Polyphenol oxidase in leaves: Is there any significance to the chloroplastic localization?

Journal of Experimental Botany

Volumn 66, Issue 12, 2015, Pages 3571-3579

  Boeckx, Tinne ^a,b   Winters, Ana L ^a   Webb, K Judith ^a   Kingston Smith, Alison H ^a  

^a ABERYSTWYTH UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Abiotic stress; Photosynthesis; Polyphenol oxidase; Secondary metabolism

Indexed keywords

CATECHOL OXIDASE;

CELL COMPARTMENTALIZATION; CHLOROPLAST; ENVIRONMENT; ENZYMOLOGY; METABOLISM; PHOTOSYNTHESIS; PLANT LEAF;

CATECHOL OXIDASE; CELL COMPARTMENTATION; CHLOROPLASTS; ENVIRONMENT; PHOTOSYNTHESIS; PLANT LEAVES;

EID: 84940676687     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv141     Document Type: Review

References (80)

1. Agati G, Matteini P, Goti A, Tattini M. 2007. Chloroplast-located flavonoids can scavenge singlet oxygen. New Phytologist 174, 77-89.
2. Apel K, Hirt H. 2004. Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annual Review of Plant Biology 55, 373-399.
3. Araji S, Grammer TA, Gertzen R, et al. 2014. Novel roles for the polyphenol oxidase enzyme in secondary metabolism and the regulation of cell death in walnut (Juglans regia). Plant Physiology 164, 1191-1203.
4. Arnon DL. 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1-15.
5. Asada K. 1999. The water-water cycle in chloroplasts: scavening of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50, 601-639.
6. Ben-Shalom N, Kahn V, Harel E, Mayer AM. 1977. Olive catechol oxidase: changes during fruit development. Journal of the Science of Food and Agriculture 28, 545-550.
7. Bhattacharjee S. 2005. Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transduction in plants. Current Science 89, 1113-1121.
8. Felton GW, Donato K, Del Vecchio RJ, Duffey SS. 1989. Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. Journal of Chemical Ecology 15, 2667-2694.
9. Flurkey WH, Inlow JK. 2008. Proteolytic processing of polyphenol oxidase from plants and fungi. Journal of Inorganic Biochemistry 102, 2160-2170.
10. Foresight. 2011. The future of food and farming: final project report. London: The Government Office for Science.
11. Fothergill M, Rees ME. 2006. Seasonal differences in polyphenol oxidase activity in red clover. In: Wachendorf M, Helgadottir A, Parente G, eds. Sward dynamics, N-flows and forage utilisation in legume-based systems. Proceedings of COST Workshop, Grado, Italy, 10-12 November 2005, 141-144.
12. Foyer CH, Noctor G. 2012. Managing the cellular redox hub in photosynthetic organisms. Plant, Cell and Environment 35, 199-201.
13. Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J. 2012. Photosynthetic control of electron transport and the regulation of gene expression. Journal of Experimental Biology 63, 1637-1661.
14. 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.
15. Gill SS, Tuteja N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48, 909-930.
16. Griffith GW. 1994. Phenoloxidases. In: Martinelli SD, Kinghorn JR, eds. Progress in industrial microbiology, Vol. 29: Aspergillus nidulans: 50 years on. Amsterdam: Elsevier Science Publishers, 763-788.
17. Grace SC, Logan BA. 2000. Energy dissipation and radical scavenging by the plant phenylpropanoid pathway. Philosophical Transactions of the Royal Society London, Series B 355, 1499-1510.
18. Grant JJ, Loake GJ. 2000. Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiology 124, 21-29.
19. Halliwell B. 1975. Hydroxylation of p-coumaric acid by illuminated chloroplasts: The role of superoxide. European Journal of Biochemistry 55, 355-360.
