Forage polyphenol oxidase and ruminant livestock nutrition

Frontiers in Plant Science

Volumn 5, Issue DEC, 2014, Pages

  Lee, Michael R F ^a,b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b ROTHAMSTED RESEARCH   (United Kingdom)

Author keywords

Biohydrogenation; Lipolysis; Polyphenol oxidase; Proteolysis; Rumen

Indexed keywords

ANIMALIA; TRIFOLIUM PRATENSE;

EID: 84917678987     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00694     Document Type: Review

References (70)

1. Albrecht, K. A., and Muck, R. E. (1991). Proteolysis in ensiled forage legumes that vary in tannin concentration.Crop Sci. 31, 464-469. doi: 10.2135/cropsci1991.0011183X003100020048x
2. Anderson, J. V., and Morris, C. F. (2001). An improved whole-seed assay for screening wheat germplasm for polyphenol oxidase activity. Crop Sci. 41, 1697-1705. doi: 10.2135/cropsci2001.1697
3. Aufrère, J., Graviou, D., and Demarquilly, C. (2003). Ruminal degradation of protein of cocksfoot and perennial ryegrass as affected by various stages of growth and conservation methods. Anim. Res. 52, 245-261. doi: 10.1051/animres:2003021
4. Bertilsson, J., and Murphy, M. (2003). Effects of feeding clover silages on feed intake, milk production and digestion in dairy cows. Grass Forage Sci. 58, 309-322. doi: 10.1046/j.1365-2494.2003.00383.x
5. Bittner, S. (2006). When quinones meet amino acids: chemical, physical and biological consequences. Amino Acids30, 205-224. doi: 10.1007/s00726-005-0298-2
6. Broderick, G. A., Brito, A. F., and Olmos Colmenero, J. J. (2007). Effects of feeding formate-treated alfalfa silage or red clover silage on the production of lactating dairy cows. J. Dairy Sci. 90, 1378-1391. doi: 10.3168/jds.S0022-0302(07)71624-7
7. Broderick, G. A., Walgenbach, R. P., and Maignan, S. (2001). Production of lactating dairy cows fed alfalfa or red clover silage at equal dry matter or crude protein contents in the diet. J. Dairy Sci. 84, 1728-1737. doi: 10.3168/jds.S0022-0302(01)74608-5
8. Broderick, G. A., Walgenbcah, R. P., and Sterrenburg, E. (2000). Performance of lactating dairy cows fed alfalfa or red clover silage as the sole forage. J. Dairy Sci. 83, 1543-1551. doi: 10.3168/jds.S0022-0302(00)75026-0
9. Buccioni, A., Decandia, M., Minieri, S., Molle, G., and Cabiddu, A. (2012). Lipid metabolism in the rumen: new insights on lipolysis with an emphasis on the role of endogenous plant factors. Anim. Feed Sci. Technol. 174, 1-25. doi: 10.1016/j.anifeedsci.2012.02.009
10. Cabiddu, A., Lee, M. R. F., Decandia, M., Molle, G., Salis, L., Vargiu, M.,et al. (2014). Characterization of polyphenol oxidase (PPO) activity in a range of forage ecotypes with different phenol substrates. A new insight for PPO and protein bound phenol evaluation. Grass Forage Sci. 69, 678-692. doi: 10.1111/gfs.12082
11. Coblentz, W. K., Fritz, J. O., Fick, W. H., Cochran, R. C., and Shirley, J. E. (1998). In situ dry matter, nitrogen and fiber degradation of alfalfa, red clover and Eastern gamagrass at four maturities. J. Dairy Sci. 81, 150-161. doi: 10.3168/jds.S0022-0302(98)75562-6
12. Constabel, C. P., and Ryan, C. A. (1998). A survey of wound- and methyl jasmonate-induced leaf polyphenol oxidase in crop plants. Phytochemistry 47, 507-511. doi: 10.1016/S0031-9422(97)00539-6
