Advanced SearchSearch Tips
Dietary Transformation of Lipid in the Rumen Microbial Ecosystem
facebook(new window)  Pirnt(new window) E-mail(new window) Excel Download
 Title & Authors
Dietary Transformation of Lipid in the Rumen Microbial Ecosystem
Kim, Eun Joong; Huws, Sharon A.; Lee, Michael R.F.; Scollan, Nigel D.;
  PDF(new window)
Dietary lipids are rapidly hydrolysed and biohydrogenated in the rumen resulting in meat and milk characterised by a high content of saturated fatty acids and low polyunsaturated fatty acids (PUFA), which contributes to increases in the risk of diseases including cardiovascular disease and cancer. There has been considerable interest in altering the fatty acid composition of ruminant products with the overall aim of improving the long-term health of consumers. Metabolism of dietary lipids in the rumen (lipolysis and biohydrogenation) is a major critical control point in determining the fatty acid composition of ruminant lipids. Our understanding of the pathways involved and metabolically important intermediates has advanced considerably in recent years. Advances in molecular microbial technology based on 16S rRNA genes have helped to further advance our knowledge of the key organisms responsible for ruminal lipid transformation. Attention has focused on ruminal biohydrogenation of lipids in forages, plant oils and oilseeds, fish oil, marine algae and fat supplements as important dietary strategies which impact on fatty acid composition of ruminant lipids. Forages, such as grass and legumes, are rich in omega-3 PUFA and are a useful natural strategy in improving nutritional value of ruminant products. Specifically this review targets two key areas in relation to forages: i) what is the fate of the lipid-rich plant chloroplast in the rumen and ii) the role of the enzyme polyphenol oxidase in red clover as a natural plant-based protection mechanism of dietary lipids in the rumen. The review also addresses major pathways and micro-organisms involved in lipolysis and biohydrogenation.
Lipid;Biohydrogenation;Rumen;Microbial Ecosystem;Chloroplast;PPO;
 Cited by
The effects of feeding fresh forage and silage on some nutritional attributes of beef: an overview, Journal of Agrobiology, 2011, 28, 1, 1  crossref(new windwow)
, Archives of Animal Nutrition, 2013, 67, 1, 77  crossref(new windwow)
Effect of forage conservation method on ruminal lipid metabolism and microbial ecology in lactating cows fed diets containing a 60:40 forage-to-concentrate ratio, Journal of Dairy Science, 2013, 96, 4, 2428  crossref(new windwow)
Recent developments in lipid metabolism in ruminants – the role of fat in maintaining animal health and performance, Animal Production Science, 2014, 54, 10, 1549  crossref(new windwow)
Lipid fraction of creams collected in the Parmigiano-Reggiano cheese production area in response to extruded linseed supplementation of dairy cows’ diets: GC-FID and FT-MIR evaluation, International Journal of Dairy Technology, 2014, 67, 4, 510  crossref(new windwow)
Quality traits and lipid composition of meat from crossbreed Santa Ines ewes fed diets including crushed crambe, Revista Brasileira de Zootecnia, 2016, 45, 6, 319  crossref(new windwow)
Manipulation of Rumen Microbial Fermentation by Polyphenol Rich Solvent Fractions from Papaya Leaf to Reduce Green-House Gas Methane and Biohydrogenation of C18 PUFA, Journal of Agricultural and Food Chemistry, 2016, 64, 22, 4522  crossref(new windwow)
Temporal Metagenomic and Metabolomic Characterization of Fresh Perennial Ryegrass Degradation by Rumen Bacteria, Frontiers in Microbiology, 2016, 7, 1664-302X  crossref(new windwow)
Effect of Sunflower and Marine Oils on Ruminal Microbiota, In vitro Fermentation and Digesta Fatty Acid Profile, Frontiers in Microbiology, 2017, 8, 1664-302X  crossref(new windwow)
Abde, M., T. Iriki, N. Tobe and H. Shibui. 1981. Sequestration of holotrich protozoa in the reticulo-rumen of cattle. Appl. Environ. Microbiol. 41:758-765

