Benefits of condensed tannins in forage legumes fed to ruminants: Importance of structure, concentration, and diet composition

Crop Science

Volumn 59, Issue 3, 2019, Pages 861-885

  Mueller Harvey, Irene ^a   Bee, Giuseppe ^b   Dohme Meier, Frigga ^b   Hoste, Hervé ^c   Karonen, Maarit ^d   Kölliker, Roland ^e   Lüscher, Andreas ^f   Niderkorn, Vincent ^g   Pellikaan, Wilbert F ^h   Salminen, Juha Pekka ^d   Skøt, Leif ⁱ   Smith, Lydia M J ^j   Thamsborg, Stig M ^k   Totterdell, Paul ^l   Wilkinson, Ian ^l   Williams, Andrew R ^k   Azuhnwi, Blasius N ^c   Baert, Nicolas ^d   Brinkhaus, Anja Grosse ^b   Copani, Giuseppe ^g   Desrues, Olivier ^k   Drake, Chris ^a   Engström, Marica ^d   Fryganas, Christos ^a   Girard, Marion ^b   Huyen, Nguyen T ^h   Kempf, Katharina ^f   Malisch, Carsten ^f   Mora Ortiz, Marina ^j   Quijada, Jessica ^c   Ramsay, Aina ^a   Ropiak, Honorata M ^a   Waghorn, Garry C ^m   more..

^a UNIVERSITY OF READING   (United Kingdom)

^b Agroscope ALP Liebefeld Posieux   (Switzerland)

^c IHAP   (France)

^d UNIVERSITY OF TURKU   (Finland)

^e ETH ZURICH   (Switzerland)

^f AGROSCOPE RECKENHOLZ TÄNIKON RESEARCH STATION ART   (Switzerland)

^g CEMAGREF   (France)

^h WAGENINGEN UNIVERSITY   (Netherlands)

ⁱ ABERYSTWYTH UNIVERSITY   (United Kingdom)

^j NATIONAL INSTITUTE OF AGRICULTURAL BOTANY   (United Kingdom)

^k UNIVERSITY OF COPENHAGEN   (Denmark)

^l Cotswold Seeds ^*  (United Kingdom)

^m MASSEY UNIVERSITY   (New Zealand)

more..

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85058215391     PISSN: 0011183X     EISSN: 14350653     Source Type: Journal    
DOI: 10.2135/cropsci2017.06.0369     Document Type: Review

References (246)

