Skip to main content
SpringerLink
Log in

Biologically active compounds from forage plants

  • Published:
Phytochemistry Reviews Aims and scope Submit manuscript

Abstract

Forage plants have attracted attention for the presence of biologically active compounds that can influence the animal nutrition but may also have a therapeutic potential for humans. These specialized metabolites are in general low-molecular-weight compounds present in low concentration in plants and belong to different chemical classes, including terpenes, saponins, cyanogenic glycosides, flavones, isoflavones, tannins, coumarins and other phenolics. They are involved in various metabolic processes or are stored as inactive precursors which are specifically activated when necessary. The knowledge of bioactive molecules from botanical sources is of great interest for their potential use in pharmaceutical and in the agro-industry. Among forage plants, the Fabaceae (syn. Leguminosae) family is the richest in specialized metabolites. Since forage legumes are widespread and extensively cultivated, they can represent an important source for the extraction of these bioactive phytochemicals. This review deals with bioactive substances from several representative legume forage plants, such as Medicago arabica Huds, M. arborea L., M. polymorpha L., M. sativa L., M. truncatula Gaertn., Trifolium alexandrinum L., T. pratense L., T. repens L., T. subterraneum L., Onobychis viciifolia Scop., Melilotus albus Medik., M. officinalis L. (Pall.), Hedysarum coronarium L., Lotus corniculatus L., L. pedunculatus Cav., Trigonella foenum-graecum L. and Bituminaria bituminosa (L.) C.H. Stirt. Emphasis was given to compounds that usually represent the most active and studied metabolites of the above-mentioned species. Detailed information on their qualitative and quantitative composition were reviewed, as their biological activities are strictly related to their chemical structure and concentration in the plant material. Some information regarding their role in livestock nutrition and their importance for pharmacological application were also reported.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14

Similar content being viewed by others

References

  • Abbruscato P, Tosi S, Crispino L, Biazzi E, Menin B, Picco AM, Pecetti L, Avato P, Tava A (2014) Triterpenoid glycosides from Medicago sativa as antifungal agents against Pyricularia oryzae. J Agric Food Chem 62:11030–11036

    Article  CAS  PubMed  Google Scholar 

  • Ahmed S, Zeb A (2020) Phytochemical profile and pharmaceutical properties of Trifolium repens. J Basic Clin Physiol Pharmacol. https://doi.org/10.1515/jbcpp-2020-0015

    Article  Google Scholar 

  • Al-Hazimi HM, Al-Andis NM (2000) Minor pterocarpanoids from Melilotus albus. J Saudi Chem Soc 4:215–218

    CAS  Google Scholar 

  • Al-Snafi AE (2020) Chemical constituents and pharmacological effect of Melilotus officinalis—a review. IOSR J Pharm 10:26–36

    CAS  Google Scholar 

  • Aminkar S, Shojaeiyan A, Monfared SR, Ayyari M (2018) Quantitative assessment of diosgenin from different ecotypes of Iraninan fenugreek (Trigonella foenum-graecum L.) by high-performance liquid chromatography. Int J Hortic Sci Technol 5:103–109

    CAS  Google Scholar 

  • Andrei V, Rubio JL, Cerni R (1995) Effect of mediterranean shrubs on water erosion control. Environ Monitor Assess 37:5–15

    Article  Google Scholar 

  • Annicchiarico P, Ruisi P, Di Miceli G, Pecetti L (2014) Morpho-physiological and adaptative variation of Italian germplasm of sulla (Hedysarum coronarium L.). Crop past Sci 65:206–213

    Article  CAS  Google Scholar 

  • Anwer SM, Mohtasheem M, Azhar I, Ahmed SW, Bano H (2008) Chemical constituents from Melilotus officinalis. J Bas Appl Sci 4:89–94

    CAS  Google Scholar 

  • Argentieri MP, D’Addabbo T, Tava A, Agostinelli A, Jurzysta M, Avato P (2008) Evaluation of nematicidal properties of saponins from Medicago spp. Eur J Plant Pathol 120:189–197

    Article  CAS  Google Scholar 

  • Avato P, Bucci R, Tava A, Vitali C, Rosato A, Bialy Z, Jurzysta M (2006) Antimicrobial activity of saponins from Medicago sp.: structure-activity relationship. Phytoter Res 20:454–457

    Article  CAS  Google Scholar 

  • Avato P, Migoni D, Argentieri M, Fanizzi FP, Tava A (2017) Activity of saponins from Medicago species against HeLa and MCF-7 cell lines and their capacity to potentiate cisplatin effect. Anti-Canc Ag Med Chem 17:1508–1518

    CAS  Google Scholar 

  • Azuhnwi BN, Boller B, Dohme-Meier F, Hess HD, Kreuzer M, Stringano M, Mueller-Harvey I (2013) Exploring variation in proanthocyanidin composition and content of sainfoin (Onobrychis viciifolia). J Sci Food Agric 93:2102. https://doi.org/10.1002/jsfa.6119

    Article  CAS  PubMed  Google Scholar 

  • Azzouzi S, Zaabat N, Medjroubi K, Akkal S, Benlabed K, Smati F, Dijoux-Franca MG (2014) Phytochemical and biological activities of Bituminaria bituminosa L. (Fabaceae). As Pac J Trop Med 7:S481–S484

    Article  CAS  Google Scholar 

  • Balestrazzi A, Agoni V, Tava A, Avato P, Biazzi E, Raimondi E, Macovei A, Carbonera D (2011a) Cell death induction and nitric oxide biosynthesis in white poplar (Populus alba L.) suspension cultures exposed to alfalfa saponins. Physiol Plant 141:227–238

    Article  CAS  PubMed  Google Scholar 

  • Balestrazzi A, Macovei A, Tava A, Avato P, Raimondi E, Carbonera D (2011b) Unravelling the response of plant cells to cytotoxic saponins—role of metallothionein and nitric oxide. Plant Signal Behav 64:516–519

    Article  CAS  Google Scholar 

  • Balestrazzi A, Carbonera D, Avato P, Tava A (2014) White poplar (Populus alba L.) suspension cultures as a model system to study apoptosis induced by alfalfa saponins. Anti-Canc Ag Med Chem 14:1324–1331

    Article  CAS  Google Scholar 

  • Barbetti MJ (2007) Resistance in annual Medicago spp. to Phoma medicaginis and Leptosphaerulina trifolii and its relationship to induction of a phytoestrogen. Plant Dis 91:239–244

    Article  PubMed  Google Scholar 

  • Barone CD, Zajac AM, Ferguson SM, Brown RN, Reed JD, Krueger CG, Petersson KH (2019) In vitro screening of 51 birdsfoot trefoil (Lotus corniculatus L.; Fabaceae) strains for anti-parasitic effects against Haemonchus contortus. Parasitol 146:828–836. https://doi.org/10.1017/S0031182018002214

    Article  CAS  Google Scholar 

  • Barreira JCM, Visnevschi-Necrasov T, Nunes E, Cunha SC, Pereira G, Oliveira MBPP (2015) Medicago spp. as a potential source of bioactive isoflavones: characterization according to phylogenetic and phenologic factors. Phytochemistry 116:230–235

    Article  CAS  PubMed  Google Scholar 

  • Barry TN, McNabb WC (1999) The implication of condensed tannins on the nutritive value of temperate forages fed to ruminants. Brit J Nutr 81:263–272

    Article  CAS  PubMed  Google Scholar 

  • Bennett RN, Wallsgrove RM (1994) Secondary metabolites in plant defense mechanisms. New Phytol 127:617–633

    Article  CAS  PubMed  Google Scholar 

  • Berard NC, Wang Y, Wittenberg KM, Krause DO, Coulman BE, McAllister TA, Ominski KH (2011) Condensed tannin concentrations found in vegetative and mature forage legumes grown in western Canada. Can J Plant Sci 91:669. https://doi.org/10.4141/cjps10153

    Article  CAS  Google Scholar 

  • Bialy Z, Jurzysta M, Oleszek W, Piacente S, Pizza C (1999) Saponins in alfalfa (Medicago sativa L.) root and their structural elucidation. J Agric Food Chem 47:3185–3192