13. Czerkawski, J. W. (1969). Methane production in ruminants and its significance. World Rev. Nutr. Diet. 11, 240-282.
14. Dewhurst, R. J., Fisher, W. J., Tweed, J. K. S., and Wilkins, R. J. (2003). Comparison of grass and legume silages for milk production. 1. Production responses with different levels of concentrate. J. Dairy Sci. 86, 2598-2611. doi: 10.3168/jds.S0022-0302(03)73855-7
15. Dogan, M., Arslan, O., and Dogan, S. (2002). Substrate specificity, heat inactivation and inhibition of polyphenol oxidase from different aubergine cultivars. Int. J. Food Sci. Technol. 37, 415-423. doi: 10.1046/j.1365-2621.2002.00580.x
16. Doreau, M., and Ferlay, A. (1994). Digestion and utilisation of fatty acids by ruminants. Anim. Feed Sci. Technol.45, 379-396. doi: 10.1016/0377-8401(94)90039-6
17. Felton, G. W., Donato, K., Del Vecchio, R. J., and Duffy, S. S. (1989). Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. J. Chem. Ecol. 15, 2667-2694. doi: 10.1007/BF01014725
18. Gomez, P. A., Geysen, S., Verlinden, B. E., Artes, F., and Nicolai, B. M. (2006). Modelling the effect of superatmospheric oxygen concentrations on in vitro mushroom PPO activity. J. Sci. Food Agric. 86, 2387-2394. doi: 10.1002/jsfa.2629
19. Gowda, L. R., and Paul, B. (2002). Diphenol activation of the monophenolase and diphenolase activities of field bean (Dolichos lablab) polyphenol oxidase. J. Agric. Food Chem. 50, 1608-1614. doi: 10.1021/jf010913s
20. Halmemies-Beauchet-Filleau, A., Vanhatalo, A., Toivonen, V., Heikkilä, T., Lee, M. R. F., and Shingfield, K. J. (2013). Effect of replacing grass silage with red clover silage on ruminal lipid metabolism in lactating cows fed diets containing 60:40 forage-to-concentrate ratio. J. Dairy Sci. 96, 5885-5900. doi: 10.3168/jds.2013-6872
21. Halmemies-Beauchet-Filleau, A., Vanhatalo, A., Toivonen, V., Heikkilä, T., Lee, M. R. F., and Shingfield, K. J. (2014). Effect of replacing grass silage with red clover silage on nutrient digestion, nitrogen metabolism and milk fatty acid composition in lactating cows fed diets containing 60:40 forage-to-concentrate ratio. J. Dairy Sci. 97, 3761-3776. doi: 10.3168/jds.2013-7358
22. Harfoot, C. G., and Hazlewood, G. P. (1997) "Lipid metabolism in the rumen," in The Rumen Microbial Ecosystem, eds P. N. Hobson and C. S. Stewart (London: Chapman & Hall), 382-426. doi: 10.1007/978-94-009-1453-7_9
23. Harpaz, I., and Klein, M. (1964). Polyphenol oxidase activity in healthy maize plants and in those infected by the maize rough dwarf virus (MRDV). Experientia 20, 274-275. doi: 10.1007/BF02151803
24. Hoffman, P. C., Combs, D. K., Brehm, N. M., and Welch, D. A. (1997). Performance of lactating dairy cows fed red clover or alfalfa silage. J. Dairy Sci. 80, 3308-3315. doi: 10.3168/jds.S0022-0302(97)76306-9
25. Huws, S. A., Lee, M. R. F., Muetzel, S. M., Scott, M. B., and Wallace, R. J. (2010). Forage type and fish oil causes shifts in rumen bacterial diversity. FEMS Microbiol. Ecol. 73, 396-407. doi: 10.1111/j.1574-6941.2010.00892.x
26. Jimenez, M., and Garcia-Carmona, F. (1996). The effect of sodium dodecyl sulphate on polyphenol oxidase.Phytochemistry 42, 1503-1509. doi: 10.1016/0031-9422(96)00175-6
27. Jones, B. A., Muck, R. E., and Hatfield, R. D. (1995). Red-clover extracts inhibit legume proteolysis. J. Sci. Food Agric. 67, 329-333. doi: 10.1002/jsfa.2740670309