1. Abeynayake, S.W., S. Panter, R. Chapman, T. Webster, S. Rochfort, A. Mouradov, and G. Spangenberg. 2012. Biosynthesis of proanthocyanidins in white clover flowers: Cross talk within the flavonoid pathway. Plant Physiol. 158:666-678. doi:10.1104/pp.111.189258
2. Agrawal, A.A., A. Hastings, M.T.J. Johnson, J.L. Maron, and J.-P. Salminen. 2012. Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338:113-116.
3. Albert, N.W. 2015. Subspecialization of R2R3-MYB repressors for anthocyanin and proanthocyanidin regulation in forage legumes. Front. Plant Sci. 6:1165. doi:10.3389/fpls.2015.01165
4. Amiri, S., H. Karimmojeni, M.M. Majidi, and A. Boromand. 2013. Evaluation of post-emergence herbicides to control weeds of newly planted sainfoin (Onobrychis sativa). Plant Knowledge J. 2:145-149.
5. Attwood, G., D. Li, D. Pacheco, and M. Tavendale. 2006. Production of indolic compounds by rumen bacteria isolated from grazing ruminants. J. Appl. Microbiol. 100:1261-1271. doi:10.1111/j.1365-2672.2006.02896.x
6. Aufrère, J., M. Dudilieu, D. Andueza, C. Poncet, and R. Baumont. 2013. Mixing sainfoin and lucerne to improve the feed value of legumes fed to sheep by the effect of condensed tannins. Animal 7:82-92. doi:10.1017/S1751731112001097
7. Ayres, J.F., M.J. Blumenthal, L.A. Lane, and J.W. O’Connor. 2006. Birdsfoot trefoil (Lotus corniculatus) and greater lotus (Lotus uliginosus) in perennial pastures in eastern Australia 2. Adaptation and applications of lotus-based pasture. Aust. J. Exp. Agric. 46:521-534. doi:10.1071/EA04242
8. Azuhnwi, B.N., B. Boller, F. Dohme-Meier, H.D. Hess, M. Kreuzer, E. Stringano, and I. Mueller-Harvey. 2013a. Exploring variation in proanthocyanidin composition and content of sainfoin (Onobrychis viciifolia). J. Sci. Food Agric. 93:2102-2109. doi:10.1002/jsfa.6119
9. Azuhnwi, B.N., H. Hertzberg, Y. Arrigo, A. Gutzwiller, H.D. Hess, I. Mueller-Harvey, et al. 2013b. Investigation of sainfoin (Onobrychis viciifolia) cultivar differences on nitrogen balance and fecal egg count in artificially infected lambs. J. Anim. Sci. 91:2343-2354. doi:10.2527/jas.2012-5351
10. Baert, N., W.F. Pellikaan, M. Karonen, and J.-P. Salminen. 2016. A study of the structure-activity relationship of oligomeric ellagitannins on ruminal fermentation in vitro. J. Dairy Sci. 99:8041-8052. doi:10.3168/jds.2016-11069
11. Barbehenn, R.V., and C.P. Constabel. 2011. Tannins in plant-herbivore interactions. Phytochemistry 72:1551-1565. doi:10.1016/j.phytochem.2011.01.040
12. Barrau, E., N. Fabre, I. Fouraste, and H. Hoste. 2005. Effect of bioactive compounds from sainfoin (Onobrychis viciifolia Scop.) on the in vitro larval migration of Haemonchus contortus: Role of tannins and flavonol glycosides. Parasitology 131:531-538. doi:10.1017/S0031182005008024
13. Barry, T.N., T.R. Manley, and S.J. Duncan. 1986. The role of condensed tannins in the nutritional value of Lotus pedunculatus for sheep. 4. Sites of carbohydrate and protein digestion as influenced by dietary reactive tannin concentrations. Br. J. Nutr. 55:123-137. doi:10.1079/BJN19860016
14. Bee, G., P. Silacci, S. Ampuero-Kragten, M. Čandek-Potokar, A.L. Wealleans, J. Litten-Brown, J.-P. Salminem, and I. Mueller-Harvey. 2017. Hydrolysable tannin-based diet rich in gallotannins has a minimal impact on pig performance but significantly reduces salivary and bulbo-urethral gland size. Animal 11:1617-1625. doi:10.1017/S1751731116002597
15. Bhattarai, S., B. Coulman, and B. Biligetu. 2016. Sainfoin (Onobrychis viciifolia Scop.): Renewed interest as a forage legume for western Canada. Can. J. Plant Sci. 96:748-756. doi:10.1139/cjps-2015-0378
16. Berard, N.C., Y. Wang, K.M. Wittenberg, D.O. Krause, B.E. Coulman, T.A. McAllister, and K.H. Ominski. 2011. Condensed tannin concentrations found in vegetative and mature forage legumes grown in western Canada. Can. J. Plant Sci. 91:669-675. doi:10.4141/cjps10153
17. Bermingham, E.N., K.J. Hutchinson, D.K. Revell, I.M. Brookes, and W.C. McNabb. 2001. The effect of condensed tannins in sainfoin (Onobrychis viciifolia) and sulla (Hedysarum coronarium) on the digestion of amino acids in sheep. Proc. N.Z. Soc. Anim. Prod. 61:116-119.
18. Bidel, L.P.R., M. Coumans, Y. Baissae, P. Doumas, and C. Jay-Allemand. 2010. Biological activity of phenolics in plant cells. In: C. Santos-Buelga, M.T. Escribano-Bailon, and V. Lattanzio, editors, Recent advances in polyphenol research. Vol. 2. Blackwell Publishing, Oxford, UK. p. 163-205.
19. Brillouet, J.-M., H. Fulcrand, S. Carrillo, L. Rouméas, and C. Romieu. 2017. Isolation of native proanthocyanidins from grapevine (Vitis vinifera) and other fruits in aqueous buffer. J. Agric. Food Chem. 65:2895-2901. doi:10.1021/acs.jafc.6b05561
20. Brown, R.H., I. Mueller-Harvey, W.E. Zeller, L. Reinhardt, E. Stringano, A. Gea, et al. 2017. Facile purification of milligram to gram quantities of condensed tannins according to mean degree of polymerization and flavan-3-ol subunit composition. J. Agric. Food Chem. 65:8072-8082. doi:10.1021/acs.jafc.7b03489
21. Brunet, S., I. Fourquaux, and H. Hoste. 2011. Ultrastructural changes in the third-stage, infective larvae of ruminant nematodes treated with sainfoin (Onobrychis viciifolia) extract. Parasitol. Int. 60:419-424. doi:10.1016/j.parint.2010.09.011
22. Brunet, S., and H. Hoste. 2006. Monomers of condensed tannins affect the larval exsheathment of parasitic nematodes of ruminants. J. Agric. Food Chem. 54:7481-7487. doi:10.1021/jf0610007
23. Burns, J.C., W.A. Cope, and E.R. Barrick. 1977. Cow and calf performance, per hectare productivity, and persistence of crownvetch under grazing. Agron. J. 69:77-81. doi:10.2134/agronj1977.00021962006900010020x
24. Burns, J.C., R.D. Mochrie, and W.A. Cope. 1972. Responses of dairy heifers to crownvetch, sericea lespedeza, and alfalfa forages. Agron. J. 64:193-195. doi:10.2134/agronj1972.00021962006400020020x
25. Campidonico, L., P.G. Toral, A. Priolo, G. Luciano, B. Valenti, G. Hervás, et al. 2016. Fatty acid composition of ruminal digesta and longissimus muscle from lambs fed silage mixtures including red clover, sainfoin, and timothy. J. Anim. Sci. 94:1550-1560. doi:10.2527/jas.2015-9922
26. Chen, M., D.R. MacGregor, A. Dave, H. Florance, K. Moore, K. Paszkiewicz, et al. 2014. Maternal temperature history activates Flowering Locus T in fruits to control progeny dormancy according to time of year. Proc. Natl. Acad. Sci. USA 111:18787-18792. doi:10.1073/pnas.1412274111
27. Cherry, N.M., M. Bullinger, B.D. Lambert, J.P. Muir, T.W. Whitney, J.E. Miller, and J.T. Sawyer. 2014. Feeding panicled tick-clover to growing goats reduces Haemonchus contortus infection without negative effects on growth. J. Appl. Anim. Nutr. 2:e15. doi:10.1017/jan.2014.9
28. Cheynier, V., G. Bomte, K.M. Davies, V. Lattanzio, and S. Martens. 2013. Plant phenolics: Recent advances on their biosynthesis, genetics and ecophysiology. Plant Physiol. Biochem. 72:1-20. doi:10.1016/j.plaphy.2013.05.009
29. Cheynier, V., F.A. Tomas-Barberan, and K. Yoshida. 2015. Polyphenols: From plants to a variety of food and nonfood uses. J. Agric. Food Chem. 63:7589-7594. doi:10.1021/acs.jafc.5b01173
30. Chezem, W.R., and N.K. Clay. 2016. Regulation of plant secondary metabolism and associated specialized cell development by MYBs and bHLHs. Phytochemistry 131:26-43. doi:10.1016/j.phytochem.2016.08.006
31. Connolly, J., M.-T. Sebastià, L. Kirwan, J.A. Finn, R. Llurba, M. Suter, et al. 2017. Weed suppression greatly increased by plant diversity in intensively managed grasslands: A continental-scale experiment. J. Appl. Ecol. (in press). doi:10.1111/1365-2664.12991
32. Cooper, S.M., N. Owen-Smith, and J.P. Bryant. 1988. Foliage acceptability to browsing ruminants in relation to seasonal changes in the leaf chemistry of woody plants in a South African savanna. Oecologia 75:336-342.
33. Copani, G., V. Niderkorn, F. Anglard, A. Quereuil, and C. Ginane. 2016. Silages containing bioactive forage legumes: A promising protein-rich feed source for growing lambs. Grass Forage Sci. 71:622-631. doi:10.1111/gfs.12225
34. de Koning, C., D. Lloyd, S. Hughes, D. McLachlan, G. Crocker, S. Boschma, and A. Craig. 2003. Solutions for a better environment. In: Proceedings of the 11th Australian Agronomy Conference, Geelong, VIC. 2-6 Feb. 2003. [CD]. Aust. Soc. Agron.
35. de Koning, C., P. Schutz, and J. Howie. 2010. Sulla (Hedysarum coronarium) production sown with cover crops. In: Food security from sustainable agriculture: Proceedings of the 15th Australian Agronomy Conference, Lincoln, New Zealand. Nov. 2010. Aust. Soc. Agron. http://www.regional.org.au/au/asa/2010/pastures-forage/dryland-perennials/6987_dekoningct.htm (accessed 22 Nov 2016).
36. De Vega, J., S. Ayling, M.J. Hegarty, D. Kudrna, J.L. Goicoechea, Å. Ergon, et al. 2015. Red clover (Trifolium pratense L.) draft genome provides a platform for trait improvement. Sci. Rep. 5:17394. doi:10.1038/srep17394