Al-Mabruk, R. M., N. F. G. Beck and R. J. Dewhurst. 2004. Effects of silage species and supplemental vitamin E on the oxidative stability of milk. J. Dairy Sci. 87:406-412 crossref(new window)

Ashes, J. R., B. D. Siebert, S. K. Gulati, A. Z. Cuthbertson and T. W. Scott. 1992. Incorporation of n-3 fatty acids of fish oil into tissue and serum lipids of ruminants. Lipids 27:629-631 crossref(new window)

Atkinson, R. L., E. J. Scholljegerdes, S. L. Lake, V. Nayigihugu, B. W. Hess and D. C. Rule. 2006. Site and extent of digestion, duodenal flow, and intestinal disappearance of total and esterified fatty acids in sheep fed a high-concentrate diet supplemented with high-linoleate safflower oil. J. Anim. Sci. 84:387-396

Bauman, D. E. and A. L. Lock. 2006. Concepts in lipid digestion and metabolism in dairy cows. In: Proceedings of the 2006 Tri-State Dairy Nutrition Conference, Ohio USA. pp. 1-14

Carriquiry, M., W. J. Weber, L. H. Baumgard and B. A. Crooker. 2008. In vitro biohydrogenation of four dietary fats. Anim. Feed Sci. Technol. 141:339-355 crossref(new window)

Collomb, M., U. Butikofer, R. Sieber, B. Jeangros and J. O. Bosset. 2002. Composition of fatty acids in cow's milk fat produced in the lowlands, mountains and highlands of Switzerland using high-resolution gas chromatography. Intl. Dairy J. 12:649-659 crossref(new window)

Counotte, G. H. M., R. A. Prins, R. H. A. M. Janssen and M. J. A. deBie. 1981. The role of Megasphaera elsdenii in the fermentation of D,L-(2-$^{13}C$)-lactate in the rumen of dairy cattle. Appl. Environ. Microbiol. 42:649-655

Dawson, R. M. C. and P. Kemp. 1969. The effect of defaunation on the phospholipids and on the hydrogenation of unsaturated fatty acids in the rumen. Biochem. J. 115:351-352

Devillard, E., F. M. McIntosh, C. J. Newbold and R. J. Wallace. 2006. Rumen ciliate protozoa contain high concentrations of conjugated linoleic acids and vaccenic acid, yet do not hydrogenate linoleic acid or desaturate stearic acid. Br. J. Nutr. 96:697-704

Dewhurst, R. J., K. J. Shingfield, M. R. F. Lee and N. D. Scollan. 2006. Increasing the concentrations of beneficial polyunsaturated fatty acids in milk produced by dairy cows in high-forage systems. Anim. Feed Sci. Technol. 131:168-206 crossref(new window)

Dohme, F., V. Fievez, K. Raes and D. I. Demeyer. 2003. Increasing levels of two different fish oils lower ruminal biohydrogenation of eicosapentaenoic and docosahexaenoic acid in vitro. Anim. Res. 52:309-320 crossref(new window)

Doreau, M. and Y. Chilliard. 1997. Effects of ruminal or postruminal fish oil supplementation on intake and digestion in dairy cows. Reprod. Nutr. Dev. 37:113-124 crossref(new window)

Doreau, M. and A. Ferlay. 1994. Digestion and utilisation of fatty acids by ruminants. Anim. Feed Sci. Technol. 45:379-396 crossref(new window)

Engle, T. E., V. Fellner and J. W. Spears. 2001. Copper status, serum cholesterol, and milk fatty acid profile in Holstein cows fed varying concentrations of copper. J. Dairy Sci. 84:2308-2313 crossref(new window)

Fievez, V., B. Vlaeminck, T. Jenkins, F. Enjalbert and M. Doreau. 2007. Assessing rumen biohydrogenation and its manipulation in vivo, in vitro and in situ. Eur. J. Lipid Sci. Technol. 109:740-756 crossref(new window)