28. Lee, M. R. F., Colmenero, J. D. O., Winters, A. L., Scollan, N. D., and Minchin, F. R. (2006a). Polyphenol oxidase activity in grass and its effect on plant-mediated lipolysis and proteolysis of Dactylis glomerata (cocksfoot) in a simulated rumen environment. J. Sci. Food Agric. 86, 1503-1511. doi: 10.1002/jsfa.2533
29. Lee, M. R. F., Dewhurst, R. J., and Minchin, F. (2006b). The concentration of oxygen and its depletion in bovine grass-boluses. Proc. Br. Soc. Anim. Sci. 181.
30. Lee, M. R. F., Connelly, P. L., Tweed, J. K. S., Dewhurst, R. J., Merry, R. J., and Scollan, N. D. (2006c). Effects of high-sugar ryegrass silage and mixtures with red clover silage on ruminant digestion. 2. Lipids. J. Anim. Sci. 84, 3061-3070. doi: 10.2527/jas.2005-736
31. Lee, M. R. F., Harris, L. J., Dewhurst, R. J., Merry, R. J., and Scollan, N. D. (2003). The effect of clover silages on long chain fatty acid rumen transformations and digestion in beef steers. Anim. Sci. 76, 491-501.
32. Lee, M. R. F., Parfitt, L. J., Scollan, N. D., and Minchin, F. R. (2007). Lipolysis in red clover with different polyphenol oxidase activities in the presence and absence of rumen fluid. J. Sci. Food Agric. 87, 1308-1314. doi: 10.1002/jsfa.2849
33. Lee, M. R. F., Theobald, V. J., Gordon, N., Leyland, M., Tweed, J. K. S., Fychan, R.,et al. (2014). The effect of high polyphenol oxidase grass silage on metabolism of polyunsaturated fatty acids and nitrogen across the rumen of beef steers. J. Anim. Sci. 92, 5076-5087. doi: 10.2527/jas2014-7812
34. Lee, M. R. F., Theobald, V. J., Tweed, J. K. S., Winters, A. L., and Scollan, N. D. (2009a). Effect of feeding fresh or conditioned red clover on milk fatty acids and nitrogen utilization in lactating dairy cows. J. Dairy Sci. 92, 1136-1147. doi: 10.3168/jds.2008-1692
35. Lee, M. R. F., Evans, P. R., Nute, G. R., Richardson, R. I., and Scollan, N. D. (2009b). A comparison between red clover silage and grass silage feeding on fatty acid composition, meat stability and sensory quality of the M. Longissimus muscle of dairy cull cows. Meat Sci. 81, 738-744. doi: 10.1016/j.meatsci.2008.11.016
36. Lee, M. R. F., Tweed, J. K. S., Minchin, F. R., and Winters, A. L. (2009c). Red clover polyphenol oxidase: activation, activity and efficacy under grazing. Anim. Feed Sci. Technol. 149, 250-264. doi: 10.1016/j.anifeedsci.2008.06.013
37. Lee, M. R. F., Tweed, J. K. S., Cookson, A., and Sullivan, M. L. (2010). Immunogold labelling to localize polyphenol oxidase (PPO) during wilting of red clover leaf tissue and the effect of removing cellular matrices on PPO protection of glycerol-based lipid in the rumen. J. Sci. Food Agric. 90, 503-510.
38. Lee, M. R. F., Tweed, J. K. S., and Sullivan, M. L. (2013). Oxidation of ortho-diphenols in red clover with and without polyphenol oxidase (PPO) activity and their role in PPO activation and inactivation. Grass Forage Sci. 68, 83-92. doi: 10.1111/j.1365-2494.2012.00873.x
39. Lee, M. R. F., Winters, A. L., Scollan, N. D., Dewhurst, R. J., Theodorou, M. K., and Minchin, F. R. (2004). Plant-mediated lipolysis and proteolysis in red clover with different polyphenol oxidase activities. J. Sci. Food Agric. 84, 1639-1645. doi: 10.1002/jsfa.1854
40. Li, L., and Steffens, J. C. (2002). Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta 215, 239-247. doi: 10.1007/s00425-002-0750-4