20. IPCC (Intergovernmental Panel on Climate Change). 2007. Summary for policy makers. In: Field CB, Barros VR, Dokken DJ et al., eds. Climate change 2014: impacts, adaptation and vulnerability. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK and New York: Cambridge University Press, 1-32.
21. Jiménez M, García-Carmona F. 1996. The effect of sodium dodecyl sulphate on polyphenol oxidase. Phytochemistry 42, 1503-1509.
22. Kaintz C, Molitor C, Thill J, Kampatsikas I, Michael C, Halbwirth H, Rompel A. 2014. Cloning and functional expression in E. coli of a polyphenol oxidase transcript from Coreopsis grandiflora involved in aurone formation. FEBS Letters 588, 3417-3426.
23. Keegstra K, Cline K. 1999. Protein import and routing systems of chloroplasts. The Plant Cell 11, 557-570.
24. Kingston-Smith AH, Marshall AH, Moorby JM. 2013. Breeding for genetic improvement of forage plants in relation to increasing animal production with reduced environmental footprint. Animal 7, Supplement 1, 79-88.
25. Kowalski SP, Eannetta NT, Hirzel AT, Steffens JC. 1992. Purification and characterization of polyphenol oxidase from glandular trichomes of Solanum berthaultii. Plant Physiology 100, 677-684.
26. Kroll J, Rawel HM. 2001. Reactions of plant phenols with myoglobin: influence of chemical structure of the phenolic compounds. The Journal of Food Science 66, 48-58.
27. Kroll J, Rawel HM, Seidelmann N. 2000. Physicochemical properties and susceptibility to proteolytic digestion of myoglobin-phenol derivatives Journal of Agricultural and Food Chemistry 48, 1580-1587.
28. Lax AR, Vaughn KC. 1991. Colocalization of polyphenol oxidase and photosystem II proteins. Plant Physiology 96, 26-31.
29. Lee B, Kim K, Jung W, Avice J, Ourry A, Kim T. 2007. Peroxidases and lignifications in relation to the intensity of water-deficit stress in white clover (Trifolium repens L.). Journal of Experimental Botany 58, 1271-1279.
30. Lee MRF, Winters AL, Scollan ND, Dewhurst RJ, Theodorou MK, Minchin FR. 2004. Plant-mediated lipolysis and proteolysis in red clover with different polyphenol oxidase activities. Journal of the Science of Food and Agriculture 84, 1639-1645.
31. Lee MRF, Tweed JKS, Minchin FR, Winters AL. 2009. Red clover polyphenol oxidase: Activation, activity and efficacy under grazing. Animal Feed Science and Technology 149, 250-264.
32. Leufken CM, Moerschbacher BM, Dirks-Hofmeister ME. 2014. Dandelion PPO-1/PPO-2 domain swaps: the C-terminal domain modulates the pH optimum and the linker affects SDS-mediated activation and stability. Biochimica et Biophysica Acta 1854, 178-186.
33. Li L, Steffens JC. 2002. Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta 215, 239-247.
34. Liu Y, Gao L, Xia T, Zhao L. 2009. Investigation of the site-specific accumulation of catechins in the tea plant (Camellia sinensis (L.) O. Kuntze) via vanillin-HCl staining. Journal of Agricultural and Food Chemistry 57, 10371-10376.
35. Marusek CM, Trobaugh NM, Flurkey WH, Inlow JK. 2006. Comparative analysis of polyphenol oxidase from plant and fungal species. Journal of Inorganic Biochemistry 100, 108-123.
36. Martinez VM, Whitaker JR. 1995. The biochemistry and control of enzymatic browning. Trends in Food Science and Technology 6, 195-200.
37. Mayer AM. 2006. Polyphenol oxidases in plants and fungi: going places? A review. Phytochemistry 67, 2318-2331.
38. Mayer AM, Harel E. 1979. Polyphenol oxidases in plants. Phytochemistry 18, 193-215.
39. Meyer HU, Biehl B. 1980. Activities and multiplicity of phenolase from spinach chloroplasts during leaf aging. Phytochemistry 19, 2267-2272.
