Extracts of forage plants affect the developmental competence of ovine oocytes in vitro
Anna Aryani Amir A B , Jennifer M. Kelly C , David O. Kleemann C , Zoey Durmic A , Dominique Blache A and Graeme B. Martin A DA UWA Institute of Agriculture and UWA School of Agriculture and Environment, The University of Western Australia, Crawley, WA 6009, Australia.
B Institute of Tropical Agriculture and Food Security, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia.
C South Australian Research and Development Institute, Turretfield Research Centre, Rosedale, SA 5350, Australia.
D Corresponding author. Email: graeme.martin@uwa.edu.au
Animal Production Science 59(10) 1814-1819 https://doi.org/10.1071/AN18170
Submitted: 26 December 2017 Accepted: 23 January 2019 Published: 7 March 2019
Abstract
Forage plants may contain secondary compounds that disrupt reproduction in ruminants so, as ‘duty of care’, proposed new forage species need to be tested for harmful effects on reproduction before industrial release. We evaluated the effects of Bituminaria bituminosa, Medicago sativa, Chicorium intybus, Trifolium subterraneum, Trifolium pratense, Biserrula pelecinus and Eremophila glabra, on the in vitro developmental competence of ovine oocytes. Crude methanolic extracts of each plant were added to the medium (final concentrations: 0, 50 or 100 μg dry extract per mL) used for in vitro maturation of cumulus-oocyte complexes derived from abattoir-sourced adult ewe ovaries. After in vitro fertilisation, we quantified cleavage rate, blastocyst rate, hatching rate, blastocyst efficiency, and total blastocyst cell number (TCN). Extract from B. pelecinus, at 50 μg/mL concentration, increased cleavage rate at (P < 0.05), and at 100 μg/mL, increased blastocyst rate and efficiency (P < 0.05). The other plant extracts did not affect these measures. TCN was affected by stage of development and treatment, but not by the interaction between stage and treatment. Within treatments, TCN was increased by C. intybus (at both 50 and 100 μg/mL) but decreased by M. sativa (at both 50 and 100 μg/mL; P < 0.05). We conclude that methanolic extracts of forage plants, present during in vitro oocyte maturation, did not disrupt subsequent fertilisation and embryo development until the blastocyst stage. On the contrary, B. pelecinus appears to improve fertilisation and embryo development. Overall, these observations suggest that these plants will not disrupt in vivo oocyte maturation but further testing is still required, especially for the other stages of the reproductive process.
Additional keywords: blastocyst, cell number, oocytes, plant extracts.
References
Adams NR (1995) Detection of the effects of phytoestrogens on sheep and cattle. Journal of Animal Science 73, 1509–1515.| Detection of the effects of phytoestrogens on sheep and cattle.Crossref | GoogleScholarGoogle Scholar | 7665383PubMed |
Amir AA, Kelly JK, Kleemann DO, Durmic Z, Blache D, Martin GB (2018) Phyto-oestrogens affect fertilization and embryo development in vitro in sheep. Reproduction, Fertility and Development 30, 1109–1115.
Banik B, Durmic Z, Erskine W, Ghamkar K, Revell C (2013) In vitro ruminal fermentation and methane production differ in selected key pasture species in Australia. Crop and Pasture Science 64, 935–942.
| In vitro ruminal fermentation and methane production differ in selected key pasture species in Australia.Crossref | GoogleScholarGoogle Scholar |
Barnes FL (2000) In vitro maturation and developmental competence of human primary oocytes. In ‘Handbook of in vitro fertilization’. (Eds A Trounson, DK Gardner) pp. 85–97. (CRC Press LLC: Boca Raton, FL)
Billo M, Cabalion P, Waikedre J, Fourneau C, Bouttier S, Hocquemiller R, Fournet A (2005) Screening of some new Caledonian and Vanuatu medicinal plants for antimycobacterial activity. Journal of Ethnopharmacology 96, 195–200.
| Screening of some new Caledonian and Vanuatu medicinal plants for antimycobacterial activity.Crossref | GoogleScholarGoogle Scholar | 15588670PubMed |
Blache D, Maloney SK, Revell DK (2008) Use and limitations of alternative feed resources to sustain and improve reproductive performance in sheep and goats. Animal Feed Science and Technology 147, 140–157.