Fotouhi, N. and T. C. Jenkins. 1992. Resistance of fatty acyl amides to degradation and hydrogenation by ruminal microorganisms. J. Dairy Sci. 75:1527-1532 crossref(new window)

Gerson, T., A. John and A. S. D. King. 1985. The effects of dietary starch and fibre on the in vitro rates of lipolysis and hydrogenation by sheep rumen digesta. J. Agric. Sci. (Camb.). 105:27-30 crossref(new window)

Gerson, T., A. John and A. S. D. King. 1986. Effects of feeding ryegrass of varying maturity on the metabolism and composition of lipids in the rumen of sheep. J. Agric. Sci. (Camb.). 106:445-448 crossref(new window)

Gerson, T., A. John and B. R. Sinclair. 1983. The effect of dietary N on in vitro lipolysis and fatty acid hydrogenation in rumen digesta from sheep fed diets high in starch. J. Agric. Sci. (Camb.). 101:97-101 crossref(new window)

Gerson, T., A. S. D. King, K. E. Kelly and W. J. Kelly. 1988. Influence of particle size and surface area on in vitro rates of gas production, lipolysis of triacylglycerol and hydrogenation of linoleic acid by sheep rumen digesta or Ruminococcus flavefaciens. J. Agric. Sci. (Camb.). 110:31-37 crossref(new window)

Girard, V. and J. C. Hawke. 1978. The role of holotrichs in the metabolism of dietary linoleic acid in the rumen. Biochim. Biophys. Acta. 528:17-27 crossref(new window)

Givens, D. I. 2005. The role of animal nutrition in improving the nutritive value of animal-derived foods in relation to chronic disease. Proc. Nutr. Soc. 64:395-402 crossref(new window)

Glasser, F., R. Schmidely, D. Sauvant and M. Doreau. 2008. Digestion of fatty acids in ruminants: a meta-analysis of flows and variation factors: 2. C18 fatty acids. Anim. 2:691-704

Goldfine, H. 1982. Lipids of prokaryotes: structure and distribution. In: Current topics in membranes and transport (Ed. F. Bronner and A. Kleinzeller). Academic Press. New York and London. pp. 1-43

Grabber, J. H. 2008. Mechanical maceration divergently shifts protein degradability in condensed-tannin vs. o-quinone containing conserved forages. Crop Sci. 48:804-813 crossref(new window)

Harfoot, C. G. 1978. Lipid metabolism in the rumen. Prog. Lipid Res. 17:21-54

Harfoot, C. G. and G. P. Hazlewood. 1997. Lipid metabolism in the rumen. In: The Rumen Microbial Ecosystem (Ed. P. N. Hobson and C. S. Stewart). Chapman & Hall. London. pp.382-426

Harfoot, C. G., R. C. Noble and J. H. Moore. 1973. Food particles as a site for biohydrogenation of unsaturated fatty acids in the rumen. Biochem. J. 132:829-832

Hawke, J. C. 1971. The incorporation of long-chain fatty acids into lipids by rumen bacteria and the effect on biohydrogenation. Biochim. Biophys. Acta. 248:167-170 crossref(new window)

Hawke, J. C. 1973. Lipids. In: Chemistry and Biochemistry of Herbage (Ed. U. W. Butler and R. W. Bailey). Academic Press.London. pp. 213-263

Hawke, J. C. and W. R. Silcock. 1970. The in vitro rates of lipolysis and biohydrogenation in rumen contents. Biochim. Biophys. Acta. 218:201-212 crossref(new window)

Hazlewood, G. P. and R. M. C. Dawson. 1975. Isolation and properties of a phospholipids-hydrolyzing bacterium from ovine rumen fluid. J. Gen. Microbiol. 89:163-174 crossref(new window)

Henderson, C. 1973. The effects of fatty acids on pure cultures of rumen bacteria. J. Agric. Sci. (Camb.). 81:107-112 crossref(new window)

