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Red clover polyphenol oxidase and lipid metabolism

Published online by Cambridge University Press:  28 October 2010

G. Van Ranst ,
M. R. F. Lee  and
V. Fievez
G. Van Ranst*
Affiliation:
Department of Animal Production, Ghent University, LANUPRO, Proefhoevestraat 10, 9090 Melle, Belgium
M. R. F. Lee
Affiliation:
Institute of Biological, Environmental & Rural Sciences, Aberystwyth University, Aberystwyth SY23 3EB, Ceredigion Wales, UK
V. Fievez
Affiliation:
Department of Animal Production, Ghent University, LANUPRO, Proefhoevestraat 10, 9090 Melle, Belgium
*
†E-mail: Gijs.VanRanst@UGent.be
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Abstract

Increasing the polyunsaturated fatty acid (PUFA) composition of milk is acknowledged to be of benefit to consumer health. Despite the high PUFA content of forages, milk fat contains only about 3% of PUFA and only about 0.5% of n-3 fatty acids. This is mainly due to intensive lipid metabolism in the rumen (lipolysis and biohydrogenation) and during conservation (lipolysis and oxidation) such as drying (hay) and ensiling (silage). In red clover, polyphenol oxidase (PPO) has been suggested to protect lipids against degradation, both in the silage as well as in the rumen, leading to a higher output of PUFA in ruminant products (meat and milk). PPO mediates the oxidation of phenols and diphenols to quinones, which will readily react with nucleophilic binding sites. Such binding sites can be found on proteins, resulting in the formation of protein-bound phenols. This review summarizes the different methods that have been used to assess PPO activity in red clover, and an overview on the current understanding of PPO activity and activation in red clover. Knowledge on these aspects is of major importance to fully harness PPO’s lipid-protecting role. Furthermore, we review the studies that evidence PPO-mediated lipid protection and discuss its possible importance in lab-scale silages and further in an in vitro rumen system. It is demonstrated that high (induction of) PPO activity can lead to lower lipolysis in the silage and lower biohydrogenation in the rumen. There are three hypotheses on its working mechanism: (i) protein-bound phenols could directly bind to enzymes (e.g. lipases) as such inhibiting them; (ii) binding of quinones in and between proteins embedded in a lipid membrane (e.g. in the chloroplast) could lead to encapsulation of the lipids; (iii) direct binding of quinones to nucleophilic sites in polar lipids also could lead to protection. There is no exclusive evidence on which mechanism is most important, although there are strong indications that only lipid encapsulation in protein–phenol complexes would lead to an effective protection of lipids against ruminal biohydrogenation. From several studies it has also become apparent that the degree of PPO activation could influence the mode and degree of protection. In conclusion, this review demonstrates that protein-bound phenols and encapsulation in protein–phenol complexes, induced by PPO-mediated diphenol oxidation, could be of interest when aiming to protect lipids against pre-ruminal and ruminal degradation.

Keywords

red cloverpolyphenol oxidaselipid metabolismrumensilage
Type
Review
Information
animal , Volume 5 , Issue 4 , 23 February 2011 , pp. 512 - 521
Copyright
Copyright © The Animal Consortium 2010