| Use and limitations of alternative feed resources to sustain and improve reproductive performance in sheep and goats.Crossref | GoogleScholarGoogle Scholar |
Crosby IM, Moor RM (1984) Oocyte maturation. In ‘In vitro fertilization and embryo transfer’. (Eds A Trounson, C Wood) pp. 19–31. (Churchill Livingstone: Edinburgh, Scotland)
Diawara MM, Kulkosky PJ (2003) Reproductive toxicity of the psoralens. Pediatric Pathology & Molecular Medicine 22, 247–258.
| Reproductive toxicity of the psoralens.Crossref | GoogleScholarGoogle Scholar |
Diawara MM, Charez KJ, Simpleman D, Williams DE, Franklin MR, Hoyer PB (2001) The psoralens adversely affect reproductive function in male Wistar rats. Reproductive Toxicology (Elmsford, N.Y.) 15, 137–144.
| The psoralens adversely affect reproductive function in male Wistar rats.Crossref | GoogleScholarGoogle Scholar |
González Altamiranda EA, Kaiser GG, Rios GL, Leunda MR, Odeón AC (2016) Interaction of bovine viral diarrhea virus with bovine cumulus–oocyte complex during IVM: detection in permissive cells. Theriogenology 86, 1999–2003.
| Interaction of bovine viral diarrhea virus with bovine cumulus–oocyte complex during IVM: detection in permissive cells.Crossref | GoogleScholarGoogle Scholar | 27481815PubMed |
Houghton PJ, Raman A (Eds) (1998) ‘Laboratory handbook for the fractionation of natural extracts.’ 1st edn. (Chapman & Hall, Thomas Sciences: London, UK)
Jiang HS, Wang WL, Lu KH, Gordon I, Polge C (1992) Examination of cell numbers of blastocysts derived from IVM, IVF and IVC of bovine follicular oocytes. Theriogenology 37, 229
| Examination of cell numbers of blastocysts derived from IVM, IVF and IVC of bovine follicular oocytes.Crossref | GoogleScholarGoogle Scholar | [abstract]
Kelly JM, Kleemann DO, Rudiger SK, Walker SK (2007) Effects of grade of oocyte–cumulus complex on the interactions between grades on the production of blastocysts in the cow, ewe and lamb. Reproduction in Domestic Animals 42, 577–582.
| Effects of grade of oocyte–cumulus complex on the interactions between grades on the production of blastocysts in the cow, ewe and lamb.Crossref | GoogleScholarGoogle Scholar | 17976063PubMed |
Kelly RW, Hay RJM, Shackell GH (1979) Formononetin content of Grasslands Pawera red clover and its oestrogenic activity in sheep. New Zealand Journal of Agricultural Research 16, 441–446.
Kelly RW, Shackell GH, Allison AJ (1980) Reproductive performance of ewes grazing red clover (Grassland Pawera) or white clover-grass pasture at mating. New Zealand Journal of Experimental Agriculture 8, 87–91.
| Reproductive performance of ewes grazing red clover (Grassland Pawera) or white clover-grass pasture at mating.Crossref | GoogleScholarGoogle Scholar |
Kessell AE, Ladmore GE, Quinn JC (2015) An outbreak of primary photosensitisation in lambs secondary to consumption of Biserrula pelecinus (biserrula). Australian Veterinary Journal 93, 174–178.
| An outbreak of primary photosensitisation in lambs secondary to consumption of Biserrula pelecinus (biserrula).Crossref | GoogleScholarGoogle Scholar | 25939266PubMed |
Khazaei M, Aghaz F (2017) Reactive Oxygen species generation and use of antioxidants during in vitro maturation of oocytes. International Journal of Fertility & Sterility 11, 63–70.
King BJ, Robertson SM, Wilkins JF, Friend MA (2010) Short-term grazing of lucerne and chicory increases ovulation rate in synchronised Merino ewes. Animal Reproduction Science 121, 242–248.
| Short-term grazing of lucerne and chicory increases ovulation rate in synchronised Merino ewes.Crossref | GoogleScholarGoogle Scholar | 20678872PubMed |
Kotze AC, O’Grady J, Emms J, Toovey AF, Hughes S, Jessop P, Bennell M, Vercoe PE, Revell DK (2009) Exploring the anthelmintic properties of Australian native shrubs with respect to their potential role in livestock grazing systems. Parasitology 136, 1065–1080.
| Exploring the anthelmintic properties of Australian native shrubs with respect to their potential role in livestock grazing systems.Crossref | GoogleScholarGoogle Scholar | 19523255PubMed |
Lawrence TH, Beers WH, Gilula NB (1978) Transmission of hormonal stimulation by cell-to-cell communication. Nature 272, 501–506.
