Structural organization and evolution of the marsupial zona pellucida

Breed, W. G.; Hope, Rory M.; Wiebkin, Ole W.; Spargo, Scott C.; Chapman, Jamie

doi:10.1530/rep.0.1230013

Cited by 19 publications

(6 citation statements)

References 26 publications

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“…To consider first the zona pellucida, while much less is known about its interaction with sperm, the marsupial zona appears to be something of a halfway-house between that of eutherians and that in many other groups. Although relatively thick at about 2 -6 µm, and constituted by the same glycoproteins (Breed et al, 2002), the marsupial zona has no structural memory and 0.1% trypsin dissolves it completely in 2-8 seconds -far faster than the > 2 minutes required for the eutherian zona. Its role is also very different in some respects in that it is invested soon after fertilization by mucoid and then a persistent elastic shell laid down by 24 -36 hours as the egg passes through the uterotubal junction (Roberts, Breed and Mayrhofer, 1994).…”

Section: The Bearing Of Marsupial Patternsmentioning

confidence: 99%

Puzzles of mammalian fertilization and beyond

Bedford¹

2008

Int. J. Dev. Biol.

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A complexity imposed on the events of conception during the evolution of eutherian mammals is reflected not only in the placenta but also in a series of gamete-related novelties that involve the design of sperm and eggs, their interactions leading to fertilization, epididymal function, and even the scrotal state. While their functional significance has been difficult to determine, I suggest on the basis of present evidence that the genesis of these novel features relates ultimately to changes in the egg associated with nidation, that they imply a new fertilization strategy, and that most are causally linked -a major first 'domino' being the formidable zona pellucida. The eutherian zona pellucida stands out by virtue of an elastic resilience and thickness which allow it to stretch around the expanding blastocyst. However, this quality of the zona together with its relative protease-insensitivity creates a physical challenge which appears to have determined the design of the sperm head, its behaviour at fertilization, and indirectly even the pattern of sperm maturation in the epididymis. In turn, that pattern appears to have evoked the development of the sperm storage function of the cauda region, with both sperm capacitation and the scrotal state as ultimate legacies of this. Coincidentally, the vulnerability of the small yolkless egg to polyspermy appears to have selected for a unique parsimonious pattern of sperm transport in the Fallopian tube, and possibly for the role of the cumulus oophorus as a sperm sequestering device. These ideas are supported generally by evidence from marsupials, as well as by the deviant patterns seen in some insectivorous mammals.

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Section: The Bearing Of Marsupial Patternsmentioning

confidence: 99%

Puzzles of mammalian fertilization and beyond

Bedford¹

2008

Int. J. Dev. Biol.

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“…(9) Related to this developmental flexibility, the egg coats acquire additional functions such as the prevention of mosaicism (early conceptus fusion) or mono-zygotic twinning (conceptus splitting). (20,21) It has been established in marsupials that coatfree cleavage in vitro results in a morula-like form, but not a blastocyst because blastocyst epithelial morphology is not maintained. (22)(23)(24) Significantly the epithelia most affected are the trophoblast and the hypoblast.…”

Section: Marsupials and Eutheriansmentioning

confidence: 99%

Trophoblast and hypoblast in the monotreme, marsupial and eutherian mammal: evolution and origins

Selwood

Johnson

2006

Bioessays

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The pregastrula stage mammalian conceptus consists of both embryonic and non-embryonic components. The latter forms the bulk of the tissues, provides nutrition for the developing embryo and also contributes developmental signals that influence events within the embryo itself. Understanding the origins and relationships between the embryonic and extraembryonic cell lineages is thus central to understanding development in mammals. Despite the apparent gross differences in early developmental strategy and form, the conceptuses of eutherian, marsupial and monotreme mammals show some remarkable similarities in the lineage allocation to trophoblast and hypoblast and in the emergent properties of the two cell types. We suggest that the gross differences can be explained by two relatively small evolutionary timing changes affecting cell adhesion patterns and the polarisation of developmentally significant information. These changes result in the conversion of a unilaminar blastocyst to a morula form composed of blastomeres with increased regulatory capacity.

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“…Unlike those of monotremes (whose gametes appear to be essentially reptilian in character), marsupial gametes display some of the novel features seen in Eutheria, but also some important contrasts. The marsupial zona is constituted by the same glycoproteins as the eutherian zona (Breed et al, 2002), but represents an intermediate type between the delicate egg coat of many invertebrates and sub-therian vertebrates, and the robust zona seen in most Eutheria (Hughes, 1974). The relative prominence of the marsupial zona may be explained by the fact that it provides a template for initial development of the blastocyst.…”

Section: (6 ) the Cumulus Oophorusmentioning

confidence: 99%

Enigmas of mammalian gamete form and function

Bedford¹

2004

Biological Reviews

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The gametes of man and some other Eutheria have been manipulated successfully for practical reasons, but many gaps remain in our basic understanding of the way that they function. This situation stems not least from a failure to recognize the extent to which eutherian spermatozoa and eggs, and elements related to their operation, have come to differ from those of other groups. Novel features in the male that reflect this include a radical design of the sperm head with the acrosome seeming to function primarily in egg-coat binding rather than its lysis, a multifaceted post-testicular sperm maturation and an androgen/low-temperature-regulated system of sperm storage--both tied to the epididymis, a variable male accessory sex gland complex, and descent of the testis and epididymis to a scrotum. In the female, such novelties are represented in a need for sperm capacitation, in an unusual regulation of sperm transport within the oviduct, in the cumulus oophorus and character of the zona pellucida around the small egg, and in a unique configuration of gamete fusion. The collective evidence now suggests that many of these features reflect a new fertilisation strategy or its consequences, with most being causally linked. One initial 'domino' in this regard appears to be the small yolkless state of the egg and its intolerance for polyspermy, as determinants of the unusual mode of oviductal sperm transport and possibly the existence and form of the cumulus oophorus. However, a particularly influential first 'domino' appears to be the physical character of the eutherian zona pellucida. This differs from the egg coats of other animal groups by virtue of a resilient elasticity and thickness. These qualities allow this primary and often only coat to stretch and so persist during later expansion of the blastocyst, usually until close to implantation. At the same time, the dimensions, physical character, and particularly the relative protease-insensitivity of the zona appear to have had profound effects on sperm form and function and, more indirectly, on sperm-related events in the male and the female tract. Marsupials display some similarities and also some strikingly different features, against which the enigmas of the eutherian situation can be evaluated.

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Structural organization and evolution of the marsupial zona pellucida

Cited by 19 publications

References 26 publications

Puzzles of mammalian fertilization and beyond

Puzzles of mammalian fertilization and beyond

Trophoblast and hypoblast in the monotreme, marsupial and eutherian mammal: evolution and origins

Enigmas of mammalian gamete form and function

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