Hobson, P. N. and C. S. Stewart. 1997. Lipid metabolism in the rumen. In: The Rumen Microbial Ecosystem (Ed. P. N. Hobson and C. S. Stewart). Blackie Academic and Professional Press. London. pp. 382-419

Hudson, J. A., Y. Cai, R. J. Corner, B. Morvan and K. N. Joblin. 2000. Identification and enumeration of oleic acid and linoleic acid hydrating bacteria in the rumen of sheep and cows. J. Appl. Microbiol. 88:286-292 crossref(new window)

Hudson, J. A., B. Morvan and K. N. Joblin. 1998. Hydration of linoleic acid by bacteria isolated from ruminants. FEMS Microbiol. Lett. 169:277-282 crossref(new window)

Hungate, R. E. 1966. The Rumen and its Microbes. Academic press, London and New York

Hungate, R. E., J. Reichl and R. Prins. 1971. Parameters of fermentation in a continuously fed sheep: evidence of a microbial rumination pool. Appl. Microbiol. 22:1104-1113

Huws, S. A., E. J. Kim, A. H. Kingston-Smith, M. R. F. Lee, S. M. Muetzel, C. J. Newbold, R. J. Wallace and N. D. Scollan. 2009. Rumen protozoa are rich in polyunsaturated fatty acids due to the ingestion of chloroplast. FEMS Microbiol. Ecol. In press crossref(new window)

Huws, S. A., M. R. F. Lee, S. Muetzel, R. J. Wallace and N. D. Scollan. 2006. Effect of forage type and level of fish oil inclusion on bacterial diversity in the rumen. Reprod. Nutr. Dev. 46(Suppl. 1):S99

Igarashi, K. and T. Yasui. 1985. Oxidation of free methionine and methionine residues in protein involved in the browning reaction of phenolic compounds. Agric. Biol. Chem. 49:2309-2315 crossref(new window)

Jenkins, T. C., R. J. Wallace, P. J. Moate and E. E. Mosley. 2008. Board-invited review: Recent advances in biohydrogenation of unsaturated fatty acids within the rumen microbial ecosystem. J. Anim. Sci. 86:397-412 crossref(new window)

Kemp, P. and D. J. Lander. 1984. Hydrogenation in vitro of alphalinolenic acid to stearic acid by mixed cultures of pure strains of rumen bacteria. J. Gen. Microbiol. 130:527-533

Kemp, P., R. W. White and D. J. Lander. 1975. The hydrogenation of unsaturated fatty acids by five bacterial isolates from the sheep rumen, including a new species. J. Gen. Microbiol. 90:100-114 crossref(new window)

Kim, E. J., S. A. Huws, M. R. F. Lee, J. D. Wood, S. M. Muetzel, R. J. Wallace and N. D. Scollan. 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. J. Nutr. 138:889-896

Kim, Y. J., R. H. Liu, J. L. Rychlik and J. B. Russell. 2002. The enrichment of a ruminal bacterium (Megasphaera elsdenii YJ-4) that produces the trans-10, cis-12 isomer of conjugated linoleic acid. J. Appl. Microbiol. 92:976-982 crossref(new window)

Kopecny, J., M. Zorec, J. Mrazek, Y. Kobayashi and R. Marinsek-Logar. 2003. Butyrivibrio hungatei sp nov and Pseudobutyrivibrio xylanivorans sp. nov., butyrate-producing bacteria from the rumen. Int. J. Syst. Evol. Microbiol. 53:201-209 crossref(new window)

Lafontan, M., M. Berlan, V. Stich, F. Crampes, D. Riviere, I. de Glisezinski, C. Sengenes and J. Galitzky. 2002. Recent data on the regulation of lipolysis by catecholamines and natriuretic peptides. Ann. Endocrinol. 63:86-90

Latham, M. J., J. E. Storry and M. E. Sharpe. 1972. Effect of lowroughage diets on the microflora and lipid metabolism in the rumen. Appl. Microbiol. 24:871-877

Lee, M. R. F., J. D. O. Colmenero, A. L. Winters, N. D. Scollan and F. R. Minchin. 2006. 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 crossref(new window)