41. Lim, Y. Y., Ginny Lim, T. T., and Liew, L. P. (2005). Autooxidation of some polyphenols in various copper (II) solutions. Malaysian J. Chem. 7, 32-37.
42. Lloyd, D., Ellis, J. E., Hillman, K., and Williams, A. G. (1992). Membrane inlet mass spectrometry: probing the rumen ecosystem. J. Appl. Bacteriol. 73, 155S-163S. doi: 10.1111/j.1365-2672.1992.tb03635.x
43. Marita, J. M., Hatfield, R. D., and Brink, G. (2010). In vitro proteolytic inhibition, polyphenol oxidase activity, and soluble o-diphenols in grasses and cereals. J. Agric. Food Chem. 58, 959-966. doi: 10.1021/jf903555e
44. Mavelli, F., Trotta, M., Ciriaco, F., Agostiano, A., Giotta, L., Italiano, F.,et al. (2014). The binding of quinone to the photosynthetic reaction centers: kinetics and thermodynamics of reactions occurring at the QB-site in zwitterionic and anionic liposomes. Eur. Biophys. J. 43, 301-315. doi: 10.1007/s00249-014-0963-z
45. Mayer, A. M. (2006). Polyphenol oxidases in plants and fungi: going places? A review. Phytochemistry 67, 2318-2331. doi: 10.1016/j.phytochem.2006.08.006
46. Mayer, A. M., and Harel, E. (1979). Polyphenol oxidases in plants. Phytochemistry 18, 193-215. doi: 10.1016/0031-9422(79)80057-6
47. McArthur, J. M., and Miltimore, J. E. (1962). Rumen gas analysis by gas-solid chromatography. Can. J. Anim. Sci.41, 187-196. doi: 10.4141/cjas61-026
48. Merry, R. J., Lee, M. R. F., Davies, D. R., Dewhurst, R. J., Moorby, J. M., Scollan, N. D.,et al. (2006). Effects of high-sugar ryegrass silage and mixtures with red clover silage on ruminant digestion. 1. In vitro and in vivo studies of nitrogen utilization. J. Anim. Sci. 84, 3049-3060. doi: 10.2527/jas.2005-735
49. Miller, A. R., Kelley, T. J., and Mujer, C. V. (1990). Anodic peroxidase isoenzymes and polyphenol oxidase activity from cucumber fruit: tissue and substrate specificity. Phytochemistry 29, 705-709. doi: 10.1016/0031-9422(90)80005-2
50. Moorby, J. M., Lee, M. R. F., Ellis, N. M., Fisher, W. J., Davies, D. R., Kim, E. J.,et al. (2009). Assessment of dietary ratios of red clover and grass silage on milk production and milk quality in dairy cows. J. Dairy Sci. 92, 1148-1160. doi: 10.3168/jds.2008-1771
51. Nicolas, J. J., Richard-Forget, F. C., Goupy, P. M., Amiot, M., and Aubert, S. Y. (1994). Enzymatic browning reactions in apple and apple products. Crit. Rev. Food Sci. Nutr. 34, 109-157. doi: 10.1080/10408399409527653
52. Parveen, I., Threadgill, M. D., Moorby, J. M., and Winters, A. (2010). Oxidative phenols in forage crops containing polyphenol oxidase enzymes. J. Agric. Food Chem. 58, 1371-1382. doi: 10.1021/jf9024294
53. Radler, F., and Torokfalvy, E. (1973). The affinity for oxygen of polyphenoloxidase in grapes. Z. Lebensm. Unters. Forsch. A 152, 38-41. doi: 10.1007/BF01810560
54. Richard-Forget, F. C., and Guillard, F. A. (1997). Oxidation of chlorogenic acid, catechins, and 4-methylcatechol in model solutions by combinations of pear (Pyrus communis Cv. Williams) polyphenol oxidase and peroxidase: a possible involvement of peroxidase in enzymatic browning. J. Agric. Food Chem. 45, 2472-2476. doi: 10.1021/jf970042f
55. Samisch, R. M. (1937). Contribution to the knowledge of plant phenolases. Plant Physiol. 12, 499-508. doi: 10.1104/pp.12.2.499
