Male effect; Oestrus; Ovulation; Plants; Small ruminants; Progesterone; Animals; Female; Ovariectomy/veterinary; Reproduction/drug effects; Juglans/chemistry; Goats/physiology; Goats/metabolism; Progesterone/blood; Plant Leaves/chemistry; Goats; Juglans; Ovariectomy; Plant Leaves; Reproduction; Animal Science and Zoology
Abstract :
[en] Intravaginal sponges impregnated with the progesterone (P4) analogue fluorogestone acetate (FGA) induce synchronous oestrous behaviour and normal ovulatory cycle in goats. To explore alternatives using natural P4 from plants, we developed a method of ethanolic extraction and a specific enzyme immunoassay (EIA) to measure P4 in the different parts of the walnut tree Juglans regia. We found a very high concentration of P4, specifically in the leaves of the three most common French varieties (∼100 mg/kg of DM) but not in flowers, fruits, septa, husk, oil or cake. High concentrations of P4-and to a lesser extent its reduction metabolites and phytosterols-were also measured by Gas Chromatography-Mass Spectrometry/Mass Spectrometry in leaf extracts. P4 concentrations were five times higher in October than in June. P4 was detected in 182 varieties of Juglans regia ranging from 35 to 287 mg of P4 per kg of leaf DM. We collected large quantities of leaves over 6 years, which were used to manufacture feed pellets containing 32% of dry leaf for distribution to female goats. To determine their dietary acceptance and their efficacy in terms of P4 blood plasma concentration, three trials in ovariectomised goats and four trials in ovary-intact goats were performed (N = 83). The distribution of 600 g of pellets per day per ovary-intact goat over 3 days, 6 and 4 days before the introduction of males in April allowed us to achieve our objective of a significant increase of P4 plasma concentration to ∼1.5 ng/mL measured by EIA from 24 to 72 h after the first distribution in the walnut pellet group (n = 13). The two control groups of goats (FGA, n = 12 and control, n = 10) showed no increase in plasma P4. However, despite this high P4 plasma concentration, goats of the walnut group had the same percentages of goats in oestrus at the first ovulation and of goats experiencing short ovulatory cycles after introduction of males (54 and 77%, respectively) as the group of control goats (80 and 90%), whereas the FGA goats showed very different percentages (100 and 0%, P < 0.01). It was concluded that whereas walnut leaves contain a high concentration of P4-and its reduction metabolites and phytosterols-the pellet feeding mode does not allow for restoration of oestrus behaviour and duration of the induced cycle consistently achieved with FGA-impregnated intravaginal sponges.
Disciplines :
Agriculture & agronomy
Author, co-author :
Chemineau, P; Physiologie de la Reproduction et des Comportements, CNRS, INRAE, Université de Tours, 37380 Nouzilly, France. Electronic address: Philippe.Chemineau@inrae.fr
Lainé, A L; Physiologie de la Reproduction et des Comportements, CNRS, INRAE, Université de Tours, 37380 Nouzilly, France
Gennetay, D; Physiologie de la Reproduction et des Comportements, CNRS, INRAE, Université de Tours, 37380 Nouzilly, France
Porte, C; Physiologie de la Reproduction et des Comportements, CNRS, INRAE, Université de Tours, 37380 Nouzilly, France
Chesneau, D; Physiologie de la Reproduction et des Comportements, CNRS, INRAE, Université de Tours, 37380 Nouzilly, France
Laclie, C; Physiologie de la Reproduction et des Comportements, CNRS, INRAE, Université de Tours, 37380 Nouzilly, France
Goudet, G; Physiologie de la Reproduction et des Comportements, CNRS, INRAE, Université de Tours, 37380 Nouzilly, France
Meunier, Maxime ; Physiologie de la Reproduction et des Comportements, CNRS, INRAE, Université de Tours, 37380 Nouzilly, France
Delmas, M; INRAE, UEA, 33210 Toulenne, France
