;

ARTICLE; CHEMISTRY; ENZYMOLOGY; GENE INACTIVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIQUID CHROMATOGRAPHY; METABOLISM; MOSS; MULTIGENE FAMILY; PHYLOGENY; TANDEM MASS SPECTROMETRY;

BRYOPHYTA; CATECHOL OXIDASE; CHROMATOGRAPHY, LIQUID; CYTOKININS; GENE KNOCKOUT TECHNIQUES; MULTIGENE FAMILY; PHYLOGENY; TANDEM MASS SPECTROMETRY;

BRYOPHYTA; PHYSCOMITRELLA; PHYSCOMITRELLA PATENS; SPERMATOPHYTA;

EID: 84865757418     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ers169     Document Type: Article

References (63)

1. Abascal F, Zardoya R, Posada D. 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104-2105.
2. Bollag JM, Shuttleworth KL, Anderson DH. 1988. Laccase-mediated detoxification of phenolic compounds. Applied and Environmental Microbiology 54, 3086-3091.
3. Boudet AM. 2007. Evolution and current status of research in phenolic compounds. Phytochemistry 68, 2722-2735.
4. Bradford M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
5. Chevalier T, Rigal D, Mbéguié-A-Mbéguié D, Gauillard F, Richard-Forget F, Fils-Lycaon B. 1999. Molecular cloning and characterization of apricot fruit polyphenol oxidase. Plant Physiology 11, 1261-1269.
6. Clamp M, Cuff J, Searle SM, Barton GJ. 2004. The Jalview Java alignment editor. Bioinformatics 20, 426-427.
7. Constabel CP, Yip L, Patton JJ, Christopher ME. 2000. Polyphenol oxidase from hybrid poplar. Cloning and expression in response to wounding and herbivory. Plant Physiology 124, 285-295.
8. Demeke T, Morris CF. 2002. Molecular characterization of wheat polyphenol oxidase (PPO). Theoretical and Applied Genetics 104, 813-818.
9. Dry IB, Robinson SP. 1994. Molecular cloning and characterisation of grape berry polyphenol oxidase. Plant Molecular Biology 26, 495-502.
10. Galuszka P, Frébortová J, Luhová L, Bilyeu KD, English JT, Frébort I. 2005. Tissue localization of cytokinin dehydrogenase in maize: possible involvement of quinone species generated from plant phenolics by other enzymatic systems in the catalytic reaction. Plant Cell Physiology 46, 716-728.
11. Gerdemann C, Eicken C, Krebs B. 2002. The crystal structure of catechol oxidase: new insight into the function of type-3 copper proteins. Accounts of Chemical Research 35, 183-191.
12. Gooding PS, Bird C, Robinson SP. 2001. Molecular cloning and characterisation of banana fruit polyphenol oxidase. Planta 213, 748-757.
13. Gruz J, Novák O, Strnad M. 2008. Rapid analysis of phenolic acids in beverages by UPLC-MS/MS. Food Chemistry 111, 789-794.
14. Hahlbrock K, Scheel D. 1989. Physiology and molecular biology of phenylpropanoid metabolism. Annual Review of Plant Physiology and Plant Molecular Biology 40, 347-369.
15. Halaouli S, Record E, Casalot L, Hamdi M, Sigoillot J.-C, Asther M, Lomascolo A. 2006. Cloning and characterization of a tyrosinase gene from the white-rot fungus Pycnoporus sanguineus, and overproduction of the recombinant protein in Aspergillus niger. Applied Microbiology and Biotechnology 70, 580-589.
16. Hohe A, Egener T, Lucht J, Holtorf H, Reinhard C, Schween G, Reski R. 2004. An improved and highly standardised transformation procedure allows efficient production of single and multiple targeted gene knockouts in a moss, Physcomitrella patens. Current Genetics 44, 339-347.
17. Hunt MD, Eannetta NT, Yu H, Newman SM, Steffens JC. 1993. cDNA cloning and expression of potato polyphenol oxidase. Plant Molecular Biology 21, 59-68.
18. Katoh K, Kuma K, Toh H, Miyata T. 2005. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33, 511-518.
19. Klabunde T, Eicken C, Sacchettini JC, Krebs B. 1998. Crystal structure of a plant catechol oxidase containing a dicopper center. Nature Structural Biology 5, 1084-1090.
20. Knight CD, Cove DJ, Boyd PJ, Ashton NW. 1988. The isolation of biochemical and developmental mutants in Physcomitrella patens. In: JM Glime, ed, Methods in Bryology. Nichinan, Miyazaki, Japan: The Hattori Botanical Laboratory, pp 47-58.
