Meiotic wave adds extra asymmetry to the development of female chicken gonads

Abstract

SUMMARYDevelopment of female gonads in the chicken is asymmetric. This asymmetry affects gene expression, morphology, and germ cell development; consequently only the left ovary develops into a functional organ, whereas the right ovary remains vestigial. In males, on the other hand, both gonads develop into functional testes. Here, we revisited the development of asymmetric traits in female (and male) chicken gonads between Hamburger Hamilton stage 16 (HH16) and hatching. At HH16, primordial germ cells migrated preferentially to the left gonad, accumulating in the left coelomic hinge between the gut mesentery and developing gonad in both males and females. Using the meiotic markers SYCP3 and phosphorylated H2AFX, we identified a previously undescribed, pronounced asymmetryc meiotic progression in the germ cells located in the central, lateral, and extreme cortical regions of the left female gonad from HH38 until hatching. Moreover, we observed that—in contrast to the current view—medullary germ cells are not apoptotic, but remain arrested in pre‐leptotene until hatching. In addition to the systematic analysis of the asymmetric distribution of germ cells in female chicken gonads, we propose an updated model suggesting that the localization of germ cells—in the left or right gonad; in the cortex or medulla of the left gonad; and in the central part or the extremities of the left cortex—has direct consequences for their development and participation in adult reproduction. Mol. Reprod. Dev. 82: 774–786, 2015. © 2015 The Authors. Molecular Reproduction and Development published by Wiley Periodicals, Inc.

Primary sex determination in birds depends on DMRT1 dosage, but gonadal sex does not determine adult secondary sex characteristics

“…3 A ). Meiotic progression was assessed by monitoring gamma H2A histone family member X (γH2AX), an indicator of double-stranded DNA breaks ( 22 , 26 ). As expected, γH2AX was not expressed in germ cells of Z D+ Z D+ gonads at either developmental stage, while germ cells in Z D+ W gonads expressed γH2AX at both stages with a reduction in expression at E17.5.…”

“…This suggests that the absence of functional DMRT1 leads to a loss of germ cells in posthatch female birds. Given that DMRT1 is highly expressed in germ cells and implicated in meiosis in other species, we analyzed meiotic progression in late stage embryos (E13.5 and E17.5) by monitoring the expression of γH2AX, which indicates DNA double-strand breaks typical of meiotic recombination ( 26 ). For Z D+ Z D- embryos, the pattern of marker expression in cortical PGCs was similar, although delayed, to that seen in wild-type female embryos.…”

Sex Reversal in Birds

“…The outer ep-ithelial layer does not hyper-proliferate. In the female (ZW), the outer cortical layer of the left gonad thickens and accumulates germs cells, which later enter meiotic arrest, while the inner medulla develops characteristic lacunae or fluid-filled cavities [Smith et al, 2008;de Melo Bernardo et al, 2015]. The right gonad of the female grows somewhat but fails to elaborate a thickened cortex, and germ cells do not enter meiosis, consistent with a loss of local Raldh2 enzyme expression (which synthesises the meiosis inducer, retinoic acid).…”

At Term, XmO and XpO Mouse Placentas Show Differences in Glucose Metabolism in the Trophectoderm-Derived Outer Zone

“…QPCR was performed on placental quarters after removal of the outer zone and analyzed as described (de Melo Bernardo et al, 2015 ); or on RNA material isolated from 5x paraffin sections of the outer zone using RecoverAll total nucleic acid isolation kit (AM1975, Ambion, Carlsbad, CA, USA) following the manufacturer's protocol. For normalization, the ΔΔCt method was used with the reference genes Ubc and B2m , stably expressed in mouse placenta (Solano et al, 2016 ).…”