37. Derksen, A., A. Hensel, W. Hafezi, F. Herrmann, T.J. Schmidt, C. Ehrhardt, et al. 2014. 3-O-galloylated procyanidins from Rumex acetosa L. inhibit the attachment of influenza A virus. PLoS One 9:e110089. doi:10.1371/journal.pone.0110089
38. Desrues, O., C. Fryganas, H.M. Ropiak, I. Mueller-Harvey, H.L. Enemark, and S.M. Thamsborg. 2016a. Impact of chemical structure of flavanol monomers and condensed tannins on in vitro anthelmintic activity against bovine nematodes. Parasitology 143:444-454. doi:10.1017/S0031182015001912
39. Desrues, O., I. Mueller-Harvey, W.F. Pellikaan, H.L. Enemark, and S.M. Thamsborg. 2017. Condensed tannins in the gastrointestinal tract of cattle after sainfoin (Onobrychis viciifolia) intake and their possible relationship with anthelmintic effects. J. Agric. Food Chem. 65:1420-1427. doi:10.1021/acs.jafc.6b05830
40. Desrues, O., M. Peña-Espinoza, T.V.A. Hansen, H.L. Enemark, and S.M. Thamsborg. 2016b. Anti-parasitic activity of pelleted sainfoin (Onobrychis viciifolia) against Ostertagia ostertagi and Cooperia oncophora in calves. Parasit. Vectors 9:329. doi:10.1186/s13071-016-1617-z
41. Dobreva, M.A., E. Stringano, R.A. Frazier, R.J. Green, and I. Mueller-Harvey. 2012. Interaction of sainfoin (Onobrychis viciifolia) condensed tannins and proteins. In: V. Lattanzio, N. Mulinacci, P. Pinelli, A. Romani, editors, Proceedings of the 26th International Conference on Polyphenols, Florence, Italy. 23-26 Jul 2012. Stabilimento Grafico Rindi, Prato, Italy. p. 151-152.
42. Döring, T.F., J.A. Baddeley, R. Brown, R. Collins, O. Crowley, S. Cuttle, et al. 2013. Using legume-based mixtures to enhance the nitrogen use efficiency and economic viability of cropping systems. Agric. Hort. Dev. Board. https://www.ruralbusinessschool.org.uk/sites/default/files/attachments/legume_link.pdf (accessed 30 Sept. 2017).
43. Dykes, L., L. Hoffmann, Jr., O. Portillo-Rodriguez, W.L. Rooney, and L.W. Rooney. 2014. Prediction of total phenols, condensed tannins, and 3-deoxyanthocyanidins in sorghum grain using near-infrared (NIR) spectroscopy. J. Cereal Sci. 60:138-142. doi:10.1016/j.jcs.2014.02.002
44. Egan, A.R., and M.J. Ulyatt. 1980. Quantitative digestion of fresh herbage by sheep. VI. Utilization of nitrogen in five herbages. J. Agric. Sci. 94:47-56. doi:10.1017/S002185960002788X
45. Engström, M.T., M. Karonen, J.R. Ahern, N. Baert, B. Payré, H. Hoste, and J.-P. Salminen. 2016. Chemical structures of plant hydrolyzable tannins reveal their in vitro activity against egg hatching and motility of Haemonchus contortus nematodes. J. Agric. Food Chem. 64:840-851. doi:10.1021/acs.jafc.5b05691
46. Engström, M.T., M. Pälijärvi, C. Fryganas, J.H. Grabber, I. Mueller-Harvey, and J.-P. Salminen. 2014. Rapid qualitative and quantitative analyses of proanthocyanidin oligomers and polymers by UPLC-MS/MS. J. Agric. Food Chem. 62:3390-3399. doi:10.1021/jf500745y
47. Escaray, F.J., V. Passeri, F.M. Babuin, F. Marco, P. Carrasco, F. Damiani, et al. 2014. Lotus tenuis × L. corniculatus interspecific hybridization as a means to breed bloat-safe pastures and gain insight into the genetic control of proanthocyanidin biosynthesis in legumes. BMC Plant Biol. 14:40. doi:10.1186/1471-2229-14-40
48. Feliciano, R.P., C.G. Krueger, D. Shanmuganayagam, M.M. Vestling, and J.D. Reed. 2012. Deconvolution of matrix-assisted laser desorption/ionization time-of-flight mass spectrometry isotope patterns to determine ratios of A-type to B-type interflavan bonds in cranberry proanthocyanidins. Food Chem. 135:1485-1493. doi:10.1016/j.foodchem.2012.05.102
49. Ferreyra, M.L.F., S.P. Rius, and P. Casati. 2012. Flavonoids: Biosynthesis, biological functions, and biotechnological applications. Front. Plant Sci. 3:222. doi:10.3389/fpls.2012.00222
50. Feucht, W., D. Treutter, H. Dithmar, and J. Polster. 2013. Loss of nuclear flavanols during drought periods in Taxus baccata. Plant Biol. (Berlin, Ger.) 15:462-470. doi:10.1111/j.1438-8677.2012.00661.x
51. Finn, J.A., L. Kirwan, J. Connolly, M.T. Sebastià, À. Helgadóttir, O.H. Baadshaug, et al. 2013. Ecosystem function enhanced by combining four functional types of plant species in intensively managed grassland mixtures: A 3-year continental-scale field experiment. J. Appl. Ecol. 50:365-375. doi:10.1111/1365-2664.12041
52. Frame, J., J. Charlton, and A. Laidlaw. 1998. Temperate forage legumes. CAB Int., Wallingford, UK.
53. Fryganas, C. 2016. Investigations into the chemical analysis and bioactivity of plant proanthocyanidins to support sustainable livestock farming. Ph.D. diss., Univ. of Reading, UK.
54. Gea, A., E. Stringano, R.H. Brown, and I. Mueller-Harvey. 2011. In situ analysis and structural elucidation of sainfoin (Onobrychis viciifolia) tannins for high throughput germplasm screening. J. Agric. Food Chem. 59:495-503. doi:10.1021/jf103609p
55. Gebrehiwot, L., P.R. Beuselinck, and C.A. Roberts. 2002. Seasonal variations in condensed tannin concentration of three Lotus species. Agron. J. 94:1059-1065. doi:10.2134/agronj2002.1059
56. Girard, M. 2016. Bioactive compounds in forage legumes: Structural changes during conservation, their fate along the digestive tract and their potential to impact ruminant products. Ph.D. diss., ETH Zurich, Zurich, Switzerland.
57. Girard, M., F. Dohme-Meier, P. Silacci, S. Ampuero Kragten, M. Kreuzer, and G. Bee. 2016a. Forage legumes rich in condensed tannins may increase n-3 fatty acid levels and sensory quality of lamb meat. J. Sci. Food Agric. 96:1923-1933. doi:10.1002/jsfa.7298
58. Girard, M., F. Dohme-Meier, D. Wechsler, D. Goy, M. Kreuzer, and G. Bee. 2016b. Ability of 3 tanniferous forage legumes to modify quality of milk and Gruyère-type cheese. J. Dairy Sci. 99:205-220. doi:10.3168/jds.2015-9952
59. Givens, D.I., E. Owen, and A.T. Adesogan. 2000. Current procedures, future requirements and the need for standardisation. In: D.I. Givens, E. Owen, R.F.E. Axford, and H. Omed, editors, Forage evaluation in ruminant nutrition. CABI Publishing, Wallingford, UK. p. 449-474. doi:10.1079/9780851993447.0449
60. Grabber, J., W.E. Zeller, and I. Mueller-Harvey. 2013. Acetone enhances the direct analysis of procyanidin- and prodelphinidin-based condensed tannins in Lotus species by the butanol-HCl-iron assay. J. Agric. Food Chem. 61:2669-2678. doi:10.1021/jf304158m
61. Grabber, J.H., W.K. Coblentz, H. Riday, T.C. Griggs, D.H. Min, J.W. MacAdam, and K.A. Cassida. 2015. Protein and dry-matter degradability of European- and Mediterranean-derived birdsfoot trefoil cultivars grown in the colder continental USA. Crop Sci. 55:1356-1364. doi:10.2135/cropsci2014.09.0659
62. Grabber, J.H., H. Riday, K.A. Cassida, T.C. Griggs, D.H. Min, and J.W. MacAdam. 2014. Yield, morphological characteristics, and chemical composition of European- and Mediterranean-derived birdsfoot trefoil cultivars grown in the colder continental United States. Crop Sci. 54:1893-1901. doi:10.2135/cropsci2013.09.0644
63. Grosse Brinkhaus, A., G. Bee, P. Silacci, M. Kreuzer, and F. Dohme-Meier. 2016. Effect of exchanging Onobrychis viciifolia and Lotus corniculatus for Medicago sativa on ruminal fermentation and nitrogen turnover in dairy cows. J. Dairy Sci. 99:4384-4397. doi:10.3168/jds.2015-9911
64. Grosse Brinkhaus, A., U. Wyss, Y. Arrigo, M. Girard, G. Bee, J.O. Zeitz, et al. 2017. In vitro ruminal fermentation characteristics and utilisable crude protein supply of sainfoin and birdsfoot trefoil silages and their mixtures with other legumes. Animal 11:580-590. doi:10.1017/S1751731116001816
65. Gruber, M., B. Skadhauge, M. Yu, A. Muir, and K. Richards. 2008. Variation in morphology, plant habit, proanthocyanidins, and flavonoids within a Lotus germplasm collection. Can. J. Plant Sci. 88:121-132. doi:10.4141/P06-158
66. Guyot, S., N. Marnet, and J.-F. Drilleau. 2001a. Thiolysis-HPLC characterization of apple procyanidins covering a large range of polymerization states. J. Agric. Food Chem. 49:14-20. doi:10.1021/jf000814z
67. Guyot, S., N. Marnet, P. Sanoner, and J.F. Drilleau. 2001b. Direct thiolysis on crude apple materials for high-performance liquid chromatography characterization and quantification of polyphenols in cider apple tissues and juices. Methods Enzymol. 335:57-70. doi:10.1016/S0076-6879(01)35231-X
68. Hagerman, A.E., and L.G. Butler. 1981. The specificity of proanthocyanidin-protein interactions. J. Biol. Chem. 256:4444-4497.
69. Hammond, K.J., J.L. Burke, J.P. Koolaard, S. Muetzel, C.S. Pinares-Patiño, and G.C. Waghorn. 2013. Effects of feed intake on enteric methane emissions from sheep fed fresh white clover (Trifolium repens) and perennial ryegrass (Lolium perenne) forages. Anim. Feed Sci. Technol. 179:121-132. doi:10.1016/j.anifeedsci.2012.11.004