21. Lang D, Zimmer AD, Rensing SA, Reski R. 2008. Exploring plant biodiversity: the Physcomitrella genome and beyond. Trends in Plant Science 13, 542-549.
22. Lax AR, Vaughn KC, Templeton GE. 1984. Nuclear inheritance of polyphenol oxidase in Nicotiana. The Journal of Heredity 75, 285-287.
23. Lewis LA. 2007. Chlorophyta on land. Independent lineages of green eukaryotes from arid lands. In: J Seckbach, editor, Algae and cyanobacteria in extreme environments: cellular origin, life in extreme habitats and astrobiology, volume 11, part 6, 569-582. Berlin: Springer.
24. Li Z-H, Wang Q, Ruan X, Pan C-D, Jiang D-A. 2010. Phenolics and plant allelopathy. Molecules 15, 8933-8952.
25. Lieberei R, Biehl B. 1976. Freisetzung und Activierung von Polyphenoloxydasen aus Thylakoid Membranen der Spinat-Chloroplasten. Berichte der Deutschen Botanischen Gesellschaft 89, 663-676.
26. Mayer AM. 2006. Polyphenol oxidases in plants and fungi: going places? A review. Phytochemistry 67, 2318-2331.
27. McCaig BC, Meagher RB, Dean JFD. 2005. Gene structure and molecular analysis of the laccase-like multicopperoxidase (LMCO) gene family in Arabidopsis thaliana. Planta 221, 619-636.
28. Newman SM, Eannetta NT, Yu H, Prince JP, de Vicente MC, Tanksley SD, Steffens JC. 1993. Organisation of the tomato polyphenol oxidase gene family. Plant Molecular Biology 21, 1035-1051.
29. Newman SM, Tantasawat P, Steffens JC. 2011. Tomato polyphenol oxidase B is spatially and temporally regulated during development and in response to ethylene. Molecules 16, 493-517.
30. Novák O, Hauserová E, Amakorová P, Doležal K, Strnad M. 2008. Cytokinin profiling in plant tissues using ultra-performance liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69, 2214-2224.
31. Novák O, Tarkowski P, Tarkowská D, Doležal K, Lenobel R, Strnad M. 2003. Stanoven?cytokininu? v rostlin?h metodou imunoafinitn?chromatografie a kapalinov?chromatografie-hmotnostní spektrometrie. Chemické listy 97, 302.
32. Ono E, Hatayama M, Isono Y, et al. 2006. Localization of a flavonoid biosynthetic polyphenol oxidase in vacuoles. The Plant Journal 45, 133-143.
33. Paszkowski J, Baur M, Bogucki A, Potrykus I. 1988. Gene targeting in plants. The EMBO Journal 7, 4021-4026.
34. Power JB, Chapman JV. 1985. Isolation, culture and genetic manipulation of plant protoplasts. In: RA Dixon, ed, Plant cell culture-a practical approach, Oxford, UK: IRL Press, pp 37-66.
35. Quideau S, Deffieux D, Douat-Casassus C, Pouységu L. 2011. Plant polyphenols: chemical properties, biological activities, and synthesis. Angewandte Chemie International Edition 50, 586-621.
36. Rensing SA, Ick J, Fawcett JA, Lang D, Zimmer A, Van de Peer Y, Reski R. 2007. An ancient genome duplication contributed to the abundance of metabolic genes in the moss Physcomitrella patens. BMC Evolutionary Biology 7, 130.
37. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T et al. 2008. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319, 64-69.
38. Reski R, Reutter K, Karsten B, Faust M, Kruse S, Gorr G, Strepp R, Abel WO. 1995. Molecular analysis of chloroplast division. In: M Terzi, R Cella, A Falavigna, editors, Current issues in plant molecular and cellular biology. Dordrecht, NL: Kluwer Academic Publishers, 291-296.
39. Rice-Evans CA, Miller NJ, Bolwell PG, Bramley PM, Pridham JB. 1995. The relative antioxidant activities of plant-derived polyphenolic flavonoids. Free Radical Research 22, 375-383.
40. Richter H. 2009. Organisation and transcriptional regulation of the polyphenol oxidase (PPO) multigene family of the moss Physcomitrella patens (Hedw.) B.S.G. and functional gene knockout of PpPPO1. PhD thesis, University of Hamburg, Germany, http://ediss.sub. uni-hamburg.de/volltexte/2009/4027/.
41. Richter H, Lieberei R, Schwartzenberg v. K. 2005. Identification and characterisation of a bryophyte polyphenol oxidase encoding gene from Physcomitrella patens. Plant Biology 7, 283-291.