40. Molitor C, Mauracher S, Kaintz C. 2013. Crystal structures of the latent and in vivo proteolytic activated aurone synthase from Coreopsis lanceolata. In: Konferenzband. 15: Osterreichische Chemietage, Graz, Austria, 23-26 September 2013.
41. Nakayama T, Yonekura-Sakakibara K, Sato T, et al. 2000. Aureusidin synthase: a polyphenol oxidase homolog responsible for flower coloration. Science 290, 1163-1166.
42. Nakayama T, Sato T, Fukui Y, Yonekura-Sakakibara K, Hayashi H, Tanaka Y, Kusumi T, Nishino T. 2001. Specificity analysis and mechanism of aurone synthesis catalyzed by aureusidin synthase, a polyphenol oxidase homolog responsible for flower coloration. FEBS Letters 499, 107-111.
43. Neill SO, Gould KS. 2003. Anthocyanines in leaves: light attenuators or antioxidants? Functional Plant Biology 30, 865-873.
44. Neumann J, Drechsler Z. 1967. Inhibition of photo-induced electron transport and related reactions in isolated chloroplasts by phenol. Plant Physiology 42, 573-577.
45. O'Brien PJ. 1991. Molecular mechanisms of quinone cytotoxicity. Chemico-Biological Interactions 80, 1-41.
46. Ono E, Hatayama M, Isono Y, et al. 2006. Localization of a flavonoid biosynthetic polyphenol oxidase in vacuoles. The Plant Journal 45, 133-143.
47. Parveen I, Threadgill MD, Moorby JM, Winters A. 2010. Oxidative phenols in forage crops containing polyphenol oxidase enzymes. Journal of Agricultural and Food Chemistry 58, 1371-1382.
48. Pietta P. 2000. Flavonoids as antioxidants. Journal of Natural Products 63, 1035-1042.
49. Rivero RM, Ruiz JM, García PC, López-Lefebre L, Sánchez E, Romero L. 2001. Resistance to cold and heat stress: accumulation of phenolic compounds in tomato and watermelon plants. Plant Science 160, 315-321.
50. Rocha AMCN, Morais AMMB. 2001. Characterization of polyphenoloxidase (PPO) extracted from 'Jonagored' apple. Food Control 12, 85-90.
51. Satô M. 1966. Metabolism of phenolic substances by the chloroplasts. II. Conversion by the isolated chloroplasts of p-coumaric acid to caffeic acid. Phytochemistry 5, 385-389.
52. Saunders JA, McClure JW. 1976a. The distribution of flavonoids in chloroplasts of twenty five species of vascular plants. Phytochemistry 15, 809-810.
53. Saunders JA, McClure JW. 1976b. The occurrence of photoregulation of flavonoids in barley plastids. Phytochemistry 15, 805-807.
54. Schmitz GE, Sullivan ML, Hatfield RD. 2008. Three polyphenol oxidases from red clover (Trifolium pratense) differ in enzymatic activities and activation properties. Journal of Agricultural and Food Chemistry 56, 272-280.
55. Sheptovitsky YG, Brudvig GW. 1996. Isolation and characterization of spinach photosystem II membrane-associated catalase and polyphenol oxidase. Biochemistry 35, 16255-16263.
56. Sofo A, Dichio B, Xiloyannis C, Masia A. 2005. Antioxidant defences in olive trees during drought stress: changes in activity of some antioxidant enzymes. Functional Plant Biology 32, 45-53.
57. Solomon EI, Sundaram UM, Machonkin TE. 1996. Multicopper oxidases and oxygenases. Chemical Reviews 96, 2563-2605.
58. Sommer A, Ne'eman E, Steffens JC, Mayer AM, Harel E. 1994. Import, targeting, and processing of a plant polyphenol oxidase. Plant Physiology 105, 1301-1311.
59. Steffens JC, Harel E, Hunt MD. 1994. Polyphenol oxidase. In: Ellis BE, Kuroki GW, Stafford HA, eds. Genetic engineering of plant secondary metabolism. New York: Plenum Publishing Corporation, 275-312.
60. Subramanian N, Venkatesh P, Ganguli S, Sinkar VP. 1999. Role of polyphenol oxidase and peroxidase in the generation of black tea theaflavins. Journal of Agricultural and Food Chemistry 47, 2571-2578.