    Article  CAS  PubMed  Google Scholar 

  • Bialy Z, Jurzysta M, Mella M, Tava A (2004) Triterpene saponins from aerial parts of Medicago arabica L. J Agric Food Chem 52:1095–1099

    Article  CAS  PubMed  Google Scholar 

  • Biazzi E, Carelli M, Tava A, Abbruscato P, Losini I, Avato P, Scotti C, Calderini O (2015) CYP72A67 catalyzes a key oxidative step in Medicago truncatula hemolytic saponin biosynthesis. Mol Plant 8:1493–1506

    Article  CAS  PubMed  Google Scholar 

  • Boller B, Posselt UK, Veronesi F (2010) In Fodder crops and amenity grasses - Handbook of plant breeding series, vol 5, Boller B, Posselt UK, Veronesi F Eds, Springer, New York, NY

  • Booth NL, Overk CR, Yao P, Totura S, Deng Y, Hedayat AS, Bolton JL, Pauli GF, Farnsworth NR (2006) Seasonal variation of red clover (Trifolium pratense L. Fabaceae) isoflavones and estrogenic activity phase. J Agric Food Chem 54:1277–1282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bora KS, Sharma A (2011a) Evaluation of antioxidant and cerebroprotective effect of Medicago sativa Linn. against ischemia and reperfusion insult. Evid Based Complement Alternat Med Article ID 792167, doi: https://doi.org/10.1093/ecam/neq019

  • Bora KS, Sharma A (2011b) Phytochemical and pharmacological potential of Medicago sativa: a review. Pharmac Biol 49:211–220

    Article  Google Scholar 

  • Bousquet-Mélou A, Louis S, Robles C, Greff S, Dupouyet S, Fernandez C (2005) Allelopathic potential of M. arborea, a Mediterranean invasive shrub. Chemoecol 15:193–198

    Article  Google Scholar 

  • Brown RH, Mueller-Harvey I, Zeller WE, Reinhardt L, Stringano E, Gea A, Drake C, Ropiak HM, Fryganas C, Ramsay A, Hardcastle EE (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

    Article  CAS  PubMed  Google Scholar 

  • Budzyńska A, Sodowska B, Więckowska-Szakiel M, Micota B, Stochmal A, Jędrejek D, Pecio Ł, Różalska B (2014) Saponins from Trifolium spp. aerial parts as modulator of Candida albicans virulence attributes. Molecules 19:10601–10617

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Burlando B, Pastorino G, Salis A, Damonte G, Clericuzio M, Cornara L (2017) The bioactivity of Hedysarum coronarium extracts on skin enzymes and cells correlates with phenolic content. Pharm Biol 55:1984–1991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Butkutė B, Lemežienė N, Dabkevičienė G, Jakštas V, Vilčinskas E, Janulis V (2014) Source of variation of isoflavone concentration in perennial clover species. Pharmacol Mag 10:S181–S188

    Article  Google Scholar 

  • Butkutė B, Padarauskas A, Cesevičiene J, Pavilonis A, Taujenis L, Lemežienė N (2017) Perennial legumes as a source of ingredients for healthy food: proximate, mineral and phytoestrogen composition and antibacterial activity. J Food Sci Technol 54:2661–2669

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cansunar E, Richardson AJ, Wallace G, Stewart CS (1990) Effect of coumarin on glucose uptake by anaerobic rumen fungi in the presence and absence of Methanobrevibacter smithii. FEMS Microb Lett 70:157–160

    CAS  Google Scholar 

  • Carelli M, Biazzi E, Panara F, Tava A, Scaramelli L, Porceddu A, Graham N, Odoardi M, Piano E, Arcioni S, May S, Scotti C, Calderini O (2011) Medicago truncatula CYP716A12 is a multifunctional oxidase involved in the biosynthesis of hemolytic saponins. Plant Cell 23:3070–3081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carelli M, Confalonieri M, Tava A, Biazzi E, Calderini O, Abbruscato P, Cammareri M, Scotti C (2020) Saponin synthesis in Medicago truncatula plants: CYP450-mediated formation of sapogenins in the different plant organs. In: The model legume Medicago truncatula. Ed. de Bruijn FJ, John Wiley & Son Inc. 111 River Street, Hoboken, NJ 07030, USA. Vol I, Ch 4.3, pp 225–236

  • Carlsen SCK, Fomsgaard IS (2008) Biologically active secondary metabolites in white clover (Trifolium repens L.)—a review focusing on content in the plant, plant-pest interactions and transformation. Chemoecol 18:129–170

    Article  CAS  Google Scholar 

  • Carlsen SCK, Mortensen AG, Oleszek W, Piacente S, Stochmal A, Fomsgaard S (2008) Variation in flavonoids in leaves, stem and flowers of white clover cultivars. Nat Prod Comm 3:1299–1306

    CAS  Google Scholar 

  • Cegiela U, Folwarczna J, Pytlik M, Zgorka G (2012) Effects of extracts from Trifolium medium L. and Trifolium pratense L. on development of estrogen deficiency-inducedosteoporosis in rats. Evid-Based Complem Altern Med Article ID 921684,doi:https://doi.org/10.1155/2012/921684

  • Chaudhary S, Chaudhary PS, Chikara SK, Sharma MC, Iriti M (2018) Review on fenugreek (Trigonella foenum-graecum L.) and its important secondary metabolite diosgenin. Not Bot Horti Agrobo 46:22–31

    Article  CAS  Google Scholar 

  • Confalonieri M, Carelli M, Gianoglio S, Moglia A, Biazzi E, Tava A (2021) CRISP/Cas9-mediated target mutagenesis of CYP93E2 modulates the triterpene saponin biosynthesis in Medicago truncatula. Front Plant Sci 12:690231. https://doi.org/10.3389/fpls.2021.690231

    Article  PubMed  PubMed Central  Google Scholar 

  • Conforti F, Perri V, Menichini F, Marrelli M, Uzunov D, Statti GA, Menichini F (2012) Wild Mediterranean dietary plants as inhibitors of pancreatic lipase. Phytother Res 26:600–604

    Article  CAS  PubMed  Google Scholar 

  • Cornara L, Xiao J, Burlando B (2016) Therapeutic potential of temperate forage legumes: a review. Crit Rev Food Sci Nutr 56:S149–S161

    Article  CAS  PubMed  Google Scholar 

  • Cornwell T, Cohick W, Raskin I (2004) Dietary phytoestrogen and health. Phytochemistry 65:995–1016

    Article  CAS  PubMed  Google Scholar 

  • Crush JR, Caradus JR (1995) Cyanogenesis potential and iodine concentration in white clover (Trifolium repens L.) cultivars. N Z J Agric Res 38:309–316

    Article  CAS  Google Scholar 

  • D’Addabbo T, Avato P, Tava A (2009) Nematicidal potential of materials from Medicago spp. Eur J Plant Pathol 125:39–49

    Article  Google Scholar 

  • D’Addabbo T, Carbonara T, Leonetti P, Radicci V, Tava A, Avato P (2011) Control of plant parasitic nematodes with active saponins and biomass from Medicago sativa. Phytochem Rev 10:503–519

    Article  CAS  Google Scholar 

  • D’Addabbo T, Laquale S, Lovelli S, Candido V, Avato P (2014) Biocide plants asa sustainable tool for the control of pests and pathogens in vegetable cropping systems. Ital J Agron 9:616

    Google Scholar 

  • D’Addabbo T, Argentieri MP, Zuchowski J, Biazzi E, Tava A, Oleszek W, Avato P (2020) Activity of saponins from Medicago species against phytoparasitic nematodes. Plants 9:443. https://doi.org/10.3390/plants9040443

    Article  CAS  PubMed Central  Google Scholar 

  • Dabkevičienė G, Butkutė B, Lemežienė N, Jakštas V, Vilčinskas E, Janulis V (2012) Distribution of formononetin, daidzein and genistein in Trifolium species and their aerial parts. Chemija 23:306–311

    Google Scholar 

  • Dangi R, Misar A, Tamhankar S, Rao S (2014) Diosgenin content in some Trigonella species. Ind J Adv Plant Res 1:47–51