| Transmission of hormonal stimulation by cell-to-cell communication.Crossref | GoogleScholarGoogle Scholar |
Leite SP, de Medeiros PL, da Silva EC, de Souza Maia MB, de Menezes Lima VL, Saul DE (2004) Embryotoxicity in vitro with extract of Indigofera suffruticosa leaves. Reproductive Toxicology (Elmsford, N.Y.) 18, 701–705.
| Embryotoxicity in vitro with extract of Indigofera suffruticosa leaves.Crossref | GoogleScholarGoogle Scholar |
Lightfoot RJ, Smith JF, Cumming IA, Marshall T, Wroth RH, Hearnshaw H (1974) Infertility in ewes caused by prolonged grazing on oestrogenic pastures: oestrus, fertilization and cervical mucus. Australian Journal of Biological Sciences 27, 409–414.
| Infertility in ewes caused by prolonged grazing on oestrogenic pastures: oestrus, fertilization and cervical mucus.Crossref | GoogleScholarGoogle Scholar | 4473975PubMed |
McDonald IW (1981) Detrimental substances in plants consumed by grazing ruminants. In ‘Grazing animals’. (Ed. FHW Morley) pp. 349–360. (Elsevier: Amsterdam, The Netherlands)
McEvoy T, Robinson JJ, Ashworth CJ, Rooke JA, Sinclair KD (2001) Feed and forage toxicants affecting embryo survival and fetal development. Theriogenology 55, 113–129.
| Feed and forage toxicants affecting embryo survival and fetal development.Crossref | GoogleScholarGoogle Scholar | 11198077PubMed |
Moor RM, Smith WH, Dawson RMC (1980) Measurement of intercellular coupling between oocytes and cumulus cells using intercellular markers. Experimental Cell Research 126, 15–29.
| Measurement of intercellular coupling between oocytes and cumulus cells using intercellular markers.Crossref | GoogleScholarGoogle Scholar | 7358087PubMed |
Mothana RA, Lindequist U (2005) Antimicrobial activity of some medicinal plants of the island Soqotra. Journal of Ethnopharmacology 96, 177–181.
| Antimicrobial activity of some medicinal plants of the island Soqotra.Crossref | GoogleScholarGoogle Scholar | 15588668PubMed |
Mu H, Bai YH, Wang ST, Zhu ZM, Zhang YW (2009) Research on antioxidant effects and estrogenic effect of formononetin from Trifolium pratense (red clover). Phytomedicine 16, 314–319.
| Research on antioxidant effects and estrogenic effect of formononetin from Trifolium pratense (red clover).Crossref | GoogleScholarGoogle Scholar | 18757188PubMed |
Mustonen E, Taponen S, Andersson M, Sukura A, Katila T, Taponen J (2014) Fertility and growth of nulliparous ewes after feeding red clover silage with high phyto-oestrogen concentrations. Animal 8, 1699–1705.
| Fertility and growth of nulliparous ewes after feeding red clover silage with high phyto-oestrogen concentrations.Crossref | GoogleScholarGoogle Scholar | 24984155PubMed |
Oldham CM, Real D, Bailey HJ, Thomas D, Van Burgel AJ, Vercoe P, Correal E, Rios S (2013) Australian and Spanish scientists are collaborating in the domestication of tedera: young Merino sheep grazing a monoculture of tedera in autumn showed preference for certain accessions but no sign of ill health. Crop and Pasture Science 64, 399–408.
| Australian and Spanish scientists are collaborating in the domestication of tedera: young Merino sheep grazing a monoculture of tedera in autumn showed preference for certain accessions but no sign of ill health.Crossref | GoogleScholarGoogle Scholar |
Pace V, Conto G, Carfi F, Chiariotti A, Catillo G (2011) Short- and long-term effects of low estrogenic subterranean clover on ewe reproductive performance. Small Ruminant Research 97, 94–100.
| Short- and long-term effects of low estrogenic subterranean clover on ewe reproductive performance.Crossref | GoogleScholarGoogle Scholar |
Papaioannou VE, Ebert KM (1988) The preimplantation pig embryo: cell number and allocation to trophectoderm and inner cell mass of the blastocyst in vivo and in vitro Development 102, 793–803.