70. Hancock, K., V. Collette, E. Chapman, K. Hanson, S. Temple, R. Moraga, and J. Caradus. 2014. Progress towards developing bloat-safe legumes for the farming industry. Crop Pasture Sci. 65:1107-1113. doi:10.1071/CP13308
71. Hancock, K.R., V. Collette, K. Fraser, M. Greig, H. Xue, K. Richardson, et al. 2012. Expression of the R2R3-MYB transcription factor TaMYB14 from Trifolium arvense activates proanthocyanidin biosynthesis in the legumes Trifolium repens and Medicago sativa. Plant Physiol. 159:1204-1220. doi:10.1104/pp.112.195420
72. Hansen, T.V.A., C. Fryganas, N. Acevedo, L.R. Carballo, S.M. Thamsborg, I. Mueller-Harvey, and A.R. Williams. 2016. Proanthocyanidins inhibit Ascaris suum glutathione-S-transferase activity and increase susceptibility of larvae to levamisole in vitro. Parasitol. Int. 65:336-339. doi:10.1016/j.parint.2016.04.001
73. Harding, S.A., L.-J. Xue, L. Du, B. Nyamdari, R.L. Lindroth, R. Sykes, et al. 2013. Condensed tannin biosynthesis and polymerization synergistically condition carbon use, defense, sink strength and growth in Populus. Tree Physiol. 34:1240-1251. doi:10.1093/treephys/tpt097
74. Häring, D.A., A. Scharenberg, F. Heckendorn, F. Dohme, A. Lüscher, V. Maurer, et al. 2008. Tanniferous forage plants: Agronomic performance, palatability and efficacy against parasitic nematodes in sheep. Renew. Agric. Food Syst. 23:19-29. doi:10.1017/S1742170507002049
75. Haslam, E. 1981. Vegetable tannins. In: E.E. Conn, editor, The biochemistry of plants. Vol. 7. Academic Press, New York. p. 527-556.
76. Hatew, B., E. Stringano, I. Mueller-Harvey, W.H. Hendriks, C. Hayot Carbonero, L.M.J. Smith, and W.F. Pellikaan. 2016. Impact of variation in structure of condensed tannins from sainfoin (Onobrychis viciifolia) on in vitro ruminal methane production and fermentation characteristics. J. Anim. Physiol. Anim. Nutr. 100:348-360. doi:10.1111/jpn.12336
77. Hayot Carbonero, C. 2011. Sainfoin (Onobrychis viciifolia), a forage legume with great potential for sustainable agriculture, an insight on its morphological, agronomical, cytological and genetic characterisation. Ph.D. diss., Manchester, UK. https://www.escholar.manchester.ac.uk/api/datastream?publicationPid=uk-ac-man-scw:120238&datastreamId=FULL-TEXT.PDF (accessed 18 Nov. 2017).
78. Hayot Carbonero, C., I. Mueller-Harvey, T.A. Brown, and L. Smith. 2011. Sainfoin (Onobrychis viciifolia): A beneficial forage legume. Plant Genet. Resour. 9:70-85. doi:10.1017/S1479262110000328
79. Heckendorn, F., D.A. Häring, V. Maurer, J. Zinsstag, W. Langhans, and H. Hertzberg. 2006. Effect of sainfoin (Onobrychis viciifolia) silage and hay on established populations of Haemonchus contortus and Cooperia curticei in lambs. Vet. Parasitol. 142:293-300. doi:10.1016/j.vetpar.2006.07.014
80. Hellström, J.K., and P.H. Mattila. 2008. HPLC determination of extractable and unextractable proanthocyanidins in plant materials. J. Agric. Food Chem. 56:7617-7624. doi:10.1021/jf801336s
81. Henning, S.M., C. Fajardo-Lira, H.W. Lee, A.A. Youssefian, V.L.W. Go, and D. Heber. 2003. Catechin content of 18 teas and a green tea extract supplement correlates with the antioxidant capacity. Nutr. Cancer 45:226-235. doi:10.1207/S15327914NC4502_13
82. Hernes, P.J., and J.I. Hedges. 2004. Tannin signatures of barks, needles, leaves, cones, and wood at the molecular level. Geochim. Cosmochim. Acta 68:1293-1307. doi:10.1016/j.gca.2003.09.015
83. Heuzé, V., G. Tran, and F. Lebas. 2015. Sulla (Hedysarum coronarium). Feedipedia, a programme by Inst. Natl. Rech. Agron., Ctr. Coop. Int. Rech. Agron. Dév., Assoc. Fran. Zootech., and FAO. http://www.feedipedia.org/node/292 (acccessed 18 Nov. 2017).
84. Hixson, J.L., K.A. Bindon, and P.A. Smith. 2015. Evaluation of direct phloroglucinolysis and colorimetric depolymerization assays and their applicability for determining condensed tannins in grape marc. J. Agric. Food Chem. 63:9954-9962. doi:10.1021/acs.jafc.5b04207
85. Hixson, J.L., J.L. Jacobs, E.N. Wilkes, and P.A. Smith. 2016. Survey of the variation in grape marc condensed tannin composition and concentration and analysis of key compositional factors. J. Agric. Food Chem. 64:7076-7086. doi:10.1021/acs.jafc.6b03126
86. Hoste, H., C. Martinez-Ortiz-De-Montellano, F. Manolaraki, S. Brunet, N. Ojeda-Robertos, I. Fourquaux, et al. 2012. Direct and indirect effects of bioactive tannin-rich tropical and temperate legumes against nematode infections. Vet. Parasitol. 186:18-27. doi:10.1016/j.vetpar.2011.11.042
87. Hoste, H., S. Sotiraki, S.Y. Landau, F. Jackson, and I. Beveridge. 2010. Goat nematode interactions: Think differently! Trends Parasitol. 26:376-381. doi:10.1016/j.pt.2010.04.007
88. Hoste, H., J.F.J. Torres-Acosta, J. Quijada, I. Chan-Perez, M.M. Dakheel, D.S. Kommuru, et al. 2016. Interactions between nutrition and infections with Haemonchus contortus and related gastrointestinal nematodes in small ruminants. In: R.B. Gasser and G. von Samson-Himmelstjerna, editors, Advances in parasitology. Vol. 93. Haemonchus contortus and Haemonchosis: Past, present and future trends. Academic Press, New York. p. 239-351.
89. Hoste, H., J.F.J. Torres-Acosta, C.A. Sandoval-Castro, I. Mueller-Harvey, S. Sotiraki, H. Louvandini, et al. 2015. Tannin containing legumes as a model for nutraceuticals against digestive parasites in livestock. Vet. Parasitol. 212:5-17. doi:10.1016/j.vetpar.2015.06.026
90. Huang, Q.Q., L. Jin, Z. Xu, S. Acharya, T.A. McAllister, T.M. Hu, et al. 2016. Effects of conservation method on condensed tannin content, ruminal degradation, and in vitro intestinal digestion of purple prairie clover (Dalea purpurea Vent.). Can. J. Anim. Sci. 96:524-531. doi:10.1139/cjas-2016-0006
91. Hümmer, A., and P. Schreier. 2008. Analysis of proanthocyanidins. Mol. Nutr. Food Res. 52:1381-1398. doi:10.1002/mnfr.200700463
92. Hunt, S.R., J.W. MacAdam, and T.C. Griggs. 2016. Seeding rate, oat companion crop, and planting season effects on irrigated organic birdsfoot trefoil stands in the mountain West United States. Crop Sci. 56:463-473. doi:10.2135/cropsci2015.04.0240
93. Huyen, N.T. 2016. Sainfoin (Onobrychis viciifolia): A forgotten crop for dairy cows with future potential. Ph.D. diss., Wageningen Univ., Wageningen, the Netherlands.
94. Huyen, N.T., O. Desrues, S.J.J. Alferink, T. Zandstra, M.W.A. Verstegen, W.H. Hendriks, and W.F. Pellikaan. 2016a. Inclusion of sainfoin (Onobrychis viciifolia) silage in dairy cow rations affects nutrient digestibility, nitrogen utilization, energy balance, and methane emissions. J. Dairy Sci. 99:3566-3577. doi:10.3168/jds.2015-10583
95. Huyen, N.T., C. Fryganas, G. Uittenbogaard, I. Mueller-Harvey, M.W.A. Verstegen, W.H. Hendriks, and W.F. Pellikaan. 2016b. Structural features of condensed tannins affect in vitro ruminal methane production and fermentation characteristics. J. Agric. Sci. 154:1474-1487. doi:10.1017/S0021859616000393
96. Huynh-Ba, T., T. Nguyen, G. Philippossian, and A. Vanstraceele. 1994. Anti-urease cosmetic or dermatological composition. US Patent CA2101234 A1. Date issued: 4 February.
97. Irani, S., M.M. Majidi, A. Mirlohi, M. Karami, and M. Zargar. 2015. Response to drought stress in sainfoin: Within and among ecotype variation. Crop Sci. 55:1868-1880. doi:10.2135/cropsci2014.07.0481
98. Jansman, A.J.M. 1993. Tannins in faba beans (Vicia faba L.). Ph.D. diss., Wageningen Univ., Wageningen, the Netherlands.
99. Jones, W.T., and J.L. Mangan. 1977. Complexes of the condensed tannins of sainfoin (Onobrychis viciifolia Scop.) with Fraction 1 leaf protein and with submaxillary mucoprotein, and their reversal by polyethylene glycol and pH. J. Sci. Food Agric. 28:126-136. doi:10.1002/jsfa.2740280204
100. Kariuki, I.W., and B.W. Norton. 2008. The digestion of dietary protein bound by condensed tannins in the gastro-intestinal tract of sheep. Anim. Feed Sci. Technol. 142:197-209. doi:10.1016/j.anifeedsci.2007.08.006
101. Karnezos, T.P., A.G. Matches, and C.P. Brown. 1994. Spring lamb production on alfalfa, sainfoin, and wheatgrass pastures. Agron. J. 86:497-502. doi:10.2134/agronj1994.00021962008600030008x
102. Kempf, K., C.S. Malisch, C. Grieder, F. Widmer, and R. Kölliker. 2017. Marker-trait association analysis for agronomic and compositional traits in sainfoin (Onobrychis viciifolia). Genet. Mol. Res. 16:Gmr16019483. doi:10.4238/gmr16019483
103. Kempf, K., M. Mora-Ortiz, L.M.J. Smith, R. Kölliker, and L. Skøt. 2016. Characterization of novel SSR markers in diverse sainfoin (Onobrychis viciifolia) germplasm. BMC Genet. 17:124. doi:10.1186/s12863-016-0431-0
104. Khanbabaee, K., and T. van Ree. 2001. Tannins: Classification and definition. Nat. Prod. Rep. 18:641-649. doi:10.1039/b101061l
105. Kingston-Smith, A.H., J.E. Edwards, S.A. Huws, E.J. Kim, and M. Abberton. 2010. Plant-based strategies towards minimising ‘livestock’s long shadow’. Proc Nutr. Soc. 69:613-620. doi:10.1017/S0029665110001953