    CAS  Google Scholar 

  • De Rijke E, Zafra-Gomez A, Ariese F, Brinkman UAT, Gooijer C (2001) determination of isoflavone glucoside malonates in Trifolium pratense L. (red clover) extracts: quantification and stability studies. J Chrom A 932:55–64

    Article  Google Scholar 

  • Demirci F, Dolar FS (2006) Effects of some plant materials on phytophtora blight (Phytophthora capsici Leon.) of pepper. Turk J Agric for 30:247–252

    Google Scholar 

  • Dombrowicz E, Światek L, Guryn R, Zadernowski R (1991) Phenolic acid in herb Melilotus officinalis. Pharmazie 46:156

    CAS  Google Scholar 

  • Dornbos DL Jr, Spencer GF, Miller RW (1990) Medicarpin delays alfalfa seed germination and seedling growth. Crop Sci 30:162–166

    Article  CAS  Google Scholar 

  • EMA (2011) Community herbal monograph on Trigonella foenum-graecum L, semen. EMA/HMPC/146221/2010-FINAL January 2011

  • EMA (2018) Medicago sativa extractum- Summary report. EMEA/MRL/453/98-FINAL June 1998

  • Farag MA, Rasheed DM, Kropf M, Heiss AG (2016) Metabolite profiling in Trigonella seeds via UPLC-MS and GC-MS analyzed using multivariate data analyses. Anal Bioanal Chem 408:8065–8078

    Article  CAS  PubMed  Google Scholar 

  • Fay FM, Dale PJ (1993) Condensed tannins in Trifolium species and their significance for taxonomy and plant breeding. Gen Res Crop Evol 40:7–17

    Article  Google Scholar 

  • Fernandes P, Cruz A, Angelova B, Pinheiro HM, Cabral JMS (2003) Microbial conversion of steroid compounds: recent developments. Enz Microb Technol 32:688–705

    Article  CAS  Google Scholar 

  • Fields RL, Barrel GK, Gash A, Zhao J, Moot DJ (2018) Alfalfa coumestrol content in response to development stage, fungi, aphids, and cultivar. Agron J 110:910–921

    Article  CAS  Google Scholar 

  • Foo LY, Jones WT, Porter LJ, Williams VM (1982) Proanthocyanidins polymers of fodder legumes. Phytochem 21:933–935

    Article  CAS  Google Scholar 

  • Foo LY, Newman R, Waghorn G, McNabb WC, Ulyatt MJ (1996) Proanthocyanidins from Lotus corniculatus. Phytochem 41:617–624

    Article  CAS  Google Scholar 

  • Foo LY, Lu Y, McNabb WC, Waghorn G, Ulyatt MJ (1997) Proanthocyanidins from Lotus pedunculatus. Phytochem 45:1689–1696

    Article  CAS  Google Scholar 

  • Foo LY, Lu Y, Molan AL, Woodfield DR, McNabb WC (2000) The phenols and prodelphinidins of white clover flowers. Phytochem 54:539–548

    Article  CAS  Google Scholar 

  • Fu F, Wang HL (2015) Metabolomics reveals consistency of the shoot system in Medicago truncatula by HPLC-UV-ESI-MS/MS. Int J Food Sci Technol 50:2183–2192

    Article  CAS  Google Scholar 

  • Goławska S, Łukasik I, Kapusta I, Janda B (2010) Analysis of flavonoid content in alfalfa. Ecol Chem Engin A 17:261–267

    Google Scholar 

  • Gómez-Zorita S, González-Arceo M, Fernández-Quintela A, Eseberri I, Trepiana J, Portillo MP (2020) Scientific evidence supporting the benefit effects of isoflavones on human health. Nutrients 12:3853. https://doi.org/10.3390/nu12123853

    Article  CAS  PubMed Central  Google Scholar 

  • Gong J, Fang K, Dong H, Wang D, Hu M, Lu F (2016) Effect of fenuggreek on hyperglycaemia and hyperlipidemia in diabetes andprediabetes: a meta-analysis. J Ethnopharmacol 194:260–268

    Article  PubMed  Google Scholar 

  • Goyal S, Gupta N, Chatterjee S (2016) Investigating therapeutic potential of Trigonella foenum-graecum L. as our defense mechanismagainst several human diseases. J Toxicol. https://doi.org/10.1155/2016/1250387

    Article  PubMed  PubMed Central  Google Scholar 

  • Grabber JH, Zeller WE, Mueller-Harvey I (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. https://doi.org/10.1021/jf304158m

    Article  CAS  PubMed  Google Scholar 

  • Greathead H (2003) Plants and plant extracts for improving animal productivity. Proc Nutr Soc 62:279–290

    Article  PubMed  Google Scholar 

  • Hanif MA, Al-Maskari AY, Al-Sabahi JN, Al-Hdhrami I, Khan MM, Al-Azkawi A, Hussain AI (2015) Chemical characterisation of bioactive compounds in Medicago sativa growing in the desert of Oman. Nat Prod Res 29:2332–2335

    Article  CAS  PubMed  Google Scholar 

  • Hedqvist H, Mueller-Harvey I, Reed JD, Krueger CG, Murphy M (2000) Characterization of tannins and in vitro protein digestibility of several Lotus corniculatus species. An Feed Sci Technol 87:41–56

    Article  CAS  Google Scholar 

  • Hloucalová P, Skládanka J, Horký P, Klejdus B, Pelikán J, Knotová D (2016) Determination of phytoestrogen content in fresh-cut legume forage. Animals 6:43. https://doi.org/10.3390/ani6070043

    Article  PubMed Central  Google Scholar 

  • Hofmann RW, Swinny EE, Bloor SJ, Markham KR, Ryan KG, Campbell BD, Jordan BR, Fountain DW (2000) Responses of nine Trifolium repens L. populations to ultraviolet-B radiation: Differential flavonol glycoside accumulation and biomass production. Ann Bot 86:527–537

    Article  CAS  Google Scholar 

  • Hughes MA, Conn EE (1976) Cyanoglucoside biosynthesis white clover (Trifolium repens). Phytochem 15:697–701

    Article  CAS  Google Scholar 

  • Huhman DV, Berhow MA, Sumner LW (2005) Quantification of saponins in aerial and subterranean tissues of Medicago truncatula. J Agric Food Chem 53:1914–1920

    Article  CAS  PubMed  Google Scholar 

  • Ingham JL (1977) Medicarpin as a phytoalexin of the genus Melilotus. Zeitsch Natur C 32:449–452

    Google Scholar 

  • Innocenti G, Piovan A, Filippini R, Caniato R, Cappelletti EM (1997) Quantitative recovery of furanocoumarins from Psoralea bituminosa. Phytochem Anal 8:84–86

    Article  CAS  Google Scholar 

  • Jonker A, Yu P (2017) The occurrence, biosynthesis, and molecular structure of proanthocyanidins and their effects on legume forage protein precipitation, digestion and absorption in the ruminant digestive tract. Int J Mol Sci 18:1105. https://doi.org/10.3390/ijms18051105

    Article  CAS  PubMed Central  Google Scholar 

  • Kagan IA, Goff BM, Flythe MD (2015) Soluble phenolic compounds in different cultivars of red clover and alfalfa, and their implication for protection against proteolysis and ammonia production in ruminants. Nat Prod Comm 10:1263–1267

    Google Scholar 

  • Kang SS, Woo WS (1988) Melilotigenin, a new sapogenin from Melilotus officinalis. J Nat Prod 51:335–338

    Article  CAS  Google Scholar 

  • Kang LP, Zhao Y, Pang X, Yu HS, Xiong CQ, Zhang J, Gao Y, Yu K, Liu C, Ma BP (2013) Characterization and identification of steroidal saponins from the seeds of Trigonella foenum-graecum by ultra high-performance liquid chromatography and hybrid time-of-flight mass spectrometry. J Pharm Biomed Anal 74:257–267

    Article  CAS  PubMed  Google Scholar 

  • Kapusta I, Stochmal A, Perrone A, Piacente S, Pizza C, Oleszek W (2005) Triterpene saponins from barrel medic (Medicago truncatula) aerial parts. J Agric Food Chem 53:2164–2170

    Article  CAS  PubMed  Google Scholar 

  • Karimi E, Oskoueian E, Oskoueian A, Omidvar V, Hendra R, Nazeran H (2013) Insight into the functional and medicinal properties of Medicago sativa (alfalfa) leaves extract. J Med Plants Res 7:290–297

    Google Scholar 

  • Khodakov GV, Akimov YA, Shashkov AS, Kintia PK, Grishkovets VI (1996) Triterpene and steroid saponins isolated from two Melilotus species. Adv Experim Med Biol Vol 405 Saponins Used in Food and Agriculture. Waller GR Yamasaki K Eds, Plenum Press New York and London 97–109.