Lee, M. R. F., P. R. Evans, G. R. Nute, R. I. Richardson and N. D. Scollan. 2009. 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 crossref(new window)

Lee, M. R. F., L. J. Harris, R. J. Dewhurst, R. J. Merry and N. D. Scollan. 2003. The effect of clover silages on long chain fatty acid rumen transformations and digestion in beef steers. Anim. Sci. 76:491-501

Lee, M. R. F., L. J. Parfitt, N. D. Scollan and F. R. Minchin. 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 crossref(new window)

Lee, M. R. F., V. J. Theobald, J. K. S. Tweed, A. L. Winters and N. D. Scollan. 2008a. Effect of feeding fresh or conditioned red clover on milk fatty acids and nitrogen utilization in lactating dairy cows. J. Dairy Sci. doi:10.3168/jds.2008-1692 crossref(new window)

Lee, M. R. F., J. K. S. Tweed, F. R. Minchin and A. L. Winters. 2008b. Red clover polyphenol oxidase: activation, activity and efficacy under grazing. Anim. Feed Sci. Technol. doi:10.1016/j.anifeedsci.2008.06.013 crossref(new window)

Lee, M. R. F., J. K. S. Tweed, N. D. Scollan and M. L. Sullivan. 2008c. Mechanism of polyphenol oxidase action in reducing lipolysis and proteolysis in red clover during batch culture incubation. Proc. Br. Soc. Anim. Sci. p. 31

Lee, M. R. F., J. K. S. Tweed, N. D. Scollan and M. L. Sullivan. 2008d. Ruminal micro-organisms do not adapt to increase utilization of poly-phenol oxidase protected red clover protein and glycerol-based lipid. J. Sci. Food Agric. 88:2479-2485 crossref(new window)

Lee, M. R. F., A. L. Winters, N. D. Scollan, R. J. Dewhurst, M. K. Theodorou and F. R. Minchin. 2004. Plant-mediated lipolysis and proteolysis in red clover with different polyphenol oxidase activities. J. Sci. Food Agric. 84:1639-1645 crossref(new window)

Li, L. and J. C. Steffens. 2002. Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta. 215:239-247 crossref(new window)

Lough, A. K. 1970. Aspects of lipid digestion in the ruminant. In: Physiology of Digestion and Metabolism in the Ruminant (Ed. A. T. Phillipson). Oriel Press. Newcastle upon Tyne, UK. pp. 519-528

Lourenco, M., G. Van Ranst and V. Fievez. 2005. Differences in extent of lipolysis in red or white clover and ryegrass silages in relation to polyphenol oxidase activity. Comm. Agr. Appl. Biol. Sci. 70:169-172

Maia, M. R. G., L. C. Chaudhary, L. Figueres and R. J. Wallace. 2007. Metabolism of polyunsaturated fatty acids and their toxicity to the microflora of the rumen. Antonie Van Leeuwenhoek. 91:303-314 crossref(new window)

Mayer, A. M. 2006. Polyphenol oxidases in plants and fungi: Going places? A review. Phytochem. 67:2318-2331 crossref(new window)

Min, B. R., T. N. Barry, G. T. Attwood and W. C. McNabb. 2003. The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: a review. Anim. Feed Sci. Technol. 106:3-19 crossref(new window)

Moore, B. M. and W. H. Flurkey. 1990. Sodium dodecyl sulphate activation of a plant polyphenoloxidase - effect of sodium dodecyl sulphate on enzymatic and physical characteristics of broad bean polyphenoloxydase. J. Biol. Chem. 265:4982-4988

Moreno, D. A., N. Ilic, A. Poulev, D. L. Brasaemle, S. K. Fried and I. Raskin. 2003. Inhibitory effects of grape seed extract on lipases. Nutr. 19:876-879 crossref(new window)

Murphy, D. J. 1999. Plant lipids - their metabolism, function and utilization. In: Plant Biochemistry and Molecular Biology (Ed. P. J. Lea and R. C. Leegood). John Wiley & Sons. New York. pp. 119-135

