Evolutionary Origin of Bone Morphogenetic Protein 15 and Growth and Differentiation Factor 9 and Differential Selective Pressure Between Mono- and Polyovulating Species1

Monestier, Olivier; Servin, Bertrand; Auclair, Sylvain; Bourquard, Thomas; Poupon, Anne; Pascal, Géraldine; Fabre, Stéphane

doi:10.1095/biolreprod.114.119735

Cited by 24 publications

(17 citation statements)

References 69 publications

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“…Compilation of current data suggests that mutations in TGF-β family genes are often involved in the tinkering of reproductive and skeletal traits during evolution and domestication. Several BMP alleles have been associated to increased fertility in domestic sheeps (BMP15 and its paralog GDF9) (Monestier et al 2014) and to fecundity and bone allocation in chicken (BMP2) (Johnsson et al 2012). Genetic studies of craniofacial diversity mapped a QTL interval containing the BMP4 gene in cichlid fishes (Albertson et al 2005) and found a strong association between a single amino acid change in BMP3 and brachycephalic (short-skulled) dog breeds (Schoenebeck et al 2012).…”

Section: à5mentioning

confidence: 99%

Morphological Evolution Repeatedly Caused by Mutations in Signaling Ligand Genes

Martin

Courtier‐Orgogozo

2017

Diversity and Evolution of Butterfly Wing Patterns

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What types of genetic changes underlie evolution? Secreted signaling molecules (syn. ligands) can induce cells to switch states and thus largely contribute to the emergence of complex forms in multicellular organisms. It has been proposed that morphological evolution should preferentially involve changes in developmental toolkit genes such as signaling pathway components or transcription factors. However, this hypothesis has never been formally confronted to the bulk of accumulated experimental evidence. Here we examine the importance of ligandcoding genes for morphological evolution in animals. We use Gephebase (http:// www.gephebase.org), a database of genotype-phenotype relationships for evolutionary changes, and survey the genetic studies that mapped signaling genes as causative loci of morphological variation. To date, 19 signaling genes represent 20% of the cases where an animal morphological change has been mapped to a gene (80/391). This includes the signaling gene Agouti, which harbors multiple cis-regulatory alleles linked to color variation in vertebrates, contrasting with the effects of coding variation in its target, the melanocortin receptor MC1R. In sticklebacks, genetic mapping approaches have identified 4 signaling genes out of 14 loci associated with lake adaptations. Finally, in butterflies, a total of 18 allelic variants of the WntA Wnt-family ligand cause color pattern adaptations related to wing mimicry, both within and between species. We discuss possible hypotheses explaining these cases of natural replication (genetic parallelism) and conclude that signaling ligand loci are an important source of sequence variation underlying morphological change in nature.

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Section: à5mentioning

confidence: 99%

Morphological Evolution Repeatedly Caused by Mutations in Signaling Ligand Genes

Martin

Courtier‐Orgogozo

2017

Diversity and Evolution of Butterfly Wing Patterns

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“…Lamb productivity of the ewe is genetically predetermined and it can vary among breeds from w1 in typically monovular breeds (eg, Merino del Pais) to >5 in the carriers of fecundity genes such as FecB or Booroola genotypes [1,2]. However, in spite of the fact that products of certain genes may program this tremendous biodiversity [3], the hormonal control of ovarian follicle kinetics and ovulation rates in sheep is not completely understood. The physiological regulation of ovulatory follicle development remains unclear [1], and continued investigations into the mechanisms governing ovulation and fertility have been central in reproductive biology across species [3].…”

Section: Introductionmentioning

confidence: 99%

“…However, in spite of the fact that products of certain genes may program this tremendous biodiversity [3], the hormonal control of ovarian follicle kinetics and ovulation rates in sheep is not completely understood. The physiological regulation of ovulatory follicle development remains unclear [1], and continued investigations into the mechanisms governing ovulation and fertility have been central in reproductive biology across species [3].…”

Section: Introductionmentioning

confidence: 99%

Is progesterone the key regulatory factor behind ovulation rate in sheep?

Bartlewski

Sohal

Paravinja

et al. 2017

Domestic Animal Endocrinology

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Ovarian antral follicles in the ewe grow in an orderly succession, producing 3 to 4 waves per estrous cycle. In prolific sheep, some large antral follicles from the second-to-last wave of the estrous cycle are added to the ovulatory follicles emerging just before estrus to give a higher ovulation rate; it is feasible that regression of these follicles is prevented by an increase in serum concentrations of FSH or LH pulsatility at proestrus. Prolific sheep tend to have a shorter luteal phase than nonprolific ewes and there is a great deal of evidence that luteal progesterone (P), in addition to regulating LH release, may govern the secretion of FSH heralding the emergence of follicular waves. The specific purpose of this study was to determine whether or not extending the duration of the luteal phase in prolific sheep to that typically seen in nonprolific breeds would alter the follicle wave dynamics and ovulation rate. In 2 separate experiments, exogenous P (7.5 mg per ewe intramuscularly) was administered on day 11 at PM and day 12 at AM (day 0 = first ovulation of the interovulatory interval studied) in moderately prolific Rideau Arcott × Polled Dorset ewes (experiment 1, n = 8) and highly prolific Olkuska ewes (experiment 2, n = 7; TRT), whereas the equinumerous groups of animals served as controls (CTR). Transrectal ovarian ultrasonography was performed daily, and jugular blood samples were drawn twice a day from day 9 until the next ovulation. Progesterone injections resulted in relatively uniform increments in serum P levels, but the mean duration of the interovulatory interval did not differ (P > 0.05) between TRT and CTR groups of ewes in either experiment. The mean ovulation rate post-treatment was 1.6 ± 0.2 vs 3.2 ± 0.4 (experiment 1, P < 0.001) and 3.2 ± 0.8 vs 4.0 ± 1.0 (experiment 2, P > 0.05) in TRT vs CTR, respectively. The number and percentage of ovulating follicles from the penultimate wave of the interovulatory interval studied was 0.25 ± 0.16 vs 1.75 ± 0.45 (P < 0.01) and 25.0 ± 16.4% vs 75.0 ± 16.4% (P < 0.05) in experiment 1, and 0.50 ± 0.30 vs 1.60 ± 0.40 (P < 0.05) and 13.8 ± 9.0% vs 53.4 ± 16.7% (P < 0.05) in experiment 2, for TRT vs CTR, respectively. In summary, administration of P at the end of diestrus decreased the incidence of ovulations from the penultimate wave of the estrous cycle in both the moderately and highly prolific strains of sheep, but it reduced the ovulation rate only in moderately prolific ewes.