  • Kicel A, Wolbis M (2012) Study of the phenolic constituents of the flowers and leaves of Trifolium repens L. Nat Prod Res 26:2050–2054

    Article  CAS  PubMed  Google Scholar 

  • Kicel A, Wolbis M (2013) Phenolic content and DPPH radical scavenging activity of the flowers and leaves of Trifolium repens. Nat Prod Comm 8:99–102

    CAS  Google Scholar 

  • Kirkbride JHJ (1999) In: Lotus systematics and distribution. Beuselinck PR (Ed), Trefoil: The science and technology of Lotus. Crop Science Society of America Special Publication, Madison, Wisconsin, USA, pp.1–20

  • Klejdus B, Vitamvasova-Sterbova D, Kuban V (2001) Identification of isoflavone conjugates in red clover (Trifolium pratense) by liquid chromatography-mass spectrometry after two-dimensional solid-phase extraction. Anal Chim Acta 450:81–97

    Article  CAS  Google Scholar 

  • Kolodziejczyk-Czepas J (2016) Trifolium species—the latest findings on chemical profile, ethnomedicinal use and pharmacological properties. J Pharm Pharmacol 68:845–861

    Article  CAS  PubMed  Google Scholar 

  • Kolodziejczyk-Czepas J, Sieradzka M, Wachowicz B, Nowal P, Oleszek W, Stochmal A (2016) The anti-adhesive and anti-aggregatory effects of phenolics from Trifolium species in vitro. Mol Cell Biochem 412:155–164

    Article  CAS  PubMed  Google Scholar 

  • Koul B, Taak P, Kumar A, Kumar A, Sanyal I (2019) Genus Psoralea: a review of the traditional and modern uses, phytochemistry and pharmacology. J Ethnoparm 232:201–226

    Article  CAS  Google Scholar 

  • Koupai-Abyazani MR, McCallum J, Muir AD, Bohm BA, Towers GHN, Gruber MY (1993) Developmental changes in the composition of proanthocyanidins from leaves of sainfoin (Onobrychis viciifolia Scop.) as determined by HPLC analysis. J Agric Food Chem 41:1066–1070

    Article  CAS  Google Scholar 

  • Kowalska I, Stochmal A, Kapusta I, Janda B, Pizza C, Piacente S, Oleszek W (2007) Flavonoids from barrel medic (Medicago truncatula) aerial parts. J Agric Food Chem 55:2645–2652

    Article  CAS  PubMed  Google Scholar 

  • Krenn L, Unterrieder I, Ruprechter R (2002) Quantification of isoflavones in red clover by high-performance liquid chromatography. J Chrom B 777:123–128

    Article  CAS  Google Scholar 

  • Lake BG (1999) Coumarin metabolism, toxicity and carcinogenicity: relevance for human risk assessment. Food Chem Toxicol 37:423–453

    Article  CAS  PubMed  Google Scholar 

  • Lemežienė N, Padarauskas A, Butkutė B, Cesevičienė J, Taujenis L, Norkevičienė E, Mikaliūnienė J (2015) The concentration of isoflavones in red clover (Trifolium pratense L.) at flowering stage. Zemdir Agric 102:443–448

    Article  Google Scholar 

  • Lesins KA, Lesins I (1979) Genus Medicago (Leguminosae). A taxogenetic study. Junk W Ed, Kluwer, Boston, MA, 199–201

  • Li Y, Tanner G, Larkin P (1996) The DMACA-HCl protocol and the threshold proanthocyanidins content for bloat safety forage legumes. J Sci Food Agric 70:89–101

    Article  CAS  Google Scholar 

  • Li Y, Liang W, Zhang X, Liu F, Xiaohong Z (2005) Allelopathic activity of root saponins of alfalfa on wheat, corn and barnyardgrass. Allelopathy J 15:119–124

    Google Scholar 

  • Lin LZ, He XG, Lindenmaier M, Yang J, Cleary M, Qui SX, Cordell GA (2000) LC-ESI-MS study of the flavonoid glycoside malonates of red clover (Trifolium pratense). J Agric Food Chem 48:354–365

    Article  CAS  PubMed  Google Scholar 

  • Liu XG, Huang MY, Gao PY, Liu CF, Sun YQ, Lv MC, Yao GD, Zhang LX, Li DQ (2018) Bioactive constituents from Medicago sativa L. with antioxidant, neuroprotective and acetylcholinesterase inhibitory activities. J Funct Foods 45:371–380

    Article  CAS  Google Scholar 

  • Liu XG, Lv MC, Huang MY, Sun YQ, Gao PY, Li DQ (2019) A network pharmacology study on the triterpene saponins from Medicago sativa L. for the treatment of neurodegenerative diseases. J Food Biochem. https://doi.org/10.1111/jfbc.12955

    Article  PubMed  Google Scholar 

  • Llorent-Martinez E, Spinola V, Gouveia S, Castilho PP (2015) HPLC-ESI-MS characterization of phenolic compounds, terpenoid saponins, and other minor compounds in Bituminaria bituminosa. Ind Crop Prod 69:80–90

    Article  CAS  Google Scholar 

  • Lu Y, Sun Y, Foo Y, McNabb WC, Molan AL (2000) Phenolic glycosides of forage legume Onobrychis viciifolia. Phytochem 55:67–75

    Article  CAS  Google Scholar 

  • Ma QG, Li T, Wei RR, Liu WM, Sang ZP, Song ZW (2016) Characterization of chalcones from Medicago sativa L. and their hypolipidemic and antiangiogenic activities. J Agric Food Chem 64:8138–8145

    Article  CAS  PubMed  Google Scholar 

  • Maegher LP, Lane G, Sivakumaran S, Tavendale MH, Fraser K (2004) Characterization of condensed tannins from Lotus species by thiolytic degradation and electrospray mass spectrometry. Anim Feed Sci Technol 117:151–163

    Article  CAS  Google Scholar 

  • Maegher LP, Widdup K, Sivakumaran S, Lucas R, Rumball W (2006) Floral Trifolium proanthocyanidins: polyphenol formation and compositional diversity. J Agric Food Chem 54:5482–5488

    Article  CAS  Google Scholar 

  • Maestrini M, Tava A, Mancini S, Tedesco D, Perrucci S (2020) In vitro anthelmintic activity of saponins from Medicago spp. against sheep gastrointestinal nematodes. Molecules. https://doi.org/10.3390/molecules25020242

    Article  PubMed  PubMed Central  Google Scholar 

  • Malisch CS, Lüscher A, Baert N, Engström MT, Studer B, Fryganas C, Suter D, Mueller-Harvey I, Salminen JP (2015) Large variability of proanthocyanidin content and composition in sainfoin (Onobrychis viciifolia). J Agric Food Chem 63:10234–10242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marais JPJ, Mueller-Harvey I, Brandt EV, Ferreira D (2000) Polyphenols, condensed tannins and other natural products in Onobrychis viciifolia (sainfoin). J Agric Food Chem 48:3440–3447

    Article  CAS  PubMed  Google Scholar 

  • Maravcová J, Kleinová T, Loučka R, Tyrolová I, Kvasnička F, Dušek M, Čeřvoský M, Matucha P (2004) Coumestrol content in lfalfa following ensilage. An Feed Sci Technol 115:159–167

    Article  CAS  Google Scholar 

  • Marczak Ł, Stobiecki M, Jasiński M, Oleszek W, Kachlicki P (2010) Fragmentation pathways of acylated flavonoid diglucuronides from leaves of Medicago truncatula. Phytochem Anal 21:224–233

