Genes Encoding Mammalian Oviductal Proteins Involved in Fertilization are Subjected to Gene Death and Positive Selection

Carla Moros-Nicolás,Philippe Monget,Ghylène Goudet,Sophie Fouchécourt

doi:10.1007/s00239-018-9878-0

Abstract

Oviductal proteins play an important role in mammalian fertilization, as proteins from seminal fluid. However, in contrast with the latter, their phylogenetic evolution has been poorly studied. Our objective was to study in 16 mammals the evolution of 16 genes that encode oviductal proteins involved in at least one of the following steps: (1) sperm–oviduct interaction, (2) acrosome reaction, and/or (3) sperm–zona pellucida interaction. Most genes were present in all studied mammals. However, some genes were lost along the evolution of mammals and found as pseudogenes: annexin A5 (ANXA5) and deleted in malignant brain tumor 1 (DMBT1) in tarsier; oviductin (OVGP1) in megabat; and probably progestagen-associated endometrial protein (PAEP) in tarsier, mouse, rat, rabbit, dolphin, and megabat; prostaglandin D2 synthase (PTGDS) in microbat; and plasminogen (PLG) in megabat. Four genes [ANXA1, ANXA4, ANXA5, and heat shock 70 kDa protein 5 (HSPA5)] showed branch-site positive selection, whereas for seven genes [ANXA2, lactotransferrin (LTF), OVGP1, PLG, S100 calcium-binding protein A11 (S100A11), Sperm adhesion molecule 1 (SPAM1), and osteopontin (SPP1)] branch-site model and model-site positive selection were observed. These results strongly suggest that genes encoding oviductal proteins that are known to be important for gamete fertilization are subjected to positive selection during evolution, as numerous genes encoding proteins from mammalian seminal fluid. This suggests that such a rapid evolution may have as a consequence that two isolated populations become separate species more rapidly.

Highlights

The oviduct, called the Fallopian tube in human, is a tubular organ that plays an important role in mammalian fertilization
The present search for pseudogenes showed that annexin A5 (ANXA5) and deleted in malignant brain tumor 1 (DMBT1) were lost in tarsier; OVGP1 in megabat; and probably progestagen-associated endometrial protein (PAEP) in tarsier, mouse, rat, rabbit, dolphin, and megabat; prostaglandin D2 synthase (PTGDS) in microbat; and PLG in megabat
Site model positive selection was found for OVGP1, PLG, S100 calcium-binding protein A11 (S100A11), and SPP1 with the M8a versus M8 comparison, whereas LTF and Sperm adhesion molecule 1 (SPAM1), likelihood ratio tests (LRTs) for both comparisons (M1 vs. M2, M8a vs. M8) were significant (p < 0.001) for the dataset

Summary

Introduction

The oviduct, called the Fallopian tube in human, is a tubular organ that plays an important role in mammalian fertilization. The oviduct is the location where fertilization takes place in amniotes. It is involved in gamete transportation and maturation, sperm capacitation, and it provides the appropriate microenvironment for the early embryo development (Coy et al 2012a; Hunter 1998, 2012). It has been demonstrated that the oviductal proteome changes with the different stages of the oestrous cycle (Lamy et al 2016; Soleilhavoup et al 2016), the presence of gametes (Georgiou et al 2005) or the presence of embryos (Smits et al 2017). The proteome of the oviduct epithelial cells has been studied in humans (Wang et al 2016) and pigs (Seytanoglu et al 2008)

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