106. Klongsiriwet, C. 2016. Phytochemical analysis of a willow germplasm collection and its pharmacological activities. PhD diss., Univ. of Reading, Reading, UK.
107. Klongsiriwet, C., A. Karp, S. Hanley, R. Barnes, L. Falchero, and I. Mueller-Harvey. 2013. Near infrared spectroscopy (NIRS) for screening condensed tannins in a willow germplasm collection. Planta Med. 79:PJ26. doi:10.1055/s-0033-1352230
108. Klongsiriwet, C., J. Quijada, A.R. Williams, I. Mueller-Harvey, E.M. Williamson, and H. Hoste. 2015. Synergistic inhibition of Haemonchus contortus exsheathment by flavonoid monomers and condensed tannins. Int. J. Parasitol. Drugs Drug Resist. 5:127-134. doi:10.1016/j.ijpddr.2015.06.001
109. Kölliker, R., K. Kempf, C.S. Malisch, and A. Lüscher. 2017. Promising options for improving performance and proanthocyanidins of the forage legume sainfoin (Onobrychis viciifolia Scop.). Euphytica 213:179. doi:10.1007/s10681-017-1965-6
110. Kommuru, D.S., T. Barker, S. Desai, J.M. Burke, A. Ramsay, I. Mueller-Harvey, et al. 2014. Use of pelleted sericea lespedeza (Lespedeza cuneata) for natural control of coccidia and gastrointestinal nematodes in weaned goats. Vet. Parasitol. 204:191-198. doi:10.1016/j.vetpar.2014.04.017
111. Kommuru, D.S., N.C. Whitley, J.E. Miller, J.A. Mosjidis, J.M. Burke, S. Gujja, et al. 2015. Effect of sericea lespedeza leaf meal pellets on adult female Haemonchus contortus in goats. Vet. Parasitol. 207:170-175. doi:10.1016/j.vetpar.2014.11.008
112. Koupai-Abyazani, M.R., J.J. McCallum, A.D. Muir, G.L. Lees, B.A. Bohm, G.H.N. Towers, and M.Y. Gruber. 1993. Purification and characterization of a proanthocyanidin polymer from seed of alfalfa (Medicago sativa Cv. Beaver). J. Agric. Food Chem. 41:565-569. doi:10.1021/jf00028a012
113. Krueger, C.G., J.D. Reed, R.P. Feliciano, and A.B. Howell. 2013. Quantifying and characterizing proanthocyanidins in cranberries in relation to urinary tract health. Anal. Bioanal. Chem. 405:4385-4395. doi:10.1007/s00216-013-6750-3
114. Laaksonen, O.A., J.-P. Salminen, L. Makila, H.P. Kallio, and B. Yang. 2015. Proanthocyanidins and their contribution to sensory attributes of black currant juices. J. Agric. Food Chem. 63:5373-5380. doi:10.1021/acs.jafc.5b01287
115. Landau, S., H. Azaizeh, H. Muklada, T. Glasser, E.D. Ungar, H. Baram, et al. 2010. Anthelmintic activity of Pistacia lentiscus foliage in two Middle Eastern breeds of goats differing in their propensity to consume tannin-rich browse. Vet. Parasitol. 173:280-286. doi:10.1016/j.vetpar.2010.07.006
116. Larkin, P.J., G.J. Tanner, R.G. Joseph, and W.M. Kelman. 1997. Modifying condensed tannin content in plants. In: J.G. Buchanan-Smith, L.D. Bailey, and P. McCaughey, editors, Proceedings of the 18th International Grasslands Congress, Winnipeg, MB, and Saskatoon, SK. 9-18 June 1997. Int. Grassl. Congr., Lexington, KY. p. 167-178. http://www.internationalgrasslands.org/files/igc/publications/1997/iii-167.pdf (accessed 30 Sept. 2017).
117. Lattanzio, V., A. Cardinali, and V. Linsalata. 2012. Plant phenolics: A biochemical and physiological perspective. In: V. Cheynier, P. Sarni-Manchado, and S. Quideau, editors, Recent advances in polyphenol research. Vol. 3. John Wiley & Sons, Chichester, UK. p. 1-39.
118. Lee, L.-S., S.-H. Kim, Y.-B. Kim, and Y.-C. Kim. 2014. Quantitative analysis of major constituents in green tea with different plucking periods and their antioxidant activity. Molecules 19:9173-9186. doi:10.3390/molecules19079173
119. Lehmann, J.R.K., A. Große-Stoltenberg, M. Römer, and J. Oldeland. 2015. Field spectroscopy in the VNIR-SWIR region to discriminate between Mediterranean native plants and exotic-invasive shrubs based on leaf tannin content. Remote Sens. 7:1225-1241. doi:10.3390/rs70201225
120. Li, C., R. Leverence, J.D. Trombley, S. Xu, J. Yang, Y. Tian, et al. 2010. High molecular weight persimmon (Diospyros kaki L.) proanthocyanidin: A highly galloylated, A-linked tannin with an unusual flavonol terminal unit, myricetin. J. Agric. Food Chem. 58:9033-9042. doi:10.1021/jf102552b
121. Li, M., and A.E. Hagerman. 2013. Interactions between plasma proteins and naturally occurring polyphenols. Curr. Drug Metab. 14:432-445. doi:10.2174/1389200211314040006
122. Li, Y., A.D. Iwaasa, Y. Wang, L. Jin, G. Han, and M. Zhao. 2014. Condensed tannins concentration of selected prairie legume forages as affected by phenological stages during two consecutive growth seasons in western Canada. Can. J. Plant Sci. 94:817-826. doi:10.4141/cjps2013-234
123. Liimatainen, J., M. Karonen, and J. Sinkkonen. 2012. Procyanidin xylosides from the bark of Betula pendula. Phytochemistry 76:178-183. doi:10.1016/j.phytochem.2012.01.008
124. Liu, Z., G.P.F. Lane, and W.P. Davies. 2008. Establishment and production of common sainfoin (Onobrychis viciifolia Scop.) in the UK. 2. Effects of direct sowing and undersowing in spring barley on sainfoin and sainfoin-grass mixtures. Grass Forage Sci. 63:242-248. doi:10.1111/j.1365-2494.2008.00629.x
125. Lorenz, M.M., T. Eriksson, and P. Udén. 2010. Effect of wilting, silage additive, PEG treatment and tannin content on the distribution of N fractions after ensiling of three different sainfoin (Onobrychis viciifolia) varieties. Grass Forage Sci. 65:175-184. doi:10.1111/j.1365-2494.2010.00736.x
126. Lüscher, A., I. Mueller-Harvey, J.F. Soussana, R.M. Rees, and J.L. Peyraud. 2014. Potential of legume-based grassland-livestock systems in Europe. Grass Forage Sci. 69:206-228. doi:10.1111/gfs.12124
127. MacAdam, J.W., and J.J. Villalba. 2015. Beneficial effects of temperate forage legumes that contain condensed tannins. Agriculture 5:475-491. doi:10.3390/agriculture5030475
128. MacAdam, J.W., R.E. Ward, T.C. Griggs, B.R. Min, and G.E. Aiken. 2011. Case study: Average daily gain and blood fatty acid composition of cattle grazing the nonbloating legumes birdsfoot trefoil and cicer milkvetch in the Mountain West. Prof. Anim. Sci. 27:574-583. doi:10.15232/S1080-7446(15)30542-8
129. Malisch, C., B. Studer, D. Suter, J.-P. Salminen, and A. Lüscher. 2014. Phenotypic variation among and within thirty accessions of Onobrychis viciifolia examined under climate change scenarios. In: Proceedings of the ASA, CSSA, and SSSA International Annual Meeting, Long Beach, CA. 2-5 Nov. 2014. ASA, CSSA, SSSA, Madison, WI. Paper 125-14. https://scisoc.confex.com/scisoc/2014am/webprogram/Paper88495.html (accessed 18 Nov. 2017).
130. Malisch, C.S., A. Lüscher, N. Baert, M.T. Engström, B. Studer, C. Fryganas, et al. 2015. Large variability of proanthocyanidin content and composition in sainfoin (Onobrychis viciifolia). J. Agric. Food Chem. 63:10234-10242. doi:10.1021/acs.jafc.5b04946
131. Malisch, C.S., J.-P. Salminen, R. Kölliker, M.T. Engström, D. Suter, B. Studer, and A. Lüscher. 2016. Drought effects on proanthocyanidins in sainfoin (Onobrychis viciifolia Scop.) are dependent on the plant’s ontogenetic stage. J. Agric. Food Chem. 64:9307-9316. doi:10.1021/acs.jafc.6b02342
132. Malisch, C.S., D. Suter, B. Studer, and A. Lüscher. 2017. Multifunctional benefits of sainfoin mixtures: Effects of partner species, sowing density and cutting regime. Grass Forage Sci. (in press). doi:10.1111/gfs.12278
133. Manolaraki, F. 2011. Propriétés anthelminthiques du sainfoin (Onobrychis viciifoliae): Analyse des facteurs de variations et du rôle des composés phénoliques impliqués. (In French.) Ph.D. diss., Univ. of Toulouse, Toulouse, France. http://ethesis.inp-toulouse.fr/archive/00001566/01/manolaraki.pdf (accessed 30 Sept. 2017).
134. Martínez-Ortíz-de-Montellano, C., C. Arroyo-López, I. Fourquaux, J.F.J. Torres-Acosta, C.A. Sandoval-Castro, and H. Hoste. 2013. Scanning electron microscopy of Haemonchus contortus exposed to tannin-rich plants under in vivo and in vitro conditions. Exp. Parasitol. 133:281-286. doi:10.1016/j.exppara.2012.11.024
135. Maughan, B., F.D. Provenza, R. Tansawat, C. Maughan, S. Martini, R. Ward, et al. 2014. Importance of grass-legume choices on cattle grazing behavior, performance, and meat characteristics. J. Anim. Sci. 92:2309-2324. doi:10.2527/jas.2013-7297
136. McCaslin, M., P. Reisen, and J. Ho. 2014. New strategies for forage quality improvement in alfalfa. In: Proceedings of the 2014 California Alfalfa, Forage, and Grain Symposium, Long Beach, CA, 10-12 Dec. 2014. Univ. of California Coop. Ext., Plant Sci. Dep., Univ. of California, Davis, CA. http://alfalfa.ucdavis.edu/+symposium/proceedings/2014/14CAS07_McCaslin_AlfalfaImprovement.pdf (accessed 30 Sept. 2017).
137. Meagher, L.P., G. Lane, S. Sivakumaran, M.H. Tavendale, and K. Fraser. 2004. Characterization of condensed tannins from Lotus species by thiolytic degradation and electrospray mass spectrometry. Anim. Feed Sci. Technol. 117:151-163. doi:10.1016/j.anifeedsci.2004.08.007