    Article  CAS  PubMed  Google Scholar 

  • Marrelli M, Morrone F, Argentieri MP, Gambacorta L, Conforti F, Avato P (2018) Phytochemical and biological profile of Moricandia arvensis (L.) DC: an inhibitor of pancreatic lipase. Molecules. https://doi.org/10.3390/molecules23112829

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin LM, Castilho MC, Silveira MI, Abren JM (2006) Liquid chromatographic validation of a quantitation method for phytoestrogens, biochanin-A, coumestrol, daidzein, formononetin and genistein in lucerne. J Liq Chromatogr Relat Technol 29:2875–2884

    Article  CAS  Google Scholar 

  • Massiot G, Lavaud C, Besson V, Le Men-Olivier L, van Binst G (1991) Saponins from aerial parts of alfalfa (Medicago sativa). J Agric Food Chem 39:78–82

    Article  CAS  Google Scholar 

  • Maul R, Kulling SE (2010) Absorption of red clover isoflavonesin human subjects: results from a pilot study. Brit J Nutrit 103:1569–1572

    Article  CAS  PubMed  Google Scholar 

  • McGorum BC, Pirie RS, Fry SC (2012) Quantification of cyanogenic glycosides in white clover (Trifolium repaens L.) from horse pastures in relation to equine grass sickness. Grass Forage Sci 67:274–279

    Article  CAS  Google Scholar 

  • Mehrafarin A, Quaderi A, Rezazadeh S, Naghdi BH, Noormohammadi G, Zand E (2010) Bioengineering of important secondary metabolites and metabolic pathways in fenugreek (Trigonella foenum-graecum L.) J Med Plants 9:1–18

  • Mohamed KM, Ohtani K, Kasai R, Yamasaki K (1995) Oleanane glycosides from seeds of Trifolium alexandrinum. Phytochem 40:1237–1242

    Article  CAS  Google Scholar 

  • Montanari R, Capelli D, Tava A, Galli A, Laghezza A, Tortorella P, Loiodice F, Pochetti G (2016) Screening of saponins and sapogenins from Medicago specie as potential PPARγ agonists and X-ray structure of the complex PPARγ/caulophyllogenin. Sci Rep 6:27658. https://doi.org/10.1038/srep27658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mueller M, Jungbauer A (2008) Red clover extract: a putative source for simultaneous treatment of menopausal disorders and the metabolic syndrome. Menopuse 15:1120–1131

    Article  Google Scholar 

  • Mueller-Harvey I, Bee G, Dohme-Meier F, Hoste H, Karonen M et al (2019) Benefits of condensed tannins in forage legumes fed to ruminants: importance of structure, concentration, and diet composition. Crop Sci 59:861. https://doi.org/10.2135/cropsci2017.06.0369

    Article  CAS  Google Scholar 

  • Murakami T, Kishi A, Matsuda H, Yoshikawa M (2000) Medicinal foodstuffs. XVII. Fenugreek seed. (3): Structures of new furostanol-type steroid saponins, trigoneosides Xa, Xb, XIb, XIIa, XIIb, and XIIIa, from the seeds of Egyptian Trigonella foenum-graecum L. Chem Pharm Bull 48:994–1000

    Article  CAS  Google Scholar 

  • Mustonen E, Touri M, Isolahti M, Taponen J, Vanhatalo A (2018) Variety, time of harvest and condition during growing season have impact on red clover isoflavone content. Agric Food Sci 27:102–109

    Article  CAS  Google Scholar 

  • Nair RM, Whittall A, Hughes SJ, Craig AD, Revell DK, Miller SM, Powell T, Auricht GC (2010) Variation in coumarin content of Melilotus species in South Australia. New Zeal J Agric Res 55:201–213

    Article  CAS  Google Scholar 

  • Nasser NM, Al-Ani MK (2014) Isolation of coumarin from Melilotus officinalis of Iraq. Pharm Glob 5:1–3

    Google Scholar 

  • Newman Y, Dubeux J (2017) Sweet clover production and use in Florida. ISAF extension SS-AGR-189/AG191

  • Niezen JH, Waghorn TS, Charleston WAG, Waghorn GC (1995) Grown and gastrointestinal nematode parasitism in lambs grazing either Lucerne (Medicago sativa) or sulla (Hedysarum coronarium) which contains condensed tannins. J Agric Sci 81:102–109

    Google Scholar 

  • Niezen JH, Charleston WAG, Robertson HA, Shelton D, Waghorn GC, Green R (2002) The effect of feeding sulla (Hedysarum coronarium) or lucerne (Medicago sativa) on lamb parasite burdens and development of immunity to gastrointestinal nematodes. Vet Parasitol 105:229–245

    Article  CAS  PubMed  Google Scholar 

  • Oleszek W (1993) Allelopathic potentials of alfalfa (Medicago sativa) saponins: their relation to antifungal and hemolytic activities. J Chem Ecol 19:1063–1074

    Article  CAS  PubMed  Google Scholar 

  • Oleszek W, Jurzysta M (1986) Isolation, chemical characterization and biological activity of red clover (Trifolium pratense L.) root saponins. Acta Soc Bot Pol 55:247–252

    Article  CAS  Google Scholar 

  • Oleszek W, Stochmal A (2002) Triterpene saponins and flavonoids in the seeds of Trifolium species. Phytochem 61:165–170

    Article  CAS  Google Scholar 

  • Oleszek W, Stochmal A, Janda B (2007) Concentration of isoflavones and other phenolics in the aerial parts of Trifolium species. J Agric Food Chem 55:8095–8100

    Article  CAS  PubMed  Google Scholar 

  • Pace V, Carbone K, Spirito F, Iacurto M, Terzano MG, Verna M, Vincenti F, Settineri D (2006) The effects of subterranean clover phytoestrogens on sheep growth, reproduction and carcass characteristics. Meat Sci 74:616–622

    Article  CAS  PubMed  Google Scholar 

  • Pang X, Kang LP, Yu HS, Zhao Y, Xiong CQ, Zhang J, Shan J, Ma BP (2012) Rapid isolation of new furostanol saponins from fenugreek seeds based on ultra-performance liquid chromatography coupled with a hybrid quadrupole time-of-flight tandem mass spectrometry. J Sep Sci 35:1538–1550

    Article  CAS  PubMed  Google Scholar 

  • Panter KE, Ralphs MH, Pfister JA, Gardner DR, Stegelmeier BL, Lee ST, Welch KD, Green BT, Davis TZ, Cook D U.S. (2011) In: Plant poisonus to livestock in the Western States. USDA Agric Res Ser, Agric Inf Bull No 415. https://www.ars.usda.gov/is/np/poisonousplants/poisonousplants

  • Pastorino G, Marchetti C, Borghesi B, Cornara L, Ribulla S, Burlando B (2017) Biological activities of the legume crops Melilotus officinalis and Lespedeza capitata for skin care and pharmaceutical applications. Ind Crop Prod 96:158–164

    Article  CAS  Google Scholar 

  • Patra AK, Min BR, Saxena J (2012) Dietary tannins on microbial ecology of the gastrointestinal tract in ruminants. In: Patra AK (ed) Dietary phytochemicals and microbes. Springer Science+Business Media Dordrecht, pp 237–262. Doi: https://doi.org/10.1007/978-94-007-3926-0_8

  • Pecetti L, Tava A, Romani M, De Benedetto MG, Corsi P (2006) Variety and environment effects on the dynamics of saponins in lucerne (Medicago sativa L.). Eur J Agron 25:187–192

    Article  CAS  Google Scholar 

  • Pecetti L, Tava A, Pagnotta MA, Russi L (2007) Variation in forage quality and chemical composition among accessions of Bituminaria bituminosa (L.) Stirt. from Italy. J Sci Food Agric 87:985–991

    Article  CAS  Google Scholar 

  • Pecetti L, Biazzi E, Tava A (2010) Variation in saponin content during the growing season of spotted medic [Medicago arabica L. (Huds.)]. J Sci Food Agric 90:2405–2410