Rajabi-Toustani R, Motamedi-Mojdehi R, Roostaei-Ali Mehr M, Motamedi-Mojdehi R (2013) Effect of Papaver rhoeas L. extract on in vitro maturation of sheep oocytes. Small Ruminant Research 114, 146–151.
| Effect of Papaver rhoeas L. extract on in vitro maturation of sheep oocytes.Crossref | GoogleScholarGoogle Scholar |
Ramírez-Restrepo CA, Barry TN (2005) Alternative temperate forages containing secondary compounds for improving sustainable productivity in grazing ruminants. Animal Feed Science and Technology 120, 179–201.
| Alternative temperate forages containing secondary compounds for improving sustainable productivity in grazing ruminants.Crossref | GoogleScholarGoogle Scholar |
Ramòn JP, Valderràbano J, Folch J (1993) Reproductive performance of Rasa Aragonesa ewes mated on lucerne (Medicago sativa cv. aragon) pastures. Small Ruminant Research 11, 323–329.
| Reproductive performance of Rasa Aragonesa ewes mated on lucerne (Medicago sativa cv. aragon) pastures.Crossref | GoogleScholarGoogle Scholar |
Reid RL (1981) Livestock disease. In ‘A manual of Australian agriculture’.4th edn. (Ed. RL Reid) pp. 489–525. (The Australian Institute of Agricultural Science: William Heinemann, Melbourne)
Revell C, Revell D (2007) Meeting ‘Duty of Care’ obligations when developing new pasture species. Field Crops Research 104, 95–102.
| Meeting ‘Duty of Care’ obligations when developing new pasture species.Crossref | GoogleScholarGoogle Scholar |
Santos RR, Schoevers EJ, Roelen BAJ (2014) Usefulness of bovine and porcine IVM/IVF models for reproductive toxicology. Reproductive Biology and Endocrinology 12, 117
| Usefulness of bovine and porcine IVM/IVF models for reproductive toxicology.Crossref | GoogleScholarGoogle Scholar | 25427762PubMed |
Schoevers EJ, Santos RR, Fink-Gremmels J, Roelen BAJ (2016) Toxicity of beauvericin on porcine oocyte maturation and preimplantation embryo development. Reproductive Toxicology (Elmsford, N.Y.) 65, 159–169.
| Toxicity of beauvericin on porcine oocyte maturation and preimplantation embryo development.Crossref | GoogleScholarGoogle Scholar |
Spinaci M, Volpe S, De Ambrogi M, Tamanini C, Galeati G (2008) Effects of epigallocatechin-3-gallate (EGCG) on in vitro maturation and fertilization of porcine oocytes. Theriogenology 69, 877–885.
| Effects of epigallocatechin-3-gallate (EGCG) on in vitro maturation and fertilization of porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 18343490PubMed |
Sweeney AP, Wyllie SG, Shalliker RA, Markham JL (2001) Xanthine oxidase inhibitory activity of selected Australian native plants. Journal of Ethnopharmacology 75, 273–277.
| Xanthine oxidase inhibitory activity of selected Australian native plants.Crossref | GoogleScholarGoogle Scholar | 11297862PubMed |
Walker SK, Hill JL, Kleemann DO, Nancarrow CD (1996) Development of ovine embryos in synthetic oviduct fluid containing amino acids at oviduct fluid concentrations. Biology of Reproduction 55, 703–708.
| Development of ovine embryos in synthetic oviduct fluid containing amino acids at oviduct fluid concentrations.Crossref | GoogleScholarGoogle Scholar | 8862790PubMed |
Wang ZG, Yu SD, Xu ZR (2007) Improvement in bovine embryo production in vitro by treatment with green tea polyphenols during in vitro maturation of oocytes. Animal Reproduction Science 100, 22–31.
| Improvement in bovine embryo production in vitro by treatment with green tea polyphenols during in vitro maturation of oocytes.Crossref | GoogleScholarGoogle Scholar | 16870363PubMed |
Wina E, Muetzel S, Becker K (2005) The impact of saponin-containing plant materials on ruminant production-a review. Journal of Agricultural and Food Chemistry 53, 8093–8105.
| The impact of saponin-containing plant materials on ruminant production-a review.Crossref | GoogleScholarGoogle Scholar | 16218650PubMed |
Yuan B, Liang S, Jin Y-X, Zhang M-J, Zhang J-B, Kim N-H (2017) Toxic effects of atrazine on porcine oocytes and possible mechanisms of action. PLoS One 12, e0179861
| Toxic effects of atrazine on porcine oocytes and possible mechanisms of action.Crossref | GoogleScholarGoogle Scholar | 28806404PubMed |