Abstract
ABSTRACTAnimal egg coats are composed of different glycoproteins collectively named zona pellucida (ZP) proteins. The characterized vertebrate genes encoding ZP proteins have been classified into six subfamilies, and exhibit low similarity to the ZP genes characterized in certain invertebrates. The origin and evolution of the vertebrate ZP genes remain obscure. A search against 97 representative metazoan species revealed various numbers (ranging from three to 33) of different putative egg-coat ZP genes in all 47 vertebrates and several ZP genes in five invertebrate species, but no putative ZP gene was found in the other 45 species. Based on phylogenetic and synteny analyses, all vertebrate egg-coat ZP genes were classified into eight ZP gene subfamilies. Lineage- and species-specific gene duplications and gene losses occurred frequently and represented the main causes of the patchy distribution of the eight ZP gene subfamilies in vertebrates. Thorough phylogenetic analyses revealed that the vertebrate ZP genes could be traced to three independent origins but were not orthologues of the characterized invertebrate ZP genes. Our results suggested that vertebrate egg-coat ZP genes should be classified into eight subfamilies, and a putative evolutionary map is proposed. These findings would aid the functional and evolutionary analyses of these reproductive genes in vertebrates.
Highlights
Animal egg coats participate in species-specific sperm-egg recognition during the process of fertilization and protect the growth of oocytes, eggs and early-developing embryos (Conner et al, 2005; Litscher and Wassarman, 2014; Modig et al, 2007)
To explore the potential origin of these identified vertebrate zona pellucida (ZP) genes, previously characterized ZP genes of invertebrates (Aagaard et al, 2006; Kürn et al, 2007) as well as those characterized in this work, were included in the phylogenetic analyses
Modification of the nomenclature of vertebrate egg-coat ZP gene subfamilies and their patchy phylogenetic distributions The egg-coat ZP proteins characterized in vertebrates are considered a group of conserved proteins (Litscher and Wassarman, 2014)
Summary
Animal egg coats participate in species-specific sperm-egg recognition during the process of fertilization and protect the growth of oocytes, eggs and early-developing embryos (Conner et al, 2005; Litscher and Wassarman, 2014; Modig et al, 2007). Received 29 May 2018; Accepted 18 September 2018 characterized glycoproteins possess a common ZP module with approximately 260 amino acids (Litscher and Wassarman, 2014; Wilburn and Swanson, 2017) and are referred to as ZP glycoproteins regardless of the species from which the egg envelope was isolated (Hedrick, 2008) The genes encoding these glycoproteins have been intensively studied in vertebrates (Conner and Hughes, 2003; Li et al, 2011; Monné et al, 2006; Sano et al, 2013, 2010; Smith et al, 2005; Yue et al, 2014) and organized into six ZP gene subfamilies using an inconsistent nomenclature system (ZP1, ZP2 or ZPA, ZP3 or ZPC, ZP4 or ZPB, ZPD and ZPAX) (Claw and Swanson, 2012; Goudet et al, 2008; Spargo and Hope, 2003). Cloned ZP genes in Xenopus laevis (such as ZPY) have not yet been included in these analyses (Hedrick, 2008)
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