Greil, M L; INRAE, UEA, 33210 Toulenne, France
Liere, P; U1195 INSERM Université Paris Saclay, Kremlin Bicêtre, France
Pianos, A; U1195 INSERM Université Paris Saclay, Kremlin Bicêtre, France
Bernard, A; INRAE, Université de Bordeaux, UMR BFP, 33882 Villenave d'Ornon, France
Dirlewanger, E; INRAE, Université de Bordeaux, UMR BFP, 33882 Villenave d'Ornon, France
Delgadillo, J A; Centro de Investigación en Reproducción Caprina (CIRCA), Universidad Autónoma Agraria Antonio Narro, 27054 Torreón, Coahuila, Mexico
Keller, M; Physiologie de la Reproduction et des Comportements, CNRS, INRAE, Université de Tours, 37380 Nouzilly, France
We thank Drs Hoa Nguyen, H. Cuong, Pham Kim Dang and Samira Sarter for collecting and sending \u2018benalu duku\u2019 leaves from Vietnam, which provided the results presented in Supplementary Material S1. We thank Olivier Lasserre and colleagues of the experimental unit (UEPAO) in Nouzilly for taking care of the animals during the study. We also thank Morgane Brachet, Timoth\u00E9e Zidat, H\u00E9l\u00E8ne Vacher and Adrien Acquistapace of UMR-PRC for their help during animal sampling and observation. We are grateful to Pascal Laurent, Daniel Vergneau, Jean-Yves Chevrollier and all technicians of the Unit\u00E9 Exp\u00E9rimentale Arboricole for their help during the collections of the walnut leaves and all technicians of the Unit\u00E9 Exp\u00E9rimentale Physiologie et Ph\u00E9notypage des Porcs in St. Gilles for their help in processing the experimental pellets. The authors are also grateful to the whole hormonal assay platform in Nouzilly, France for undertaking the hormonal determinations. We thank Pierre Martin from CAPGENES for his enduring support of the programme. This work was supported by the Centre Val de Loire regional authority under CAPRINOIX Contract Numbers 85-C4646 and 2020-00138613, by the programme cadre CNE \u201CMa\u00EEtrise de la reproduction des petits ruminants\u201D Number C18042/32001390 and by INRAE-PHASE specific funding. Phytosterol assays were supported by the INRAE grant Vegetruies of the METABIO programme Number C12603.This work was supported by the Centre Val de Loire regional authority under CAPRINOIX Contract Numbers 85-C4646 and 2020-00138613, by the programme cadre CNE \u201CMa\u00EEtrise de la reproduction des petits ruminants\u201D Number C18042/32001390 and by INRAE-PHASE specific funding. Phytosterol assays were supported by the INRAE grant Vegetruies of the METABIO programme Number C12603.
Adlercreutz, H., Martin, F., Biliary-excretion and intestinal metabolism of progesterone and estrogens in man. Journal of Steroid Biochemistry and Molecular Biology 13 (1980), 231–244, 10.1016/0022-4731(80)90196-X.
Akkopru, E.P., Atlihan, R., Okut, H., Chi, H., Demographic assessment of plant cultivar resistance to insect pests: a case study of the Dusky-Veined Walnut Aphid (Hemiptera: Callaphididae) on five walnut cultivars. Journal of Economic Entomology 108 (2015), 379–387.
Andrade-Esparza, J.D., Espinoza-Flores, L.A., Hernandez, H., Chemineau, P., Keller, M., Delgadillo, J.A., Progesterone doses of 5, 3 or 1 mg do not prevent short ovulatory cycles in goats exposed to photo-stimulated bucks. Theriogenology 130 (2019), 36–40, 10.1016/j.theriogenology.2019.02.036.
Bennett, R.D., Heftmann, E., Progesterone - Biosynthesis From Pregnenolone In Holarrhena Floribunda. Science, 149(3684), 1965, 652, 10.1126/science.149.3684.652.
Bernard, A., Lheureux, F., Dirlewanger, E., Walnut: past and future of genetic improvement. Tree Genetics & Genomes, 14, 2018, 1, 10.1007/s11295-017-1214-0.
Bernard, A., Crabier, J., Donkpegan, A.S.L., Marrano, A., Lheureux, F., Dirlewanger, E., Genome-wide association study reveals candidate genes involved in fruit trait variation in Persian Walnut (Juglans regia L.). Frontiers in Plant Science, 11, 2021, 607213, 10.3389/fpls.2020.607213.