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“…They subsequently found that defects in the production of mouse BMP15 mature protein could correlate with species-specific differences(Hashimoto et al, 2005). Moreover, a phylogenetic analysis found that a better conservation in areas involved in dimer formation and stability of BMP15 within mono-ovulatory species, but high variations in these areas within poly-ovulatory species, implying the correlation with altered equilibrium between homodimers and heterodimers, and modified biological activity for allowing polyovulation to occur(Monestier et al, 2014). Hence, it seems that the role of BMP15 in regulation of follicular development and ovulation rate was more critical in mono-ovulatory mammalian species than poly-ovulatory animals.…”

Section: Introductionmentioning

confidence: 99%

Essential role of Bone morphogenetic protein 15 in porcine ovarian and follicular development and ovulation

Qin

Tang

et al. 2019

Preprint

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13Bone morphogenetic protein 15 (BMP15) is a multifunctional oocyte-specific secreted factor. It controls 14 female fertility and follicular development in both species-specific and dosage-sensitive manners. Previous 15 studies found that BMP15 played a critical role on follicular development and ovulation rate of 16 mono-ovulatory mammalian species, but has minimal impact on poly-ovulatory mice. However, whether this 17 is true in non-rodent poly-ovulatory species need to be validated. To investigate this question, we generated a 18 BMP15 knockdown pig model. We found that BMP15 knockdown gilts showed markedly reduced fertility 19 accompanied with phenotype of dysplastic ovaries containing significantly declined number of follicles, 20 increased number of abnormal follicles, and abnormally enlarged antral follicles resulting in disordered 21 ovulation. Molecular and transcriptome analysis revealed that knockdown of BMP15 significantly suppressed 22 cell proliferation, differentiation, Fshr expression, leading to premature luteinization and reduced estradiol 23 production in GCs, and simultaneously decreased the quality and meiotic maturation of oocyte. Our results 24 provide in vivo evidences for the essential role of BMP15 in porcine ovarian and follicular development, and 25 new insight into the complicated regulatory function of BMP15 in female fertility of poly-ovulatory species. 26 KEY WORDS: BMP15; transgenic pig; follicular development; ovarian development 27 28 96cells (PEFs) derived from a male Yorkshire pig. Transfected PEFs then were subjected to G418 selection to 97 screen the cells with stable expression of EGFP as donor cells for somatic cell nuclear transfer (SCNT). Clone 98 embryos then were transferred into Large White sow recipients to generate F0 TG pigs as described in our 99 previous report (Liu et al., 2019) (Fig. S1A). We obtained two healthy F0 TG males at last. After sexual 100 maturity, one F0 TG boar was mated with wild-type sows to generate F1 TG gilts for subsequent experiments. 101Both F0 and F1 TG pigs showed visible intense GFP fluorescence on toes and muscle while subjected to 102 sunlight (Fig. 1C, Fig. S1B), directly suggesting that the pEGFP-BMP15 shRNA plasmid was successfully 103 integrated into the genome of F0 TG boar, and can be transmitted to the next generation through the germline. 104This was confirmed by PCR analysis of fragment of integrated plasmid in muscle tissue of F1 TG gilts ( Fig. 105 S2A). The copy number of integrated plasmid was estimated to be approximate seven in F1 TG pigs through 106 the combination of both qPCR that using a transferrin receptor gene to normalize the genomic DNA (data 107 not shown), and Southern blot analysis ( Fig. S2B). More importantly, evidently decrease level of BMP15 108 mRNA ( Fig. 1E) in 365 days old TG ovaries and BMP15 protein level in 30 days old TG ovaries ( Fig. 1F, G) 109 strongly demonstrated the successful generation of the BMP15 knockdown model, and implied an in vivo 110 BMP15 knockdown efficiency of about 50%...

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Evolutionary Origin of Bone Morphogenetic Protein 15 and Growth and Differentiation Factor 9 and Differential Selective Pressure Between Mono- and Polyovulating Species1

Cited by 24 publications

References 69 publications

Morphological Evolution Repeatedly Caused by Mutations in Signaling Ligand Genes

Morphological Evolution Repeatedly Caused by Mutations in Signaling Ligand Genes

Is progesterone the key regulatory factor behind ovulation rate in sheep?

Essential role of Bone morphogenetic protein 15 in porcine ovarian and follicular development and ovulation

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