56. Schmitz, G. E., Sullivan, M. L., and Hatfield, R. D. (2008). Three polyphenol oxidases from red clover (Trifolium pratense) differ in enzymatic activities and activation properties. J. Agric. Food Chem. 56, 272-280. doi: 10.1021/jf072488u
57. Steinite, I., Gailite, A., and Ievinsh, G. (2004). Reactive oxygen and ethylene are involved in the regulation of regurgitant-induced responses in bean plants. J. Plant Physiol. 161, 191-196. doi: 10.1078/0176-1617-01098
58. Stewart, R. J., Sawyer, B. J. B., Bucheli, C. S., and Robinson, S. P. (2001). Polyphenol oxidase is induced by chilling and wounding in pineapple. Aust. J. Plant Physiol. 28, 181-191. doi: 10.1071/PP00094
59. Vamos-Vigyazo, L. (1981). Polyphenol oxidase and peroxidase in fruits and vegetables. Crit. Rev. Food Sci. Nutr.15, 49-127. doi: 10.1080/10408398109527312
60. Van Dorland, H. A., Wettstein, H.-R., Leuenberger, H., and Kreuzer, M. (2006). Comparison of fresh and ensiled white and red clover added to ryegrass on energy and protein utilization of lactating cows. Anim. Sci. 82, 691-700. doi: 10.1079/ASC200685
61. Van Dorland, H. A., Wettstein, H.-R., Leuenberger, H., and Kreuzer, M. (2007). Effect if supplementation of fresh and ensiled clover to ryegrass on nitrogen loss and methane emission of dairy cows. Livestock Sci. 111, 57-69. doi: 10.1016/j.livsci.2006.11.015
62. Vanhatalo, A., Kuoppala, K., Ahvenjärvi, S., and Rinne, M. (2009). Effects of feeding grass or red clover silage cut at two maturity stages in dairy cows. 1. Nitrogen metabolism and supply of amino acids. J. Dairy Sci. 92, 5620-5633. doi: 10.3168/jds.2009-2249
63. Van Ranst, G., Fievez, V., Vandewalle, M., De Riek, J., and Van Bockstaele, E. (2009). In vitro study of red clover polyphenol oxidase activity, activation, and effect on measured lipase activity and lipolysis. J. Agric. Food Chem. 57, 6611-6617. doi: 10.1021/jf900808p
64. Van Ranst, G., Lee, M. R. F., and Fievez, V. (2011). Red clover polyphenol oxidase and lipid metabolism. Animal 5, 512-521. doi: 10.1017/S1751731110002028
65. Veltman, R. H., Larrigaudiere, C., Wichers, H. J., Van Schaik, A. C. R., Van der Plas, L. H. W., and Oosterhaven, J. (1999). PPO activity and polyphenol content are not limiting factors during brown cove development in pears (Pyrus communis L-cv. conference). J. Plant Phys. 154, 697-702. doi: 10.1016/S0176-1617(99)80247-8
66. Winters, A. L., and Minchin, F. R. (2001). Red clover and the future for pasture legumes as an alternative protein source for ruminants. IGER Innov. 5, 30-33.
67. Winters, A. L., and Minchin, F. R. (2005). Modification of the Lowry assay to measure protein and phenols in covalently bonded complexes. Anal. Biochem. 346, 43-48. doi: 10.1016/j.ab.2005.07.041
68. Winters, A. L., Minchin, F. R., Merry, R. J., and Morris, P. (2003). Comparison of polyphenol oxidase activity in red clover and perennial ryegrass. Asp. Appl. Biol. 70, 121-128. doi: 10.1071/AN12183
69. Winters, A. L., Minchin, F. R., Michaelson-Yeates, T. P. T., Lee, M. R. F., and 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. J. Agric. Food Chem. 56, 2817-2824. doi: 10.1021/jf0726177
70. Yoruk, R., and Marshall, M. R. (2003). Physicochemical properties and function of plant polyphenol oxidase: a review. J. Food Biochem. 27, 361-422. doi: 10.1111/j.1745-4514.2003.tb00289.x