Buisson, D., Astruc, J.M., Barillet, F., Bilan et perspectives de la gestion de la variabilité génétique des ovins laitiers en France. INRA Productions Animales 31 (2018), 1–12, 10.20870/productions-animales.2018.31.1.2202.
Canépa, S., Lainé, A.L., Bluteau, A., Fagu, C., Flon, C., Monniaux, D., Validation d'une méthode immunoenzymatique pour le dosage de la progestérone dans le plasma des ovins et des bovins. Cahier Des Techniques De l'INRA 64 (2008), 19–30.
Chemineau, P., Poulin, N., Cognie, Y., Progesterone secretion in the creole goat during male-induced ovarian cycles - seasonal effect. Reproduction Nutrition Development 24 (1984), 557–561, 10.1051/rnd:19840505.
Chemineau, P., Chupin, D., Cognié, Y., Thimonier, J., La maîtrise de la reproduction des mammifères domestiques. Levasseur, M.C., Thibault, C., (eds.) Reproduction chez Les Mammifères et L'homme, 1991, Publications Ellipses, Paris, France, 655–676.
Chemineau, P., Malpaux, B., Delgadillo, J.A., Guerin, Y., Ravault, J.P., Thimonier, J., Pelletier, J., Control of sheep and goat reproduction - use of light and melatonin. Animal Reproduction Science 30 (1992), 157–184, 10.1016/0378-4320(92)90010-B.
Dagnelie, P., (ed.) 1970. Théorie et Méthodes Statistiques: applications agronomiques. Volume 2: les méthodes de l'inférence statistique. Presses Agronomiques de Gembloux, Gembloux, Belgique, 451 pp., pp. 21–26 and 98–105.
De Lignières, B., Dennerstein, L., Backstrom, T., Influence of route of administration on progesterone metabolism. Maturitas 21 (1995), 251–257, 10.1016/0378-5122(94)00882-8.
Gatti, M., Zunino, P., Ungerfeld, R., Changes in the aerobic vaginal bacterial mucous load after treatment with intravaginal sponges in anoestrous ewes: effect of medroxiprogesterone acetate and antibiotic treatment use. Reproduction in Domestic Animals 46 (2011), 205–208, 10.1111/j.1439-0531.2010.01626.x.
Goudet, G., Liere, P., Pianos, A., Fernandez, N., Cambourg, A., Savoie, J., Staub, C., Venturi, E., Douet, C., Ferchaud, S., Maupertuis, F., Roinsard, A., Boulot, S., Prunier, A., Evolution of steroid concentrations in saliva from immature to pubertal gilts for the identification of biomarkers of gilts receptivity to boar effect. Livestock Science 228 (2019), 5–17, 10.1016/j.livsci.2019.07.018.
Goudet, G., Prunier, A., Nadal-Desbarats, L., Grivault, D., Ferchaud, S., Pianos, A., Haddad, L., Montigny, F., Douet, C., Savoie, J., Maupertuis, F., Roinsard, A., Boulot, S., Liere, P., Steroidome and metabolome analysis in gilt saliva to identify potential biomarkers of boar effect receptivity. Animal, 15, 2021, 2, 10.1016/j.animal.2020.100095.
Goudet, G., Douet, C., Pianos, A., Haddad, L., Reigner, F., Deleuze, S., Liere, P., Saliva and plasma steroidome in mare during reproductive stages: a GC-MS/MS study. Frontiers in Animal Science, 3, 2023, 1055179, 10.3389/fanim.2022.1055179.
Lazuardi, M., Hermanto, B., LC ESI-MS and FT-IR analysis of Dendrophthoe pentandra L. Miq leaf methanolic extracts to identify compounds with Progesterone-like effects. Pakistan Journal of Nutrition 15 (2016), 274–282.
Lazuardi, M., Hermanto, B., Hestianah, E.P., Determination of progesterone compounds in the crude methanol extract of benalu duku leaves. Veterinary World 12 (2019), 358–366, 10.14202/vetworld.2019.358-366.