138. Mechineni, A., D.S. Kommuru, S. Gujja, J.A. Mosjidis, J.E. Miller, J.M. Burke, et al. 2014. Effect of fall-grazed sericea lespedeza (Lespedeza cuneata) on gastrointestinal nematode infections, skin and carcass microbial load, and meat quality of growing goats. Vet. Parasitol. 204:221-228. doi:10.1016/j.vetpar.2014.06.002
139. Mena, P., L. Calani, R. Bruni, and D. Del Rio. 2015. Bioactivation of high-molecular-weight polyphenols by the gut microbiome. In: K.T.D. Rio, editor, Diet-microbe interactions in the gut. Academic Press, San Diego, CA. p. 73-101. doi:10.1016/B978-0-12-407825-3.00006-X
140. Mengistu, G., H. Hoste, M. Karonen, J.-P. Salminen, W.H. Hendriks, and W.F. Pellikaan. 2017. The in vitro anthelmintic properties of browse plant species against Haemonchus contortus is determined by the polyphenol content and composition. Vet. Parasitol. 237:110-116. doi:10.1016/j.vetpar.2016.12.020
141. 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. doi:10.1016/S0377-8401(03)00041-5
142. Minnée, E.M.K., S.L. Woodward, G.C. Waghorn, and P.G. Laboyrie. 2002. The effect of ensiling forage legumes on condensed tannins. Agron. N. Z. 32:117-119.
143. Mora-Ortiz, M. 2015. Pre-breeding, functional genomics and agronomic improvement of the tanniniferous forage crop Onobrychis viciifolia. Ph.D. diss., Univ. of Reading, Reading, UK.
144. Mora-Ortiz, M., and L. Smith. 2016. Sainfoin: Surprising science behind a forgotten forage. Cotswold Grass Seeds, Moreton-in-Marsh, UK.
145. Mora-Ortiz, M., M.T. Swain, M.J. Vickers, M.J. Hegarty, R. Kelly, L.M.J. Smith, and L. Skøt. 2016. De-novo transcriptome assembly for gene identification, analysis, annotation, and molecular marker discovery in Onobrychis viciifolia. BMC Genomics 17:756. doi:10.1186/s12864-016-3083-6
146. Mosjidis, J.A. 2001. Forage legume breeding and evaluation at Auburn University in the last 16 years. In: Proceedings of the 56th Southern Pasture and Forage Crop Improvement Conference, Springdale, AR. 21-22 Apr. 2001. Texas A&M Agrilife Ext., College Station. http://agrilife.org/spfcic/annual-proceedings/56th/forage-legume-breeding-and-evaluation/ (accessed 30 Sept. 2017).
147. Mouradov, A., and G. Spangenberg. 2014. Flavonoids: A metabolic network mediating plants adaptation to their real estate. Front. Plant Sci. 5:620. doi:10.3389/fpls.2014.00620
148. Moyer, J.R., R. Hironaka, G.C. Kozub, and P. Bergen. 1990. Effect of herbicide treatments on dandelion, alfalfa and sainfoin yields and quality. Can. J. Plant Sci. 70:1105-1113. doi:10.4141/cjps90-133
149. Mueller-Harvey, I. 2006. Unravelling the conundrum of tannins in animal nutrition and health. J. Sci. Food Agric. 86:2010-2037.
150. Mueller-Harvey, I., M. Martin-Lorenzo, E. Stringano, R.J. Barnes, J. Oliver, K. Theodoridou, et al. 2011. NIR spectroscopy for predicting the nutritional, anthelmintic and environmental effects of sainf. Proceedings of the 8th International Symposium on the Nutrition of Herbivores (ISNH8), ‘Herbivores in a Changing World’; Aberystwyth, UK, 6-9 Sep 2011. Adv. Anim. Biosci. 2:265.
151. Muir, J.P., T.H. Terrill, J.A. Mosjidis, J.-M. Luginbuhl, J.E. Miller, and J.M. Burke. 2017. Season progression, ontogenesis and environment affect Lespedeza cuneata herbage condensed tannin, fiber and crude protein content. Crop Sci. 57:515-524. doi:10.2135/cropsci2016.07.0605
152. Naumann, H.D., J.P. Muir, B.D. Lambert, L.O. Tedeschi, and M.M. Kothmann. 2013. Condensed tannins in the ruminant environment: A perspective on biological activity. J. Agric. Sci. 1:8-20.
153. Neilson, E.H., J.Q.D. Goodger, I.E. Woodrow, and B. Lindberg Moller. 2013. Plant chemical defense: At what cost? Trends Plant Sci. 18:250-258. doi:10.1016/j.tplants.2013.01.001
154. Niezen, J.H., W.A.G. Charleston, H.A. Robertson, D. Shelton, G.C. Waghorn, and R. Green. 2002. The effect of feeding sulla (Hedysarum coronarium) or lucerne (Medicago sativa) on lamb parasite burdens and development of immunity to gastro intestinal nematodes. Vet. Parasitol. 105:229-245. doi:10.1016/S0304-4017(02)00014-6
155. Niezen, J.H., G.C. Waghorn, and W.A.G. Charleston. 1998a. Establishment and fecundity of Ostertagia circumcincta and Trichostrongylus colubriformis in lambs fed lotus (Lotus pedunculatus) or perennial ryegrass (Lolium perenne). Vet. Parasitol. 78:13-21. doi:10.1016/S0304-4017(98)00121-6
156. Niezen, J.H., T.S. Waghorn, W.A.G. Charleston, and G.C. Waghorn. 1995. Growth and gastrointestinal nematode parasitism in lambs grazing either lucerne (Medicago sativa) or sulla (Hedysarum coronarium) which contains condensed tannins. J. Agric. Sci. 125:281-284. doi:10.1017/S0021859600084422
157. Niezen, J.H., G.C. Waghorn, T.B. Lyons, and D.C. Corson. 1998b. The potential benefits of ensiling the forage legume sulla compared with pasture. Proc. N. Z. Grassl. Assoc. 60:105-109.
158. Nyfeler, D., O. Huguenin-Elie, M. Suter, E. Frossard, J. Connolly, and A. Lüscher. 2009. Strong mixture effects among four species in fertilized agricultural grassland led to persistent and consistent transgressive overyielding. J. Appl. Ecol. 46:683-691. doi:10.1111/j.1365-2664.2009.01653.x
159. Nyfeler, D., O. Huguenin-Elie, M. Suter, E. Frossard, and A. Lüscher. 2011. Grass-legume mixtures can yield more nitrogen than legume pure stands due to mutual stimulation of nitrogen uptake from symbiotic and non-symbiotic sources. Agric. Ecosyst. Environ. 140:155-163. doi:10.1016/j.agee.2010.11.022
160. Pagán-Riestra, S., J.P. Muir, B.D. Lambert, L.O. Tedeschi, and L. Redmon. 2010. Phosphorus and other nutrient disappearance from plants containing condensed tannins using the nylon bag technique. Anim. Feed Sci. Technol. 156:19-25. doi:10.1016/j.anifeedsci.2009.12.006
161. Paolini, V., F. De-La-Farge, F. Prevot, P. Dorchies, and H. Hoste. 2005. Effects of the repeated distribution of sainfoin hay on the resistance and the resilience of goats naturally infected with gastrointestinal nematodes. Vet. Parasitol. 127:277-283. doi:10.1016/j.vetpar.2004.10.015
162. Papagiannopoulos, M., H.R. Wollseifen, A. Mellenthin, B. Haber, and R. Galensa. 2004. Identification and quantification of polyphenols in carob fruits (Ceratonia siliqua L.) and derived products by HPLC-UV-ESI/MSn. J. Agric. Food Chem. 52:3784-3791. doi:10.1021/jf030660y
163. Patra, A.K., and J. Saxena. 2010. A new perspective on the use of plant secondary metabolites to inhibit methanogenesis in the rumen. Phytochemistry 71:1198-1222. doi:10.1016/j.phytochem.2010.05.010
164. Pawelek, D.L., J.P. Muir, B.D. Lambert, and R.D. Wittie. 2008. In sacco rumen disappearance of condensed tannins, fiber, and nitrogen from herbaceous native Texas legumes in goats. Anim. Feed Sci. Technol. 142:1-16. doi:10.1016/j.anifeedsci.2007.02.014
165. Per, T.S., N.A. Khan, P.S. Reddy, A. Masood, M. Hasanuzzaman, M.I.R. Khan, and N.A. Anjum. 2017. Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: Phytohormones, mineral nutrients and transgenics. Plant Physiol. Biochem. 115:126-140. doi:10.1016/j.plaphy.2017.03.018
166. Pérez-Díaz, R., M. Ryngajllo, J. Pérez-Díaz, H. Peña-Cortés, J.A. Casaretto, E. González-Villanueva, and S. Ruiz-Lara. 2014. VvMATE1 and VvMATE2 encode putative proanthocyanidin transporters expressed during berry development in Vitis vinifera L. Plant Cell Rep. 33:1147-1159. doi:10.1007/s00299-014-1604-9
167. Pérez-Jiménez, J., and J. Lluís Torres. 2011. Analysis of nonextractable phenolic compounds in foods: The current state of the art. J. Agric. Food Chem. 59:12713-12724. doi:10.1021/jf203372w
168. Petersen, J.C., N.S. Hill, and J.A. Mosjidis. 1991. Screening sericea lespedeza germplasm for herbage quality. Agron. J. 83:581-588. doi:10.2134/agronj1991.00021962008300030016x
169. Piluzza, G., L. Sulas, and S. Bullitta. 2014. Tannins in forage plants and their role in animal husbandry and environmental sustainability: A review. Grass Forage Sci. 69:32-48.
170. Porter, L.J. 1988. Flavans and proanthocyanidins. In: J.B. Harborne, editor, The flavonoids: Advances in research since 1980. Springer, Boston, MA. p. 21-62. doi:10.1007/978-1-4899-2913-6_2
171. Powell, J.M., M.J. Aguerre, and M.A. Wattiaux. 2011. Tannin extracts abate ammonia emissions from simulated dairy barn floors. J. Environ. Qual. 40:907-914. doi:10.2134/jeq2010.0492
172. Priolo, A., M. Bella, M. Lanza, V. Galofaro, L. Biondi, D. Barbagallo, et al. 2005. Carcass and meat quality of lambs fed fresh sulla (Hedysarum coronarium L.) with or without polyethylene glycol or concentrate. Small Rumin. Res. 59:281-288. doi:10.1016/j.smallrumres.2005.05.012
173. Purchas, R.W., and R.G. Keogh. 1984. Fatness of lambs grazed on ‘Grasslands Maku’ lotus and ‘Grasslands Huia’ white clover. Proc. N. Z. Soc. Anim. Prod. 44:219-221.
174. Quijada, J., C. Drake, E. Gaudin, R. El-Korso, H. Hoste, and I. Mueller-Harvey. 2018. Condensed tannin changes along the digestive tract in lambs fed with sainfoin pellets or hazelnut skins. J. Agric. Food Chem. (in press). doi:10.1021/acs.jafc.7b05538