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References

Al-Mabruk, RM, Beck, NFG, Dewhurst, RJ 2004. Effects of silage species and supplemental vitamin E on the oxidative stability of milk. Journal of Dairy Science 87, 406–412.CrossRefGoogle Scholar
Constabel, CP, Ryan, CA 1998. A survey of wound- and methyl jasmonate-induced leaf polyphenol oxidase in crop plants. Phytochemistry 47, 507–511.CrossRefGoogle Scholar
Dewhurst, RJ, Fisher, WJ, Tweed, JKS, Wilkins, RJ 2003a. Comparison of grass and legume silages for milk production. 1. Production responses with different levels of concentrate. Journal of Dairy Science 86, 2598–2611.CrossRefGoogle ScholarPubMed
Dewhurst, RJ, Evans, RT, Scollan, ND, Moorby, JM, Merry, RJ, Wilkins, RJ 2003b. Comparison of grass and legume silages for milk production. 2. In vivo and in sacco evaluations of rumen function. Journal of Dairy Science 86, 2612–2621.CrossRefGoogle ScholarPubMed
Dogan, M, Arslan, O, Dogan, S 2002. Substrate specificity, heat inactivation and inhibition of polyphenol oxidase from different aubergine cultivars. International Journal of Food Science and Technology 37, 415–423.CrossRefGoogle Scholar
Fothergill, M, Rees, ME 2006. Seasonal differences in polyphenol oxidase activity in red clover. In Sward dynamics, N-flows and forage utilisation in legume based systems. Proceedings of the 2nd COST 852 Workshop (ed. M Wachendorf, A Helgadóttir and G Parente), pp. 141–144, Grado, Italy.Google Scholar
Gerdemann, C, Eicken, C, Galla, HJ, Krebs, B 2002. Comparative modeling of the latent form of a plant catechol oxidase using a molluskan hemocyanin structure. Journal of Inorganic Biochemistry 89, 155–158.CrossRefGoogle ScholarPubMed
Gowda, LR, Paul, B 2002. Diphenol activation of the monophenolase and diphenolase activities of field bean (Dolichos lablab) polyphenol oxidase. Journal of Agricultural and Food Chemistry 50, 1608–1614.CrossRefGoogle ScholarPubMed
Grabber, JH 2008. Mechanical maceration divergently shifts protein degradability in condensed-tannin vs. o-quinone containing conserved forages. Crop Science 48, 804–813.CrossRefGoogle Scholar
Huws, SA, Lee, MRF, Muetzel, SM, Scott, MB, Wallace, RJ, Scollan, ND 2010. Forage type and fish oil cause shifts in rumen bacterial diversity. FEMS Microbiology Ecology 73, 396–407.Google ScholarPubMed
Jimenez, M, Garcia-Carmona, F 1996. The effect of sodium dodecyl sulphate on polyphenol oxidase. Phytochemistry 42, 1503–1509.CrossRefGoogle Scholar
Jones, BA, Muck, RE, Hatfield, RD 1995. Red-clover extracts inhibit legume proteolysis. Journal of the Science of Food and Agriculture 67, 329–333.CrossRefGoogle Scholar
Kim, EJ, Huws, SA, Lee, MRF, Wood, JD, Muetzel, SM, Wallace, RJ, Scollan, ND 2008. Fish oil increases the duodenal flow of long chain polyunsaturated fatty acids and trans-11 18 : 1 and decreases 18 : 0 in steers via changes in the rumen bacterial community. Journal of Nutrition 138, 889–896.CrossRefGoogle Scholar
Lee, MRF, Parfitt, LJ, Minchin, FR 2006a. Lipolysis of red clover with differing polyphenol oxidase activities in batch culture. Journal of Animal Science 84 (suppl. 1), 101.Google Scholar
Lee, MRF, Colmenero, JDO, Winters, AL, Scollan, ND, Minchin, FR 2006b. Polyphenol oxidase activity in grass and its effect on plant-mediated lipolysis and proteolysis of Dactylis glomerata (cocksfoot) in a simulated rumen environment. Journal of the Science of Food and Agriculture 86, 1503–1511.CrossRefGoogle Scholar
Lee, MRF, Parfitt, LJ, Scollan, ND, Minchin, FR 2007. Lipolysis in red clover with different polyphenol oxidase activities in the presence and absence of rumen fluid. Journal of the Science of Food and Agriculture 87, 1308–1314.CrossRefGoogle Scholar