    Article  CAS  PubMed  Google Scholar 

  • Pecetti L, Mella M, Tava A (2016) Variation in herbage biochemical composition among pich trefoil (Bituminaria bituminosa) populations from Elba Island, Italy. J Agric Food Chem 64:195–203

    Article  CAS  PubMed  Google Scholar 

  • Petit P, Sauvaire Y, Ponsin G, Manteghetti M, Fave A, Ribes G (1993) Effects of a fenugreek seed extract on feeding behaviour in the rat: metabolic-endocrine correlates. Pharmacol Biochem Behav 45:369–374

    Article  CAS  PubMed  Google Scholar 

  • Piano E, Pecetti L (2010) Minor legume species. In: Boller B, Posselt UK, Veronesi F (eds) Fodder crops and amenity grasses—Handbook of plant breeding series, vol 5. Springer, New York, NY, pp 477–500

    Chapter  Google Scholar 

  • Piluzza G, Bullitta S, Deroma M, Odoardi M (2000) The accumulation of condensed tannins in local populations of sulla. Cah Opt Medit 45:199–202

    Google Scholar 

  • Piluzza G, Sulas L, Bullitta S (2013) Tannins in forage plants and their role in animal husbandry and environmental sustainability: a review. Grass Forage Sci 69:32–48

    Article  CAS  Google Scholar 

  • Pistelli L, Nccioli C, Appendino G, Bianchi F, Sterner O, Ballero M (2003) Pterocarpans from Bituminaria morisiana and Bituminaria bituminosa. Phytochem 64:595–598

    Article  CAS  Google Scholar 

  • Pollier J, Moses T, Gonzallez-Guzman M, De Geyter N, Lippens S, Vanden Bossche R, Marhavy P, Kremer A, Morreel K, Guerin CJ, Tava A, Oleszek W, Thevelein JM, Campos N, Goormachtig S, Goossens A (2013) The protein quality control system manages plant defense compound synthesis. Nature 504:148–152. https://doi.org/10.1038/nature12685

    Article  CAS  PubMed  Google Scholar 

  • Porter L J (1988) Flavans and proanthocyanidins. In: Harborne JB Ed. The flavonoids: Advances in research since 1980. Springer, Boston, MA. p. 21–62. doi: https://doi.org/10.1007/978-1-4899-2913-6_2

  • Poutaraud A, Michelot-Antalik A, Plantureux S (2017) Grasslands: a source of secondary metabolites for livestock health. J Agric Food Chem 65:6535–6553

    Article  CAS  PubMed  Google Scholar 

  • Quiros FC, Bauchan GR (1988) The genus Medicago and the origin of the Medicago sativa complex. In: Hanson AA, Barnes DK, Hill RR (eds) Alfalfa and alfalfa improvement, Agronomy – a series of monography nr 29. ASA, CSSA, SSSA, Madison, WI, pp 93–124

    Google Scholar 

  • Rafińska K, Pomastowski P, Wrona O, Górecki R, Buszewski B (2017) Medicago sativa as a source of secondary metabolites for agriculture and pharmaceutical industry. Phytochem Letters 20:520–539

    Article  CAS  Google Scholar 

  • Ramos GP, Dias PMB, Morais CB, Fröehlich PE, Dall’Agnol M, Zuanazzi JAS, (2008) LC determination of four isoflavone aglycones in red clover (Trifolium pratense L.). Chromatogr 67:125–129

    Article  CAS  Google Scholar 

  • Reed KFM (2016) Fertility of herbivores consuming phytoestrogen containing Medicago and Trifolium species. Agriculture 6:35

    Article  Google Scholar 

  • Regos I, Urbanella A, Treutter D (2009) Identification and quantification of phenolic compounds from the forage legume sainfoin (Onobrychis viciifolia). J Agric Food Chem 57:5843–5852

    Article  CAS  PubMed  Google Scholar 

  • Reynaud J, Lussignol M (2005) The flavonoids in Lotus corniculatus. Lotus Newslett 35:75–82

    Google Scholar 

  • Riasat M, Heidaria B, Pakniyata H, Jafaric AA (2018) Assessment of variability in secondary metabolites and expected response to genotype selection in fenugreek (Trigonella spp.). Ind Crop Prod 123:221–231

    Article  CAS  Google Scholar 

  • Rietjens IMCM, Louisse J, Beekmann K (2017) The potential health effects of dietary phytoestrogens. Brit J Pharmacol 174:1263–1280

    Article  CAS  Google Scholar 

  • Rodrigues F, Almeida I, Sarmento B, Amaral MH, Oliveira MBPP (2014) Study of the isoflavone content of different extracts of Medicago spp. as potential active ingredient. Ind Crops Prod 57:110–115

    Article  CAS  Google Scholar 

  • Ropiak HM, Lachmann P, Ramsay A, Green RJ, Mueller-Harvey I (2017) Identification of structural features of condensed tannins that affect protein aggregation. PLoS ONE 12:e0170768. https://doi.org/10.1371/journal.pone.0170768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sabudak T, Guler N (2009) Trifolium L. – A review on its phytochemical and pharmaceutical profile. Phytoter Res 23:439–446

    Article  CAS  Google Scholar 

  • Sadowska B, Budzynska W-S, Paszkiewicz M, Stochmal A, Moniuszko-Szajwaj B, Kowalczyk M, Rozalska B (2014) New pharmacological properties of Medicago sativa and Saponaria officinalis saponin-rich fractions addressed to Candida albican. J Med Microbiol 63:1076–1086

    Article  PubMed  Google Scholar 

  • Sakamoto S, Kofuji S, Kuroyanagi M, Ueno A, Sekita S (1992) Saponins from Trifolium repens. Phytochem 31:1773–1777

    Article  CAS  Google Scholar 

  • Saviranta NMM, Anttonen MJ, von Wright A, Karjalainen RO (2008) Red clover (Trifolium pratense L.) isoflavones: determination of concentration by plant stage, flower colour, plant part and cultivar. J Sci Food Agric 88:125–132

    Article  CAS  Google Scholar 

  • Saviranta NMM, Julkunen-Tiitto R, Oksanen E, Karjalainen RO (2010) Leaf phenolic compounds in red clover (Trifolium pratense L.) induced by exposure to moderately elevated ozone. Environ Poll 158:440–446

    Article  CAS  Google Scholar 

  • Scharenberg A, Arrigo Y, Gutzwiller A, Soliva CR, Wyss U, Kreuzer M, Dohme F (2007) Palatability in sheep and in vitro nutritional value of dried and ensiled sainfoin (Onobrychis viciifolia) birdsfoot trefoil (Lotus corniculatus), and chicory (Cichorium intybus). Arch Anim Nutr 61:481–496

    Article  CAS  PubMed  Google Scholar 

  • Schreiner M, Mewis I, Huyskens-Keil S, Jansen MAK, Zrenner R, Winkler JB, O’Brien N, Krumbein A (2012) UV-B-induced secondary plant metabolites—Potential benefits for plant and human health. Crit Rev Plant Sci 31:229–240. https://doi.org/10.1080/07352689.2012.664979

    Article  CAS  Google Scholar 

  • Schreurs NM, Tavendale MH, Lane GA, Barry TN, Lopez-Villalobos N, McNabb WC (2007) Effect of different condensed tannin-containing forages, forage maturity and nitrogen fertiliser application on the formation of indole and skatole in in vitro rumen fermentation. J Sci Food Agric 87:1076–1087

    Article  CAS  Google Scholar 

  • Seguin P, Zheng W, Souleimanov A (2004) Alfalfa phytoestrogen content: impact of plant maturity and herbage components. J Agron Crop Sci 190:211–217

    Article  CAS  Google Scholar 

  • Setchell KDR, Brown NM, Desai P, Zimmer-Nechemias L, Wolfe BE, Brashear WT, Kirschner AS, Cassidy A, Heubi JE (2001) Bioavailability of pure isoflavones in healthy humans and analysis of commercial soy isoflavone supplements. J Nutrit 131:1362S-1375S

    Article  CAS  PubMed  Google Scholar 

  • Shehata MN, Hassan A, El-Shazly K (1982) Identification of the oestrogenic isoflavones in fresh and fermented berseem clover (Trifolium alexandrinum). Austr J Agric Res 33:951–956