Leboeuf, M., Cave, A., Goutarel, R., Steroidal Alkaloids LXXXII. Composition chimique des feuilles de l'Holarrhena floribunda Dur et Schinz. Isolement de la progestérone et de quatre nouveaux alcaloïdes: méthyl-holaphylline, hoaphyllinol, holaphyllidine et dihydroholaphyllamine. Annales Pharmaceutiques Françaises, 27, 1969, 217.
Lindemann, P., Steroidogenesis in plants – biosynthesis and conversions of progesterone and other pregnane derivatives. Steroids 103 (2015), 145–152, 10.1016/j.steroids.2015.08.007.
Manes, J., Hozbor, F., Alberio, R., Ungerfeld, R., Intravaginal placebo sponges affect negatively the conception rate in sheep. Small Ruminant Research 120 (2014), 108–111, 10.1016/j.smallrumres.2014.05.006.
Manes, J., Rios, G., Fiorentino, M.A., Ungerfeld, R., Vaginal mucus from ewes treated with progestogen sponges affects quality of ram spermatozoa. Theriogenology 85 (2016), 856–861, 10.1016/j.theriogenology.2015.10.033.
Menchaca, A., Miller, V., Salveragiol, V., Rubianes, E., Endocrine, luteal and follicular responses after the use of the short-term protocol to synchronize ovulation in goats. Animal Reproduction Science 102 (2007), 76–87, 10.1016/j.anireprosci.2006.10.001.
Oldham, C.M., Pearce, D.T., Gray, S.J., Progesterone priming and age of Ewe affect the life-span of corpora lutea induced in the seasonally anovulatory Merino Ewe by the “ram effect. Journal of Reproduction and Fertility 75 (1985), 29–33.
Pauli, G.F., Friesen, J.B., Gödecke, T., Norman, R., Farnsworth, N.R., Glodny, B., Occurrence of progesterone and related animal steroids in two higher plants. Journal of Natural Products 73 (2010), 338–345, 10.1021/np9007415.
Pearce, D.T., Martin, G.B., Oldham, C.M., Corpora lutea with a short life-span induced by rams in seasonally anovulatory ewes are prevented by progesterone delaying the preovulatory surge of LH. Journal of Reproduction and Fertility, 75, 1985, 79e84.
Pellicer-Rubio, M.T., Leboeuf, B., Bernelas, D., Forgerit, Y., Pougnard, J.L., Bonnet, J.L., Senty, E., Sylvain Breton, S., Brun, F., Chemineau, P., High fertility using artificial insemination during deep anoestrus after induction and synchronisation of ovulatory activity by the “male effect” in lactating goats subjected to treatment with artificial long days and progestogens. Animal Reproduction Science 109 (2008), 172–188, 10.1016/j.anireprosci.2007.11.026.
Pellicer-Rubio, M.T., Boissard, K., Forgerit, Y., Pougnard, J.L., Bonné, J.L., Leboeuf, B., Evaluation of hormone-free protocols based on the “male effect” for artificial insemination in lactating goats during seasonal anestrus. Theriogenology 85 (2016), 960–969, 10.1016/j.theriogenology.2015.11.005.
Snedecor, G.W., Cochran, W.G., Statistical Methods. Sixth ed., 1971, Iowa State University Press, Ames, IA, USA.
Suarez, G., Zunino, P., Carol, H., Ungerfeld, R., Changes in the aerobic vaginal bacterial mucous load and assessment of the susceptibility to antibiotics after treatment with intravaginal sponges in anestrous ewes. Small Ruminant Research 63 (2006), 39–43, 10.1016/j.smallrumres.2005.01.011.
Téteau, O., Liere, P., Pianos, A., Desmarchais, A., Lasserre, O., Papillier, P., Vignault, C., Lebachelier de la Rivière, M.E., Maillard, V., Binet, A., Uzbekova, S., Saint-Dizier, M., Elis, S., Bisphenol s alters the steroidome in the preovulatory follicle, oviduct fluid and plasma in ewes with contrasted metabolic status. Frontiers in Endocrinology (lausanne), 13, 2022, 892213, 10.3389/fendo.2022.892213.
Ungerfeld, R., Silva, L., The presence of normal vaginal flora is necessary for normal sexual attractiveness of estrous ewes. Applied Animal Behaviour Science 93 (2005), 245–250, 10.1016/j.applanim.2004.11.014.