Lee, MRF, Tweed, JKS, Scollan, ND, Sullivan, ML 2008a. Ruminal micro-organisms do not adapt to increase utilization of poly-phenol oxidase protected red clover protein and glycerol-based lipid. Journal of the Science of Food and Agriculture 88, 2479–2485.CrossRefGoogle Scholar
Lee, MRF, Scott, MB, Tweed, JKS, Minchin, FR, Davies, DR 2008b. Effects of polyphenol oxidase on lipolysis and proteolysis of red clover silage with and without a silage inoculant (Lactobacillus plantarum L54). Animal Feed Science and Technology 144, 125–136.CrossRefGoogle Scholar
Lee, MRF, Tweed, JKS, Minchin, FR, Winters, AL 2009a. Red clover polyphenol oxidase: activation, activity and efficacy under grazing. Animal Feed Science and Technology 149, 250–264.CrossRefGoogle Scholar
Lee, MRF, Theobald, VJ, Tweed, JKS, Winters, AL, Scollan, ND 2009b. Effect of feeding fresh or conditioned red clover on milk fatty acids and nitrogen utilization in lactating dairy cows. Journal of Dairy Science 92, 1136–1147.CrossRefGoogle ScholarPubMed
Lee, MRF, Tweed, JKS, Cookson, A, Sullivan, ML 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. Journal of the Science of Food and Agriculture 90, 503–510.CrossRefGoogle ScholarPubMed
Lee, MRF, Harris, LJ, Dewhurst, RJ, Merry, RJ, Scollan, ND 2003. The effect of clover silages on long chain fatty acid rumen transformations and digestion in beef steers. Animal Science 76, 491–501.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Li, L, Steffens, JC 2002. Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta 215, 239–247.CrossRefGoogle ScholarPubMed
Loor, JJ, Hoover, WH, Miller-Webster, TK, Herbein, JH, Polan, E 2003. Biohydrogenation of unsaturated fatty acids in continuous culture fermenters during digestion of orchardgrass or red clover with three levels of ground corn supplementation. Journal of Animal Science 81, 1611–1627.CrossRefGoogle ScholarPubMed
Lourenço, M, Van Ranst, G, Vlaeminck, B, De Smet, S, Fievez, V 2008. Influence of different dietary forages on the fatty acid composition of rumen digesta as well as ruminant meat and milk. Animal Feed Science and Technology 145, 418–437.CrossRefGoogle Scholar
Mayer, AM 2006. Polyphenol oxidases in plants and fungi: going places? A review. Phytochemistry 67, 2318–2331.CrossRefGoogle ScholarPubMed
Mayer, AM, Harel, E 1979. Polyphenol oxidases in plants. Phytochemistry 18, 193–215.CrossRefGoogle Scholar
Mazzafera, P, Robinson, SP 2000. Characterization of polyphenol oxidase in coffee. Phytochemistry 55, 285–296.CrossRefGoogle ScholarPubMed
Moore, BM, Flurkey, WH 1990. Sodium dodecyl-sulfate activation of a plant polyphenoloxidase – effect of sodium dodecyl-sulfate on enzymatic and physical characteristics of purified broad bean polyphenoloxidase. Journal of Biological Chemistry 265, 4982–4988.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Polovnikova, MG, Voskresenskaya, OL 2008. Activities of antioxidant system components and polyphenol oxidase in ontogeny of lawn grasses under megapolis conditions. Russian Journal of Plant Physiology 55, 699–705.CrossRefGoogle Scholar
Richter, H, Lieberei, R, von Schwartzenberg, K 2005. Identification and characterisation of a bryophyte polyphenol oxidase encoding gene from Physcomitrella patens. Plant Biology 7, 283–291.CrossRefGoogle ScholarPubMed
Robinson, SP, Dry, IB 1992. Broad bean leaf polyphenol oxidase is a 60-kilodalton protein susceptible to proteolytic cleavage. Plant Physiology 99, 317–323.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Sherman, TD, Le Gardeur, T, Lax, AR 1995. Implications of the phylogenetic distribution of polyphenol oxidase in plants. Enzymatic Browning and Its Prevention 600, 103–119.CrossRefGoogle Scholar
Steinite, I, Gailite, A, Ievinsh, G 2004. Reactive oxygen and ethylene are involved in the regulation of regurgitant-induced responses in bean plants. Journal of Plant Physiology 161, 191–196.CrossRefGoogle ScholarPubMed
