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Abstract
Mammalian eggs are surrounded by an extracellular matrix called the zona pellucida (ZP). This envelope participates in processes such as acrosome reaction induction, sperm binding, protection of the oviductal embryo, and may be involved in speciation. In eutherian mammals, this coat is formed of three or four glycoproteins (ZP1–ZP4). While Mus musculus has been used as a model to study the ZP for more than 35 years, surprisingly, it is the only eutherian species in which the ZP is formed of three glycoproteins Zp1, Zp2, and Zp3, Zp4 being a pseudogene. Zp4 was lost in the Mus lineage after it diverged from Rattus, although it is not known when precisely this loss occurred. In this work, the status of Zp4 in several murine rodents was tested by phylogenetic, molecular, and proteomic analyses. Additionally, assays of cross in vitro fertilization between three and four ZP rodents were performed to test the effect of the presence of Zp4 in murine ZP and its possible involvement in reproductive isolation. Our results showed that Zp4 pseudogenization is restricted to the subgenus Mus, which diverged around 6 MYA. Heterologous in vitro fertilization assays demonstrate that a ZP formed of four glycoproteins is not a barrier for the spermatozoa of species with a ZP formed of three glycoproteins. This study identifies the existence of several mouse species with four ZPs that can be considered suitable for use as an experimental animal model to understand the structural and functional roles of the four ZP proteins in other species, including human.
Highlights
The zona pellucida (ZP) is an extracellular coat that surrounds mammalian oocytes and early embryos
Sequences of the mRNA obtained from Mus mattheyi, Mus pahari, and Mastomys coucha ovaries were added to determine the limits of the exons
Our observations showed that Mus mattheyi and Mus pahari sperm were still able to adhere to the heterologous ZP, but we observed that the number of spermatozoa that adhere to the ZP was much lower than in the control group
Summary
The zona pellucida (ZP) is an extracellular coat that surrounds mammalian oocytes and early embryos. The composition of the ZP matrix has been elucidated in many species, and Murine Zona Pellucida has been seen to be composed of three to four glycoproteins in eutherians (Bleil and Wassarman, 1980; Hedrick and Wardrip, 1987; Lefièvre et al, 2004; Hoodbhoy et al, 2005; Ganguly et al, 2008; Goudet et al, 2008; Izquierdo-Rico et al, 2009; Stetson et al, 2012, 2015; Moros-Nicolás et al, 2018c), and four to seven in marsupials and monotremes (Frankenberg and Renfree, 2018; Moros-Nicolás et al, 2018a; Wu et al, 2018). One of the copies (ZP1 or ZP4) was lost after a duplication event due to a pseudogenization process (Goudet et al, 2008)
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