175. Quijada, J., C. Fryganas, H.M. Ropiak, A. Ramsay, I. Mueller-Harvey, and H. Hoste. 2015. Anthelmintic activities against Haemonchus contortus or Trichostrongylus colubriformis from small ruminants are influenced by structural features of condensed tannins. J. Agric. Food Chem. 63:6346-6354. doi:10.1021/acs.jafc.5b00831
176. Ramírez-Restrepo, C.A., A. Pernthaner, T.N. Barry, N. López-Villalobos, R.J. Shaw, W.E. Pomroy, and W.R. Hein. 2010. Characterization of immune responses against gastrointestinal nematodes in weaned lambs grazing willow fodder blocks. Anim. Feed Sci. Technol. 155:99-110. doi:10.1016/j.anifeedsci.2009.10.006
177. Ramsay, A., C. Drake, A. Grosse Brinkhaus, M. Girard, F. Dohme-Meier, G. Bee, et al. 2015. NaOH enhances extractability and analysis of proanthocyanidins in ensiled sainfoin (Onobrychis viciifolia). J. Agric. Food Chem. 63:9471-9479. doi:10.1021/acs.jafc.5b04106
178. Ramsay, A., A.R. Williams, S.M. Thamsborg, and I. Mueller-Harvey. 2016. Galloylated proanthocyanidins from shea (Vitellaria paradoxa) meal have potent anthelmintic activity against Ascaris suum. Phytochemistry 122:146-153. doi:10.1016/j.phytochem.2015.12.005
179. Rautio, P., U.A. Bergvall, M. Karonen, and J.-P. Salminen. 2007. Bitter problems in ecological feeding experiments: Commercial tannin preparations and common methods for tannin quantifications. Biochem. Syst. Ecol. 35:257-262. doi:10.1016/j.bse.2006.10.016
180. Reid, C.S.W., M. Ulyatt, and J.M. Wilson. 1974. Plant tannins, bloat and nutritive value. Proc. N. Z. Soc. Anim. Prod. 34:82-92.
181. Ríos-De Álvarez, L., A.W. Greer, F. Jackson, S. Athanasiadou, I. Kyriazakis, and J.F. Huntley. 2008. The effect of dietary sainfoin (Onobrychis viciifolia) on local cellular responses to Trichostrongylus colubriformis in sheep. Parasitology 135:1117-1124. doi:10.1017/S0031182008004563
182. Rochfort, S., A.J. Parker, and F.R. Dunshea. 2008. Plant bioactives for ruminant health and productivity. Phytochemistry 69:299-322. doi:10.1016/j.phytochem.2007.08.017
183. Rodríguez-Pérez, C., R. Quirantes-Pine, N. Amessis-Ouchemoukh, K. Madani, A. Seguar-Carretero, and A. Fernandex-Gutierrez. 2013. A metabolite-profiling approach allows the identification of new compounds from Pistacia lentiscus leaves. J. Pharm. Biomed. Anal. 77:167-174. doi:10.1016/j.jpba.2013.01.026
184. Ropiak, H.M., O. Desrues, A.R. Williams, A. Ramsay, I. Mueller-Harvey, and S.M. Thamsborg. 2016a. Structure-activity relationship of condensed tannins and synergism with trans-cinnamaldehyde against Caenorhabditis elegans. J. Agric. Food Chem. 64:8795-8805. doi:10.1021/acs.jafc.6b03842
185. Ropiak, H.M., P. Lachmann, A. Ramsay, R.J. Green, and I. Mueller-Harvey. 2017. Identification of structural features of condensed tannins that affect protein aggregation. PLoS One 12:e0170768. doi:10.1371/journal.pone.0170768
186. Ropiak, H.M., A. Ramsay, and I. Mueller-Harvey. 2016b. Condensed tannins in extracts from European medicinal plants and herbal products. J. Pharm. Biomed. Anal. 121:225-231. doi:10.1016/j.jpba.2015.12.034
187. Salminen, J.-P., and M. Karonen. 2011. Chemical ecology of tannins and other phenolics: We need a change in approach. Funct. Ecol. 25:325-338. doi:10.1111/j.1365-2435.2010.01826.x
188. Saratsis, A., N. Voutzourakis, T. Theodosiou, A. Stefanakis, and S. Sotiraki. 2016. The effect of sainfoin (Onobrychis viciifolia) and carob pods (Ceratonia siliqua) feeding regimes on the control of lamb coccidiosis. Parasitol. Res. 115:2233-2242. doi:10.1007/s00436-016-4966-9
189. Scharenberg, A., Y. Arrigo, A. Gutzwiller, U. Wyss, D.H. Hess, M. Kreuzer, and F. Dohme. 2007. Effect of feeding dehydrated and ensiled tanniferous sainfoin (Onobrychis viciifolia) on nitrogen and mineral digestion and metabolism of lambs. Arch. Anim. Nutr. 61:390-405. doi:10.1080/17450390701565081
190. Schofield, P., D.M. Mbugua, and A.N. Pell. 2001. Analysis of condensed tannins: A review. Anim. Feed Sci. Technol. 91:21-40. doi:10.1016/S0377-8401(01)00228-0
191. Schreurs, N.M., D.M. Marotti, M.H. Tavendale, G.A. Lane, T.N. Barry, N. López-Villalobos, and W.C. McNabb. 2007. Concentration of indoles and other rumen metabolites in sheep after a meal of fresh white clover, perennial ryegrass or Lotus corniculatus and the appearance of indoles in the blood. J. Sci. Food Agric. 87:1042-1051. doi:10.1002/jsfa.2804
192. Scioneaux, A.N., M.A. Schmidt, M.A. Moore, R.L. Lindroth, S.C. Wooley, and A.E. Hagerman. 2011. Qualitative variation in proanthocyanidin composition of Populus species and hybrids: Genetics is the key. J. Chem. Ecol. 37:57-70. doi:10.1007/s10886-010-9887-y
193. Self, R., J. Eagles, G.C. Galletti, I. Mueller-Harvey, R.D. Hartley, A.G.H. Lea, et al. 1986. Fast atom bombardment mass spectrometry of polyphenols (syn. vegetable tannins). Biomed. Environ. Mass Spectrom. 13:449-468. doi:10.1002/bms.1200130902
194. Sheldrick, R.D., and D.J. Thomson. 1982. Management and utilization of sainfoin (Onobrychis sativa). Inf. Leaflet no. 13. Grassl. Res. Inst., Hurley, Berkshire, UK.
195. Sivakumaran, S., A.L. Molan, L.P. Meagher, B. Kolb, L.Y. Foo, G.A. Lane, et al. 2004. Variation in antimicrobial action of proanthocyanidins from Dorycnium rectum against rumen bacteria. Phytochemistry 65:2485-2497. doi:10.1016/j.phytochem.2004.08.046
196. Sivakumaran, S., W. Rumball, G.A. Lane, K. Fraser, L.Y. Foo, M. Yu, and L.P. Meagher. 2006. Variation of proanthocyanidins in Lotus species. J. Chem. Ecol. 32:1797-1816. doi:10.1007/s10886-006-9110-3
197. Spencer, P., S. Sivakumaran, K. Fraser, L.Y. Foo, G.A. Lane, P.J.B. Edwards, and L.P. Meagher. 2007. Isolation and characterisation of procyanidins from Rumex obtusifolius. Phytochem. Anal. 18:193-203. doi:10.1002/pca.967
198. Springer, T.L., R.L. McGraw, and G.E. Aiken. 2002. Variation of condensed tannins in roundhead lespedeza germplasm. Crop Sci. 42:2157-2160. doi:10.2135/cropsci2002.2157
199. Stienezen, M., G.C. Waghorn, and G.B. Douglas. 1996. Digestibility and effects of condensed tannins on digestion of sulla (Hedysarum coronarium) when fed to sheep. N. Z. J. Agric. Res. 39:215-221. doi:10.1080/00288233.1996.9513180
200. Stringano, E. 2011. Analysis of sainfoin (Onobrychis viciifolia) proanthocyanidins by complementary and newly developed techniques. Ph.D. diss., Univ. of Reading, Reading, UK.
201. Stringano, E., R. Cramer, W. Hayes, C. Smith, T. Gibson, and I. Mueller-Harvey. 2011. Deciphering the complexity of sainfoin (Onobrychis viciifolia) proanthocyanidins by MALDI-TOF mass spectrometry with a judicious choice of isotope patterns and matrices. Anal. Chem. 83:4147-4153. doi:10.1021/ac2003856
202. Stringano, E., C. Hayot Carbonero, L.M.J. Smith, R.H. Brown, and I. Mueller-Harvey. 2012. Proanthocyanidin diversity in the EU ‘HealthyHay’ sainfoin (Onobrychis viciifolia) germplasm collection. Phytochemistry 77:197-208. doi:10.1016/j.phytochem.2012.01.013
203. Suter, M., D. Hofer, and A. Lüscher. 2017. Weed suppression enhanced by increasing functional trait dispersion and resource capture in forage ley mixtures. Agric. Ecosyst. Environ. 240:329-339. doi:10.1016/j.agee.2017.01.007
204. Szabados, L., and A. Savouré. 2010. Proline: A multifunctional amino acid. Trends Plant Sci. 15:89-97. doi:10.1016/j.tplants.2009.11.009
205. Szczyglowski, K., and J. Stougaard. 2008. Lotus genome: Pod of gold for legume research. Trends Plant Sci. 13:515-517. doi:10.1016/j.tplants.2008.08.001
206. Takeuchi, H., V.T. Trang, N. Morimoto, Y. Nishida, Y. Matsumura, and T. Sugiura. 2014. Natural products and food components with anti-Helicobacter pylori activities. World J. Gastroenterol. 20:8971-8978. doi:10.3748/wjg.v20.i27.8971
207. Tedeschi, L.O., C.A. Ramírez-Restrepo, and J.P. Muir. 2014. Developing a conceptual model of possible benefits of condensed tannins for ruminant production. Animal 8:1095-1105. doi:10.1017/S1751731114000974
208. Terrill, T.H., J.E. Miller, J.M. Burke, J.A. Mosjidis, and R.M. Kaplan. 2012. Experiences with integrated concepts for the control of Haemonchus contortus in sheep and goats in the United States. Vet. Parasitol. 186:28-37. doi:10.1016/j.vetpar.2011.11.043
209. Terrill, T.H., W.R. Windham, C.S. Hoveland, H.E. Amos, B. Kouakou, and S. Gelaye. 1997. Nitrogen and fiber digestion in sheep fed fresh-frozen and field-dried high- and low-tannin sericea lespedeza. In: J.G. Buchanan-Smith, L.D. Bailey, and P. McCaughey, editors, Proceedings of the 18th International Grasslands Congress, Winnipeg, MB, and Saskatoon, SK. 9-18 June 1997. Int. Grassl. Congr., Lexington, KY. p. 8-11-8-12. http://www.internationalgrasslands.org/files/igc/publications/1997/1-08-011.pdf (accessed 30 Sept. 2017).
210. Terrill, T.H., E. Griffin, D.S. Kommuru, J.E. Miller, J.A. Mosjidis, M.T. Kearney, and J.M. Burke. 2016. Effect of ensiling on anti-parasitic properties of sericea lespedeza. Am. Forage Grassl. Counc., Berea, KY. http://www.afgc.org/proceedings/2016/TerrillAFGCpaper.pdf (accessed 30 Sept. 2017).