Nam, I. S. and P. C. Garnsworthy. 2007. Biohydrogenation of linoleic acid by rumen fungi compared with rumen bacteria. J. Appl. Microbiol. 103:551-556 crossref(new window)

Nozue, M., D. Arakawa, Y. Iwata, H. Shioiri and M. Kojima. 1999. Activation by proteolysis in vivo of 60-kd latent polyphenol oxidases in sweet potato cells in suspension culture. J. Plant Physiol. 155:297-301 crossref(new window)

Or-Rashid, M. M., N. E. Odongo and B. W. McBride. 2007. Fatty acid composition of ruminal bacteria and protozoa, with emphasis on conjugated linoleic acid, vaccenic acid, and odd chain and branched-chain fatty acids. J. Anim. Sci. 85:1228-1234 crossref(new window)

Paillard, D., N. McKain, L. C. Chaudhary, N. D. Walker, F. Pizette, I. Koppova, N. R. McEwan, J. Kopecny, P. E. Vercoe, P. Louis and R. J. Wallace. 2007. Relation between phylogenetic position, lipid metabolism and butyrate production by different Butyrivibrio-like bacteria from the rumen. Antonie Van Leeuwenhoek. 91:417-422 crossref(new window)

Palmquist, D. L., A. L. Lock, K. J. Shingfield and D. E. Bauman. 2005. Biosynthesis of conjugated linoleic acid in ruminants and humans. In: Advances in Food and Nutrition Research (Ed. S. L. Taylor) No. 50. Elsevier Academic Press. San Diego, CA. pp. 179-217

Park, Y., J. Storkson, K. Albright, W. Liu and M. Pariza. 1999. Evidence that the trans-10,cis-12 isomer of conjugated linoleic acid induces body composition changes in mice. Lipids 34:235-241 crossref(new window)

Richardson, R. I., P. Costa, G. R. Nute and N. D. Scollan. 2005. The effect of feeding clover silage on polyunsaturated fatty acid and vitamin E content, sensory, colour and lipid oxidative shelf life of beef loin steaks. In: Proceedings of the 51st international congress of meat science and technology, Exploring the wide world of meat, Baltimore, USA. pp. 1654-1661

Schauff, D. J. and J. H. Clark. 1989. Effects of prilled fatty acids and calcium salts of fatty acids in rumen fermentation, nutrient digestibilities, milk production and milk composition. J. Dairy Sci. 72:917-927 crossref(new window)

Scollan, N., J.-F. Hocquette, K. Nuernberg, D. Dannenberger, I. Richardson and A. Moloney. 2006. Innovations in beef production systems that enhance the nutritional and health value of beef lipids and their relationship with meat quality. Meat Sci. 74:17-33 crossref(new window)

Scollan, N. D., M. S. Dhanoa, N. J. Choi, W. J. Maeng, M. Enser and J. D. Wood. 2001. Biohydrogenation and digestion of long chain fatty acids in steers fed on different sources of lipid. J. Agric. Sci. 136:345-355

Scollan, N. D., M. Enser, S. K. Gulati, I. Richardson and J. D. Wood. 2003. Effects of including a ruminally protected lipid supplement in the diet on the fatty acid composition of beef muscle. Br. J. Nutr. 90:709-716 crossref(new window)

Shi, J., K. Arunasalam, D. Yeung, Y. Kakuda, G. Mittal and Y. M. Jiang. 2004. Saponins from edible legumes: Chemistry, processing, and health benefits. J. Med. Food 7:67-78 crossref(new window)

Shingfield, K. J. and J. M. Griinari. 2007. Role of biohydrogenation intermediates in milk fat depression. Eur. J. Lipid Sci. Technol. 109:799-816 crossref(new window)

Sinclair, L. A. 2007. Nutritional manipulation of sheep of the fatty acid composition neat: a review. J. Agric. Sci. 145:419-434 crossref(new window)