    Article  CAS  Google Scholar 

  • Silva LR, Pereira MJ, Azevedo J, Gonçalves RF, Valentão P, Guedes de Pinho P, Andrade PB (2013) Glycine max (L.) Merr., Vigna radiata L. and Medicago sativa L. sprouts: a natural source of bioactive compounds. Food Res Int 50:167–175

    Article  CAS  Google Scholar 

  • Sivakumaran S, Maegher LP, Ly F, Lane Ga, Fraser K, Rumball W (2004) Floral procyanidins of the forage legume red clover (Trifolium pratense L.). J Agric Food Chem 52:1581–1585

    Article  CAS  PubMed  Google Scholar 

  • Sivakumaran S, Rumball W, Lane GA, Fraser K, Foo LY, Yu M, Maegher LP (2006) Variation of proanthocyanidins in Lotus species. J Chem Ecol 32:1797–1816

    Article  CAS  PubMed  Google Scholar 

  • Sivesind E, Seguin P (2005) Effects of the environment, cultivar, maturity, and preservation method on red clover isoflavone concentration. J Agric Food Chem 53:6397–6402

    Article  CAS  PubMed  Google Scholar 

  • Smith GR, Randel RD, Bradshaw C (1986) Influence of harvest date, cultivar, and simple storage method on concentration of isoflavones in subterranean clover. Crop Sci 26:1013–1016

    Article  CAS  Google Scholar 

  • Srinivasan K (2006) Fenugreek (Trigonella foenum-graecum): a review of helth beneficial physiological effects. Food Rev Int 22:203–224

    Article  CAS  Google Scholar 

  • Sroka Z, Jurzysta M, Tylcz J, Rzadkowska-Bodalska H (1997) Stimulation of pancreatic lipase activity by saponins isolated from Medicago sativa L. Z. Naturforsch. 52c:235–239

  • Steele HL, Werner D, Cooper JE (1999) Flavonoids in seed and root exudates of Lotus pedunculatus and their transformation by Mesorhizobium loti. Physiol Plant 107:251–258

    Article  CAS  Google Scholar 

  • Stochmal A, Oleszek W (1994) Determination of cyanogenic glucosides in white clover (Trifolium repens L.) by high performance liquid chromatography. Phytochem Anal 5:271–272

    Article  Google Scholar 

  • Stochmal A, Oleszek W (1997) Changes of cyanogenic glucosides in white clover (Trifolium repens L.) during the growing season. J Agric Food Chem 45:4333–4336

    Article  CAS  Google Scholar 

  • Stochmal A, Oleszek W (2007) Seasonal and structural changes of flavones in alfalfa (Medicago sativa) aerial parts. J Food Agric Environ 5:84–88

    Google Scholar 

  • Stochmal A, Piacente S, Pizza C, De Riccardis F, Leitz R, Oleszek W (2001a) Alfalfa (Medicago sativa L.) flavonoids. 1. Apigenin and luteolin glycosides from aerial parts. J Agric Food Chem 49:753–758

    Article  CAS  PubMed  Google Scholar 

  • Stochmal A, Simonet AM, Macias FA, Oleszek W (2001b) Alfalfa (Medicago sativa L.) flavonoids. 2. Tricin and chrysoeriol glycosides from aerial parts. J Agric Food Chem 49:5310–5314

    Article  CAS  PubMed  Google Scholar 

  • Stochmal A, Simonet AM, Macias FA, Oliveira MA, Abreu JM, Nash R, Oleszek W (2001c) Acylated apigenin glycosides from alfalfa (Medicago sativa L.) var. Artal Phytochemistry 57:1223–1226

    Article  CAS  PubMed  Google Scholar 

  • Stringano E, Carbonero CH, Smith LMJ, Brown RH, Mueller-Harvey I (2012) Proanthocyanidin diversity in the EU ‘HealthyHay’ sainfoin (Onobrychis viciifolia) germplasm collection. Phytochem 77:197. https://doi.org/10.1016/j.phytochem.2012.01.013

    Article  CAS  Google Scholar 

  • Sun N-N, Wu T-Y, Chau C-F (2016) Natural dietary and herbal products in anti-obesity treatment. Molecules. https://doi.org/10.3390/molecules21101351

    Article  PubMed  PubMed Central  Google Scholar 

  • Tava A, Annicchiarico P (2000) Spectrophotometer-aided evaluation of cyanogenic potential in white clover (Trifolium repens L.). Phytochem Anal 11:169–173

    Article  CAS  Google Scholar 

  • Tava A, Avato P (2006) Chemical and biological activity of triterpene saponins from Medicago species. Nat Prod Comm 1:1159–1180

    CAS  Google Scholar 

  • Tava A, Pecetti L (2012) Chemical investigation of saponins from twelve Medicago species and their bioassay with the brine shrimp Artemia salina. Nat Prod Comm 7:837–840

    CAS  Google Scholar 

  • Tava A, Mella M, Avato P, Argentieri MP, Bialy Z, Jurzysta M (2005a) Triterpenoid glycosides from the leaves of Medicago arborea L. J Agric Food Chem 53:9954–9965

    Article  CAS  PubMed  Google Scholar 

  • Tava A, Pecetti L, Bertoli A, Piano E (2006) Oestrogenic isoflavone content in natural strains of subterranean clover (Trifolium subterraneum L.) from Sardinia. Nat Prod Comm 1:557–562

    CAS  Google Scholar 

  • Tava A, Pecetti L, Ricci M, Pagnotta MA, Russi L (2007) Volatile compounds from leaves and flowers of Bituminaria bituminosa (L.) Stirt. from Italy. Flav Fragr J 22:363–370

    Article  CAS  Google Scholar 

  • Tava A, Mella M, Avato P, Biazzi E, Pecetti L, Bialy Z, Jurzysta M (2009) New triterpenic saponins from the aerial parts of Medicago arabica (L.) Huds. J Agric Food Chem 57:2826–2835

    Article  CAS  PubMed  Google Scholar 

  • Tava A, Pecetti L, Romani M, Mella M, Avato P (2011a) Triterpenoid glycosides from the leaves of two cultivars of Medicago polymorpha L. J Agric Food Chem 59:6142–6149

    Article  CAS  PubMed  Google Scholar 

  • Tava A, Scotti C, Avato P (2011b) Biosynthesis of saponins in the genus Medicago. Phytochem Rev 10:459–469

    Article  CAS  Google Scholar 

  • Tava A, Pecio Ł, Stochmal A, Pecetti L (2015) Clovamide and flavonoids from leaves of Trifolium pratense and T. pratense subsp. nivale grown in Italy. Nat Prod Comm 10:933–936

    Google Scholar 

  • Tava A, Stochmal A, Pecetti L (2016) Isoflavone content in subterranean clover germplasm from Sardinia. Chem Biodiv 13:1038–1045

    Article  CAS  Google Scholar 

  • Tava A, Pecio Ł, Lo Scalzo R, Stochmal A, Pecetti L (2019) Phenolic content and antioxidant activity in Trifolium germplasm from different environments. Molecules. https://doi.org/10.3390/molecules24020298

    Article  PubMed  PubMed Central  Google Scholar 

  • Tava A, De Benedetto MG, Tedesco D, Di Miceli G, Piluzza G (2005b) Proanthocyanidins from Hedisarum, Lotus and Onobrychis spp. Growing in Sardinia and Sicily and their antioxidant activity. Proc. XX Int Grass Congr Dublin, Ireland p. 271

  • Tava A, Biazzi E, Ronga D, Mella M, Doria F, D’Addabbo T, Candido V, Avato P (2021) Chemical identification of specialized metabolites from sulla (Hedysarum coronarium L.) collected in southern Italy. Molecules 26:4606. https://doi.org/10.3390/molecules26154606

  • Taylor W, Zaman MS, Mir Z, Mir PS, Acharya SN, Mears GJ, Elder JL (1997) Analysis of steroidal sapogenins from amber fenugreek (Trigonella foenum-graecum) by capillary gas chromatography and combined gas chromatography/mass spectrometry. J Agric Food Chem 45:753–759