Stewart, RJ, Sawyer, BJB, Bucheli, CS, Robinson, SP 2001. Polyphenol oxidase is induced by chilling and wounding in pineapple. Australian Journal of Plant Physiology 28, 181–191.Google Scholar
Sullivan, ML, Hatfield, RD 2006. Polyphenol oxidase and o-diphenols inhibit postharvest proteolysis in red clover and alfalfa. Crop Science 46, 662–670.CrossRefGoogle Scholar
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(1[w]). Plant Physiology 136, 3234–3244.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Van Dorland, HA, Kreuzer, M, Leuenberger, H, Wettstein, HR 2008. Comparative potential of white and red clover to modify the milk fatty acid profile of cows fed ryegrass-based diets from zero-grazing and silage systems. Journal of the Science of Food and Agriculture 88, 77–85.CrossRefGoogle Scholar
Van Ranst, G 2009. Effect of ensiling on fatty acid composition and lipid metabolism in forages and the possible role of polyphenol oxidase. PhD, Ghent University.Google Scholar
Van Ranst, G, De Riek, J, Fievez, V, Van Bockstaele, E 2006a. Effects of components in red clover on plant lipase activity with possible consequences on PUFA-content of dairy products. Communications in Agricultural and Applied Biological Sciences 71, 307–310.Google ScholarPubMed
Van Ranst, G, Lourenço, M, De Riek, J, Fievez, V, Van Bockstaele, E 2006b. Detections of potential selection factors in red clover forages to enhance silage quality with possible consequences on PUFA-content of dairy products. In XXVI EUCARPIA Fodder Crops and Amenity Grasses Section, Perugia, Italy, pp. 87–90.Google Scholar
Van Ranst, G, Fievez, V, De Riek, J, Van Bockstaele, E 2009a. Influence of ensiling forages at different dry matters and silage additives on lipid metabolism and fatty acid composition. Animal Feed Science and Technology 150, 62–74.CrossRefGoogle Scholar
Van Ranst, G, Fievez, V, Vandewalle, M, De Riek, J, Van Bockstaele, E 2009b. Influence of herbage species, cultivar and cutting date on fatty acid composition of herbage and lipid metabolism during ensiling. Grass and Forage Science 64, 196–207.CrossRefGoogle Scholar
Van Ranst, G, Fievez, V, Vandewalle, M, De Riek, J, Van Bockstaele, E 2009c. In vitro study of red clover polyphenol oxidase activity, activation, and effect on measured lipase activity and lipolysis. Journal of Agricultural and Food Chemistry 57, 6611–6617.CrossRefGoogle ScholarPubMed
Van Ranst, G, Fievez, V, Vandewalle, M, Van Waes, C, De Riek, J, Van Bockstaele, E 2010. Influence of damaging and wilting red clover on lipid metabolism during ensiling and in vitro rumen incubation. Animal 4, 1528–1540.CrossRefGoogle ScholarPubMed
Vanhatalo, A, Kuoppala, K, Toivonen, V, Shingfield, KJ 2007. Effects of forage species and stage of maturity on bovine milk fatty acid composition. European Journal of Lipid Science and Technology 109, 856–867.CrossRefGoogle Scholar
Veltman, RH, Larrigaudiere, C, Wichers, HJ, Van Schaik, ACR, Van der Plas, LHW, Oosterhaven, J 1999. PPO activity and polyphenol content are not limiting factors during brown cove development in pears (Pyrus communis L-cv. conference). Journal of Plant Physiology 154, 697–702.CrossRefGoogle Scholar
Winters, AL, Minchin, FR, Morris, P 2005. Substrate-dependent activation of polyphenol oxidase in red clover. XX International Grassland Congress, Dublin, Ireland.Google Scholar
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.CrossRefGoogle Scholar
Winters, A, Heywood, S, Farrar, K, Donnison, I, Thomas, A, Webb, KJ 2009. Identification of an extensive gene cluster among a family of PPOs in Trifolium pratense L. (red clover) using a large insert BAC library. BMC Plant Biology 9, 94.CrossRefGoogle ScholarPubMed
Yoruk, R, Marshall, MR 2003. Physicochemical properties and function of plant polyphenol oxidase: a review. Journal of Food Biochemistry 27, 361–422.CrossRefGoogle Scholar