Sinclair, L. A., S. L. Cooper, J. A. Huntington, R. G. Wilkinson, K. G. Hallett, M. Enser and J. D. Wood. 2005. In vitro biohydrogenation of n-3 polyunsaturated fatty acids protected against ruminal microbial metabolism. Anim. Feed Sci. Technol. 124:579-596

Stewart, R. J., B. J. B. Sawyer, C. S. Bucheli and S. P. Robinson. 2001. Polyphenol oxidase is induced by chilling and wounding in pineapple. Aust. J. Plant Physiol. 28:181-191

Sullivan, M. L., R. D. Hatfield, S. L. Thoma and D. A. Samac. 2004. Cloning and characterization of red clover polyphenol oxidase cDNAs and expression of active protein in Escherichia coli and transgenic alfalfa. Plant Physiol. 136:3234-3244 crossref(new window)

Thipyapong, P., J. Melkonian, D. W. Wolfe and J. C. Steffens. 2004. Suppression of polyphenol oxidases increases stress tolerance in tomato. Plant Sci. 167:693-703 crossref(new window)

van de Vossenberg, J. and K. N. Joblin. 2003. Biohydrogenation of C18 unsaturated fatty acids to stearic acid by a strain of Butyrivibrio hungatei from the bovine rumen. Lett. Appl. Microbiol. 37:424-428 crossref(new window)

Van Dorland, H. A., M. Kreuzer, H. Leuenberger and H. R. Wettstein. 2008. Comparative potential of white and red clover to modify the milk fatty acid profile of cows fed ryegrassbased diets from zero-grazing and silage systems. J. Sci. Food Agric. 88:77-85 crossref(new window)

Wachira, A. M., L. A. Sinclair, R. G. Wilkinson, K. Hallett, M. Enser and J. D. Wood. 2000. Rumen biohydrogenation of n-3 polyunsaturated fatty acids and their effects on microbial efficiency and nutrient digestibility in sheep. J. Agric. Sci. 135:419-428 crossref(new window)

Wallace, R. J. 2004. Antimicrobial properties of plant secondary metabolites. Proc. Nutr. Soc. 63:621-629 crossref(new window)

Wallace, R. J., L. C. Chaudhary, N. McKain, N. R. McEwan, A. J. Richardson, P. E. Vercoe, N. D. Walker and D. Paillard. 2006. Clostridium proteoclasticum: a ruminal bacterium that forms stearic acid from linoleic acid. FEMS Microbiol. Lett. 265:195-201 crossref(new window)

Wallace, R. J., N. McKain, K. J. Shingfield and E. Devillard. 2007. Isomers of conjugated linoleic acids are synthesized via different mechanisms in ruminal digesta and bacteria. J. Lipid Res. 48:2247-2254 crossref(new window)

Wang, J. H. and C. P. Constabel. 2004. Polyphenol oxidase overexpression in transgenic Populus enhances resistance to herbivory by forest tent caterpillar (Malacosoma disstria). Planta. 220:87-96 crossref(new window)

Williams, A. G. and C. S. Coleman. 1992. The rumen protozoa. Springer-Verlag, New York

Williams, C. M. 2000. Dietary fatty acids and human health. Ann. Zootech. (Paris). 49:165-180 crossref(new window)

Williams, P. P., J. Gutierrez and R. E. Davis. 1963. Lipid metabolism of rumen ciliates and bacteria. II. Uptake of fatty acids and lipid analysis of Isotrichia intestinalis and rumen bacteria with further information on Entodinium simplex. Appl. Microbiol. 11:260-264

Winters, A. L. and F. R. Minchin. 2001. Red clover and the future for pasture legumes as an alternative protein source for ruminants. In: IGER Innovation No. 5. pp. 30-33

Winters, A. L., F. R. Minchin, T. P. T. Michaelson-Yeates, M. R. F. Lee and P. Morris. 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 crossref(new window)

Wright, D. E. 1959. Hydrogenation of lipids by rumen protozoa. Nature 184:875-876 crossref(new window)