61. Sullivan ML, Hatfield RD, Thoma SL, Samac DA. 2004. Cloning and characterization of red clover polyphenol oxidase cDNAs and expression of active protein in Escherichia coli and transgenic alfalfa. Plant Physiology 136, 3234-3244.
62. Sullivan ML, Hatfield RD, Samac DA. 2008. Cloning of an alfalfa polyphenol oxidase gene and evaluation of its potential in preventing postharvest protein degradation. Journal of the Science of Food and Chemistry 88, 1406-1414.
63. Sullivan ML, Zarnowski R. 2010. Red clover coumarate 3′-hydroxylase (CYP98A44) is capable of hydroxylating p-coumaryl-shikimate but not p-coumaryl-malate: implications for the biosynthesis of phaselic acid. Planta 231, 319-328.
64. 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
65. Thipyapong P, Hunt MD, Steffens JC. 2004a. Antisense downregulation of polyphenol oxidase results in enhanced disease susceptibility. Planta 220, 105-117.
66. Thipyapong P, Melkonian J, Wolfe DW, Steffens JC. 2004b. Suppression of polyphenol oxidases increases stress tolerance in tomato. Plant Science 167, 693-703.
67. Thipyapong P, Stout MJ, Attajarusit J. 2007. Functional analysis of polyphenol oxidases by antisense/sense technology. Molecules 12, 1569-1595.
68. Tolbert NE. 1973. Activation of polyphenol oxidase of chloroplasts. Plant Physiology 51, 234-244.
69. Tóth SZ, Schansker G, Garab G. 2013. The physiological roles and metabolism of ascorbate in chloroplasts. Physiologia Plantarum 105, 1301-1311.
70. Tran LT, Taylor JS, Constabel CP. 2012. The polyphenol oxidase gene family in land plants: lineage-specific duplication and expansion. BMC Genomics 13, 395.
71. Trebst A, Eck H, Wagner S. 1963. Effects of quinones and oxygen in the electron transport system of chloroplasts. In: National Research Council Committee on Photobiology, ed. Photosynthetic mechanisms of green plants. Washington, US: National Academy of Sciences, publication 1145, 174-194.
72. Trebst A, Depka B. 1995. Polyphenol oxidase and photosynthesis research. Photosynthesis Research 46, 41-44.
73. Vaughn KC, Duke SO. 1984. Function of polyphenol oxidases in higher plants. Physiologia Plantarum 60, 106-112.
74. Veljovic-Jovanonvic S, Kukavica B, Navari-Izzo F. 2008. Characterisation of polyphenol oxidase changes induced by dessication of Ramonda serbica leaves. Physiologia Plantarum 132, 407-416.
75. Vinyard DJ, Ananyev GM, Dismukes GC. 2013. Photosystem II: the reaction center of oxygenic photosynthesis. Annual Review of Biochemistry 82, 577-606.
76. Webb KJ, Cookson A, Allison G, Sullivan M, Winters AL. 2013. Gene expression patterns, localization and substrates of polyphenol oxidase in red clover (Trifolium pratense L.). Journal of Agricultural and Food Chemistry 61, 7421-7430.
77. Webb KJ, Cookson A, Allison G, Sullivan M, Winters AL. 2014. Polyphenol oxidase affects normal nodule development in red clover (Trifolium pratense L.). Frontiers in Plant Science doi: 10.3389/fpls.2014.00700
78. Winters AL, Minchin FR, Merry RJ, Morris P. 2003. Comparison of polyphenol oxidase activity in red clover and perennial ryegrass. In: Abberton MT, Andrews M, Skøt L, Theodorou MK, eds. Aspects 70: Crop quality: its role in sustainable livestock production. Association of Applied Biologists Conference, Manchester, 15-16 December 2003, 121-128.
79. Winters AL, Minchin FR, Michaelson-Yeates TPT, Lee MRF, Morris P. 2008. Latent and active polyphenol oxidase (PPO) in red clover (Trifolium pratense) and use of a low PPO mutant to study the role of PPO in proteolysis reduction. Journal of Agricultural and Food Chemistry 56, 2817-2824.
80. Yoruk R, Marshall MR. 2003. Physicochemical properties and function of plant polyphenol oxidase: a review. Journal of Food Biochemistry 27, 361-422.