42. Roleda MY., Hanelt D, Kräbs G, Wiencke C. 2004. Morphology, growth, photosynthesis and pigments in Laminaria ochroleuca (Laminariales, Phaeophyta) under ultraviolet radiation. Phycologia 43, 603-613.
43. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574.
44. Schaefer D, Zryd JP. 1997. Efficient gene targeting in the moss Physcomitrella patens. The Plant Journal 11, 1195-1206.
45. Schulz P, Hofmann A, Russo V, Hartmann E, Laloue M, v Schwartzenberg K. 2001. Cytokinin overproducing ove mutants of Physcomitrella show increased riboside to base conversion. Plant Physiology 126, 1224-1231.
46. Schwartzenberg v K, Pethe C, Laloue M. 2003. Cytokinin metabolism in Physcomitrella patens-differences and similarities to higher plants. Plant Growth Regulation 39 99-106.
47. Schwartzenberg v K, Fernández Núñez M, Blaschke H, Dobrev PI, Novák O, Motyka V, Strnad M 2007 Cytokinins in the bryophyte Physcomitrella patens: Analyses of activity, distribution and cytokinin oxidase/dehydrogenase overexpression reveal the role of extracellular cytokinins. Plant Physiology 145 786-800.
48. Selinheimo E, Saloheimo M, Ahola E, Westerholm-Parvinen A, Kalkkinen N, Buchert J, Kruus K. 2006. Production and characterization of a secreted, C-terminally processed tyrosinase from the filamentous fungus Trichoderma reesei. FEBS Journal 273, 4322-4335.
49. Sherman TD, Vaughn KC, Duke SO. 1991. A limited survey of the phylogenetic distribution of polyphenol oxidase. Phytochemistry 30, 2499-2506.
50. Steffens JC, Harel E, Hunt MD. 1994. Polyphenol oxidase. In: BE Ellis, and HA Stafford, editors, Recent advances in phytochemistry, genetic engineering of plant secondary metabolism, vol. 28. New York: Plenum Press, pp 275-312.
51. Sullivan ML, Hatfield RD, Thoma SL, Samac DA. 2004. Cloning and characterisation of red clover polyphenol oxidase cDNAs and expression of active protein in Escherichia coli and transgenic alfalfa. Plant Physiology 136, 3234-3244.
52. Thipyapong P, Joel DM, Steffens JC. 1997. Differential expression and turnover of the tomato polyphenol oxidase gene family during vegetative and reproductive development. Plant Physiology 113, 707-718.
53. Thipyapong P, Melkonian J, Wolfe DW, Steffens JC. 2004. Suppression of polyphenol oxidases increases stress tolerance in tomato. Plant Science 167, 693-703.
54. Thipyapong P, Steffens JC. 1997. Tomato polyphenol oxidase: differential response of the polyphenol oxidase F promoter to injuries and wound signals. Plant Physiology 115, 409-418.
55. Thygesen PW, Dry IB, Robinson SP. 1995. Polyphenol oxidase in potato-a multigene family that exhibits differential expression patterns. Plant Physiology 109, 525-531.
56. Tran LT, Constabel CP. 2011. The polyphenol oxidase gene family in poplar: phylogeny, differential expression and identification of a novel, vacuolar isoform. Planta 234, 799-813.
57. von Schwartzenberg K. 2009. Hormonal regulation by auxin and cytokinin in moss. Annual Plant Reviews 36, 246-281.
58. Wang GD, Li QJ, Luo B, Chen XY. 2004. Ex planta phytoremediation of trichlorophenol and phenolic allelochemicals via an engineered secretory laccase. Nature Biotechnology 22, 893-897.
59. Wang TL, Cove DJ, Beutelmann P, Hartmann E. 1980. Isopentenyladenine from mutants of the moss Physcomitrella patens. Phytochemistry 19, 1103-1105.
60. Waterman PG, Mole S. 1994. Analysis of phenolic plant metabolites. Oxford, UK: Blackwell Scientific Publications.
61. Whelan S, Goldman N. 2001. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Molecular Biology and Evolution 18, 691-699.
62. Wolf L, Rizzini L, Stracke R, Ulm R, Rensing SA. 2010. The molecular and physiological responses of Physcomitrella patens to unltraviolet-B radiation. Plant Physiology 153, 1123-1134.
63. Yoruk R, Marshall MR. 2003. Physicochemical properties and function of plant polyphenol oxidase: a review. Journal of Food Biochemistry 27, 361-422.