211. Theodoridou, K., J. Aufrère, D. Andueza, A. Le Morvan, F. Picard, J. Pourrat, and R. Baumont. 2012. Effects of condensed tannins in wrapped silage bales of sainfoin (Onobrychis viciifolia) on in vivo and in situ digestion in sheep. Animal 6:245-253. doi:10.1017/S1751731111001510
212. Theodoridou, K., J. Aufrère, D. Andueza, A. Le Morvan, F. Picard, E. Stringano, et al. 2011. Effect of plant development during first and second growth cycle on chemical composition, condensed tannins and nutritive value of three sainfoin (Onobrychis viciifolia) varieties and lucerne. Grass Forage Sci. 66:402-414. doi:10.1111/j.1365-2494.2011.00798.x
213. Theodoridou, K., J. Aufrère, D. Andueza, J. Pourrat, A. Le Morvan, E. Stringano, et al. 2010. Effects of condensed tannins in fresh sainfoin (Onobrychis viciifolia) on in vivo and in situ digestion in sheep. Anim. Feed Sci. Technol. 160:23-38. doi:10.1016/j.anifeedsci.2010.06.007
214. Thomson, D.J., D.E. Beever, D.G. Harrison, I.W. Hill, and D.F. Osbourn. 1971. The digestion of dried lucerne (Medicago sativa, L) and dried sainfoin (Onobrychis viciifolia, Scop) by sheep. Proc. Nutr. Soc. 30:14A.
215. Tibe, O., L.P. Meagher, K. Fraser, and D.R.K. Harding. 2011. Condensed tannins and flavonoids from the forage legume sulla (Hedysarum coronarium). J. Agric. Food Chem. 59:9402-9409. doi:10.1021/jf2014759
216. Tibe, O., A. Pernthaner, I. Sutherland, L. Lesperance, and D.R.K. Harding. 2012. Condensed tannins from Botswanan forage plants are effective priming agents of gd T cells in ruminants. Vet. Immunol. Immunopathol. 146:237-244. doi:10.1016/j.vetimm.2012.03.003
217. Tyrrell, H.F., and P.W. Moe. 1975. Effect of intake on digestive efficiency. J. Dairy Sci. 58:1151-1163. doi:10.3168/jds.S0022-0302(75)84694-7
218. Vasileva, V., and A. Ilieva. 2016. Changes in some parameters in mixtures of sainfoin with subterranean clover. Int. J. Waste Resour. 6:226. doi:10.4172/2252-5211.1000226
219. Verdier, J., J. Zhao, I. Torres-Jerez, S. Ge, C. Liu, X. He, et al. 2012. MtPAR MYB transcription factor acts as an on switch for proanthocyanidin biosynthesis in Medicago truncatula. Proc. Natl. Acad. Sci. USA 109:1766-1771. doi:10.1073/pnas.1120916109
220. Vernhet, A., S. Dubascoux, B. Cabane, H. Fulcrand, E. Dubreucq, and C. Poncet-Legrand. 2011. Characterization of oxidized tannins: Comparison of depolymerization methods, asymmetric flow field-flow fractionation and small-angle X-ray scattering. Anal. Bioanal. Chem. 401:1559-1569. doi:10.1007/s00216-011-5076-2
221. Villalba, J.J., R. Cabassu, and S.A. Gunter. 2015. Forage choice in pasturelands: Influence on cattle foraging behavior and performance. J. Anim. Sci. 93:1729-1740. doi:10.2527/jas.2014-8667
222. Waghorn, G. 2008. Beneficial and detrimental effects of dietary condensed tannins for sustainable sheep and goat production: Progress and challenges. Anim. Feed Sci. Technol. 147:116-139. doi:10.1016/j.anifeedsci.2007.09.013
223. Waghorn, G.C., A. John, W.T. Jones, and I.D. Shelton. 1987. Nutritive value of Lotus corniculatus L. containing low and medium concentrations of condensed tannins for sheep. Proc. N. Z. Soc. Anim. Prod. 47:25-30.
224. Waghorn, G.C., and W.J. Jones. 1989. Bloat in cattle 46. The potential of dock (Rumex obtusifolius) as an antibloat agent for cattle. N. Z. J. Agric. Res. 32:227-235. doi:10.1080/00288233.1989.10423458
225. Waghorn, G.C., W.T. Jones, I.D. Shelton, and W.C. McNabb. 1990. Condensed tannins and the nutritive value of herbage. Proc. N. Z. Grassl. Assoc. 51:171-179.
226. Waghorn, G.C., and A.L. Molan. 2001. Effect of condensed tannins in Dorycnium rectum on its nutritive value and on the development of sheep parasite larvae. Proc. N. Z. Grassl. Assoc. 63:273-278.
227. Waghorn, G.C., and I.D. Shelton. 1997. Effect of condensed tannins in Lotus corniculatus on the nutritive value of pasture for sheep. J. Agric. Sci. 128:365-372. doi:10.1017/S0021859697004218
228. Waghorn, G.C., J.D. Reed, and L.R. Ndlovu. 1997. Condensed tannins and herbivore nutrition. In: J.G. Buchanan-Smith, L.D. Bailey, and P. McCaughey, editors, Proceedings of the 18th International Grasslands Congress, Winnipeg, MB, and Saskatoon, SK. 9-18 June 1997. Int. Grassl. Congr., Lexington, KY. p. 153-166. http://www.internationalgrasslands.org/files/igc/publications/1997/iii-153.pdf (accessed 30 Sept. 2017).
229. Wang, Y., L.R. Barbieri, B.P. Berg, and T.A. McAllister. 2007. Effects of mixing sainfoin with alfalfa on ensiling, ruminal fermentation and total tract digestion of silage. Anim. Feed Sci. Technol. 135:296-314. doi:10.1016/j.anifeedsci.2006.07.002
230. Wang, Y., B.P. Berg, L.R. Barbieri, D.M. Veira, and T.A. McAllister. 2006. Comparison of alfalfa and mixed alfalfa-sainfoin pastures for grazing cattle: Effects on incidence of bloat, ruminal fermentation, and feed intake. Can. J. Anim. Sci. 86:383-392. doi:10.4141/A06-009
231. Wang, Y., W. Majak, and T.A. McAllister. 2012. Forthy bloat in ruminants: Cause, occurrence, and mitigation strategies. Anim. Feed Sci. Technol. 172:103-114. doi:10.1016/j.anifeedsci.2011.12.012
232. Wang, Y., T.A. McAllister, and S. Acharya. 2015. Condensed tannins in sainfoin: Composition, concentration, and effects on nutritive and feeding value of sainfoin forage. Crop Sci. 55:13-22. doi:10.2135/cropsci2014.07.0489
233. Wang, Y., A.P. Singh, W.J. Hurst, J.A. Glinski, H. Koo, and N. Vorsa. 2016. Influence of degree-of-polymerization and linkage on the quantification of proanthocyanidins using 4-dimethylaminocinnamaldehyde (DMAC) assay. J. Agric. Food Chem. 64:2190-2199. doi:10.1021/acs.jafc.5b05408
234. Wang, Y., G.C. Waghorn, W.C. McNabb, T.N. Barry, M.J. Hedley, and I.D. Shelton. 1996. Effect of condensed tannins in Lotus corniculatus upon the digestion of methionine and cysteine in the small intestine of sheep. J. Agric. Sci. 127:413-421. doi:10.1017/S0021859600078576
235. Williams, A.R., C. Fryganas, A. Ramsay, I. Mueller-Harvey, and S.M. Thamsborg. 2014a. Direct anthelmintic effects of condensed tannins from diverse plant sources against Ascaris suum. PLoS One 9:e97053. doi:10.1371/journal.pone.0097053 [erratum: 9:e99738.]
236. Williams, A.R., C. Fryganas, K. Reichwald, S. Skov, I. Mueller-Harvey, and S.M. Thamsborg. 2016. Polymerization-dependent activation of porcine gd T-cells by proanthocyanidins. Res. Vet. Sci. 105:209-215. doi:10.1016/j.rvsc.2016.02.021
237. Williams, A.R., E.J. Klaver, L.C. Laan, A. Ramsay, C. Fryganas, R. Difborg, et al. 2017. Co-operative suppression of inflammatory responses in human dendritic cells by proanthocyanidins and products from the parasitic nematode Trichuris suis. Immunology 150:312-328. doi:10.1111/imm.12687
238. Williams, A.R., A. Ramsay, T.V.A. Hansen, H.M. Ropiak, H. Mejer, P. Nejsum, et al. 2015. Anthelmintic activity of trans-cinnamaldehyde and A- and B-type proanthocyanidins derived from cinnamon (Cinnamomum verum). Nat. Sci. Rep. 5:14791. doi:10.1038/srep14791
239. Williams, A.R., H.M. Ropiak, C. Fryganas, O. Desrues, I. Mueller-Harvey, and S.M. Thamsborg. 2014b. Assessment of the anthelmintic activity of medicinal plant extracts and purified condensed tannins against free-living and parasitic stages of Oesophagostomum dentatum. Parasit. Vectors 7:518. doi:10.1186/s13071-014-0518-2
240. Zarrabian, M., M.M. Majidi, and M.H. Ehtemam. 2013. Genetic diversity in a worldwide collection of sainfoin using morphological, anatomical, and molecular markers. Crop Sci. 53:2483-2495. doi:10.2135/cropsci2013.03.0130
241. Zeller, W.E. 2019. Activity, purification, and analysis of condensed tannins: Current state of affairs and future endeavors. Crop Sci. 59:886-904. doi:10.2135/cropsci2018.05.0323
242. Zeller, W.E., and J.H. Grabber. 2015. Redesigning forages with condensed tannins. Progressive Forage Grower 16:7-8.
243. 13C HSQC NMR spectroscopy for estimating procyanidin/prodelphinidin and cis/trans flavanol ratios of condensed tannin fractions: Correlation with thiolysis. J. Agric. Food Chem. 63:1967-1973. doi:10.1021/jf504743b
244. Zeller, W.E., M.L. Sullivan, I. Mueller-Harvey, J.H. Grabber, A. Ramsay, C. Drake, and R.H. Brown. 2015b. Protein precipitation behavior of condensed tannins from Lotus pedunculatus and Trifolium repens with different mean degrees of polymerization. J. Agric. Food Chem. 63:1160-1168. doi:10.1021/jf504715p
245. Zhou, M., L. Wei, Z. Sun, L. Gao, Y. Meng, Y. Tang, and Y. Wu. 2015. Production and transcriptional regulation of proanthocyanidin biosynthesis in forage legumes. Appl. Microbiol. Biotechnol. 99:3797-3806. doi:10.1007/s00253-015-6533-1
246. Zhu, Q., S. Sui, X. Lei, Z. Yang, K. Lu, G. Liu, et al. 2015. Ectopic expression of the Coleus R2R3 MYB-type proanthocyanidin regulator gene SsMYB3 alters the flower color in transgenic tobacco. PLoS One 10:e0139392. doi:10.1371/journal.pone.0139392