    Article  CAS  Google Scholar 

  • Tibe O, Maegher LP, Fraser K, Harding DRK (2011) Condensed tannins and flavonoids from the forage legume sulla (Hedysarum coronarium). J Agric Food Chem 59:9402–9409

    Article  CAS  PubMed  Google Scholar 

  • Timbekova AE, Isaev MI, Abubakirov NK (1996) Chemistry and biological activity of triterpenoid glycosides from Medicago sativa. In Advances in experimental medicine and biology. Saponins used in food and agriculture. Vol 405, Waller GR and Yamasaki K (Eds) Plenum Press, New York, 171–182

  • Tsao R, Papadopoulos Y, Yang R, Young JC, McRae K (2006) Isoflavone profiles of red clovers and their distribution in different parts harvested at different growing stages. J Agric Food Chem 54:5797–5805

    Article  CAS  PubMed  Google Scholar 

  • Tucak M, Čupić T, Horvat D, Popović S, Krizmanić G, Ravlić M (2020) Variation of phytoestrogen content and major agronomic traits in alfalfa (Medicago sativa L.) populations. Agronomy 10:87

  • Upton R, Romm A, Swisher D (2017) Red clover flowering tops, aerial parts and dry extracts Trifolium pratense L. Standards of identity, analysis and quantity control. Am Herbal Pharmacopoeia, Scotts Valley, USA, 1–76.

  • Van de Weijer PHM, Barentsen R (2002) Isoflavones from red clover (Promensil®) significantly reduce menopausal hot flush symptoms compared to placebo. Maturitas 42:187–193

    Article  PubMed  Google Scholar 

  • Ventura MR, Flores MP, Castanon JIR (1999) Nutritive value of forage shrubs: Bituminaria bituminosa, Acacia salicina and Medicago arborea. Cha Opt Med 39:171–173

    Google Scholar 

  • Ventura MR, Mendez P, Flores MP, Rodriguez R, Castanon JIR (2000) Energy and protein content of Tedera (Bituminaria bituminosa). Cha Opt Med 45:219–221

    Google Scholar 

  • Veronesi F, Brummer EC, Huyghe C (2010) Alfalfa. In: Boller B, Posselt UK, Veronesi F (eds) Fodder crops and amenity grasses - Handbook of plant breeding series, vol 5. Springer, New York, NY, pp 395–438

    Chapter  Google Scholar 

  • Vetter J (1995) Isoflavones in different parts of common Trifolium species. J Agric Food Chem 43:106–108

    Article  CAS  Google Scholar 

  • Vickery PJ, Wheeler JL, Mulcahy C (1987) Factors affecting the hydrogen cyanide potential of white clover (Trifolium pratense L.). Austr J Agric Res 38:1053–1059

    Article  CAS  Google Scholar 

  • Viladomat F, Bastida J (2015) General overview of plant secondary metabolism. In Plant biology and biotechnology. Vol. I: Plant diversity, organization, function and improvement, 1st ed.; Springer: Berlin, 539–568

  • Visnevschi-Necrasov T, Faria MA, Cunha SC, Harris J, Meimberg HWE, Curto MAC, Pereira MG, Oliveira MBPP, Nunes E (2013) Isoflavone synthase (ISF)gene phylogeny in Trifolium species associated with plant isoflavone contents. Plant System Evol 299:357–367

    Article  CAS  Google Scholar 

  • Visnevschi-Necrasov T, Barreira JCM, Cunha SC, Pereira G, Nunes E, Oliveira MBPP (2015) Advances in isoflavone profile characterization using matrix solid-phase dispersion coupled to HPLC/DAD in Medicago species. Phytochem Anal 26:40–46

    Article  CAS  PubMed  Google Scholar 

  • Vlaisavljević S, Kaurinović B, Popović M, Vasiljević S (2017) Profile of phenolic compounds in Trifolium pratense L. extracts at different growth stages and their biological activities. Int J Food Prop 20:3090–3101

    Article  CAS  Google Scholar 

  • Wang Y, McAllister TA, Acharya S (2015) Condensed tannins in sainfoin: composition, concentration and effects on nutritive and feeding value of sainfoin forage. Crop Sci 55:13–22

    Article  CAS  Google Scholar 

  • Wang J, Jiang W, Liu Z, Fu T, Wang Y (2017b) Analysis and identification of chemical constituents of fenugreek by UPLC-IT-MSn and UPLC-Q-TOF-MS. Chem Res Chin Univ 33:721–730

    Article  CAS  Google Scholar 

  • Wang RL, Liu SW, Xin XW, Chen S, Peng GX, Su YJ, Song ZK (2017a) Phenolic acids contents and allelopathic potential of 10-cultivars of alfalfa and their bioactivity Allelopathy J 40:63–70

  • Wani SA, Kumar P (2018) Fenugreek: a review on its nutraceutical properties and utilization in various food products. J Saudi Soc Agric Sci 17:97–106

    Google Scholar 

  • Wolff LP, Martins MR, Bedone AJ, Monteiro IM (2006) Endometrial Evaluation in Menopausal Women after Six Months of Isoflavones. Rev Ass Med Bras 52:419–423

    Article  Google Scholar 

  • Wu Q, Wang M, Simon JE (2003) Determination of isoflavones in red clover and related species by high-performance liquid chromatography combined with ultraviolet and mass spectrometric detection. J Chrom A 1016:195–209

    Article  CAS  Google Scholar 

  • Yadav UCS, Baquer NZ (2014) Pharmacological effects of Trigonella foenum-graecum L. in health and disease. Pharma Biol 52:243–254

    Article  Google Scholar 

  • Yadav M, Tomar R, Prasad GBKS, Jain S, Yadav H (2008) Complementary hypoglycemic and anti-hyperglycemic activity of various extracts of fenugreek seeds in rats. Asian J Biochem 3:182–187

    Article  CAS  Google Scholar 

  • Yokoyama S, Kodera M, Hirai A, Nakada M, Ueno Y, Osawa T (2020) Red clover (Trifolium pratense L.) prevents metabolic syndrome. J Nutr Sci Vitaminol 66:48–53

    Article  CAS  PubMed  Google Scholar 

  • Zeller WE, Sullivan ML, Mueller-Harvey I, Grabber JH, Ramsay A, Drake C, Brown RH (2015) Protein precipitation behavior of condensed tannins from Lotus pedunculatus and Trifolium repens with different mean degrees of polymerization. J Agric Food Chem 63:1160. https://doi.org/10.1021/jf504715p

    Article  CAS  PubMed  Google Scholar 

  • Zeng J, Huang T, Xue M, Chen J, Feng L, Du R, Feng Y (2018) Current knowledge and development of hederagenin as a promising medicinal agent: a comprehensive review. RSC Adv 8:24188–24202

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang J, Di H, Lou K, Jahufer Z, Wu F, Duan Z, Stewart A, Yan Z, Wang Y (2018) Coumarin content, morphological variation and molecular phylogenetics of Melilotus. Molecules 23:810. https://doi.org/10.3390/molecules23040810

    Article  CAS  PubMed Central  Google Scholar 

  • Zobel AM, Brown SA, March RE (1991) Histological localization of psoralens in fruits of Psoralea bituminosa. Can J Bot 69:1673–1678

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. CREA Research Centre for Animal Production and Aquaculture, viale Piacenza 29, 26900, Lodi, Italy

    Aldo Tava, Elisa Biazzi & Luciano Pecetti

  2. Pharmacy Department, University of Salerno, via Giovanni Paolo II 132, 84084, Fisciano, SA, Italy

    Domenico Ronga

  3. Department of Pharmacy – Drug Science, University of Bari Aldo Moro, via Orabona 4, 70125, Bari, Italy

    Pinarosa Avato

Authors
  1. Aldo Tava
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elisa Biazzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Domenico Ronga
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luciano Pecetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pinarosa Avato
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aldo Tava.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tava, A., Biazzi, E., Ronga, D. et al. Biologically active compounds from forage plants. Phytochem Rev 21, 471–501 (2022). https://doi.org/10.1007/s11101-021-09779-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11101-021-09779-9

Keywords

Search

Navigation