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Evolution and Multiple Origins of Zona Pellucida Genes in Vertebrates Jin-Mei Feng1,*, Hai-Feng Tian2,*, Qiao-Mu Hu2, Yan Meng2 and Han-Bing Xiao2,‡

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Evolution and Multiple Origins of Zona Pellucida Genes in Vertebrates Jin-Mei Feng1,*, Hai-Feng Tian2,*, Qiao-Mu Hu2, Yan Meng2 and Han-Bing Xiao2,‡ © 2018. Published by The Company of Biologists Ltd | Biology Open (2018) 7, bio036137. doi:10.1242/bio.036137 RESEARCH ARTICLE Evolution and multiple origins of zona pellucida genes in vertebrates Jin-Mei Feng1,*, Hai-Feng Tian2,*, Qiao-Mu Hu2, Yan Meng2 and Han-Bing Xiao2,‡ ABSTRACT characterized glycoproteins possess a common ZP module with Animal egg coats are composed of different glycoproteins collectively approximately 260 amino acids (Litscher and Wassarman, 2014; named zona pellucida (ZP) proteins. The characterized vertebrate Wilburn and Swanson, 2017) and are thus referred to as ZP genes encoding ZP proteins have been classified into six subfamilies, glycoproteins regardless of the species from which the egg envelope and exhibit low similarity to the ZP genes characterized in certain was isolated (Hedrick, 2008). The genes encoding these invertebrates. The origin and evolution of the vertebrate ZP genes glycoproteins have been intensively studied in vertebrates (Conner remain obscure. A search against 97 representative metazoan and Hughes, 2003; Li et al., 2011; Monné et al., 2006; Sano et al., species revealed various numbers (ranging from three to 33) of 2013, 2010; Smith et al., 2005; Yue et al., 2014) and organized into different putative egg-coat ZP genes in all 47 vertebrates and several six ZP gene subfamilies using an inconsistent nomenclature system ZP genes in five invertebrate species, but no putative ZP gene was (ZP1, ZP2 or ZPA, ZP3 or ZPC, ZP4 or ZPB, ZPD and ZPAX) found in the other 45 species. Based on phylogenetic and synteny (Claw and Swanson, 2012; Goudet et al., 2008; Spargo and Hope, analyses, all vertebrate egg-coat ZP genes were classified into 2003). The systematic distribution of ZP genes in vertebrates was eight ZP gene subfamilies. Lineage- and species-specific gene recently reviewed (Litscher and Wassarman, 2014; Shu et al., 2015; duplications and gene losses occurred frequently and represented Wu et al., 2018), although the evolutionary relationships among the main causes of the patchy distribution of the eight ZP gene these ZP gene subfamilies remain unresolved. Based on gene subfamilies in vertebrates. Thorough phylogenetic analyses revealed structure and organization and synteny analyses, the ZP genes in that the vertebrate ZP genes could be traced to three independent vertebrates are thought to have been derived from a common origins but were not orthologues of the characterized invertebrate ancestral gene that generated the ZP3 gene subfamily in one branch ZP genes. Our results suggested that vertebrate egg-coat ZP and the ZPD, ZPAX, ZP2, ZP1 and ZP4 gene subfamilies on the genes should be classified into eight subfamilies, and a putative other branch through an ancient gene duplication event (Claw and evolutionary map is proposed. These findings would aid the Swanson, 2012; Litscher and Wassarman, 2014; Spargo and Hope, functional and evolutionary analyses of these reproductive genes 2003). However, ZPX, which is mainly found in invertebrates, in vertebrates. might be the result of a more ancient duplication event, as determined through a phylogenetic analysis (Wong and Wessel, KEY WORDS: Zona pellucida, Egg coat, Vertebrate, Evolution 2006). Moreover, cloned ZP genes in Xenopus laevis (such as ZPY) have not yet been included in these analyses (Hedrick, 2008). INTRODUCTION Interestingly, ZP proteins and their corresponding coding genes Animal egg coats participate in species-specific sperm-egg have also been characterized in cephalochordates (Branchiostoma recognition during the process of fertilization and protect the belcheri) (Xu et al., 2012), urochordates (Ciona savignyi and Ciona growth of oocytes, eggs and early-developing embryos (Conner intestinalis) (Kürn et al., 2007) and the archeogastropod abalone et al., 2005; Litscher and Wassarman, 2014; Modig et al., 2007). (Haliotis spp.) (Aagaard et al., 2010, 2006). These reports suggest Egg coats are called different names in different organisms, such as an invertebrate origin for vertebrate egg-coat ZP genes (Xu et al., vitelline membranes in echinoderms, chorions in fish, vitelline 2012), although a systematic phylogenetic analysis including both envelopes (VEs) in birds, reptiles and amphibians, and zona invertebrate and vertebrate egg-coat ZPs has not yet been pellucida (ZP) in mammals. conducted. Therefore, the origin and evolution of the vertebrate Egg coats are composed of different numbers of glycoproteins, egg-coat ZP genes and the evolutionary relationships between the which also have different names depending on the methods through vertebrate and invertebrate egg-coat ZP genes have yet to be which they were identified (Goudet et al., 2008). All such resolved. Genomic data of diverse metazoans are becoming increasingly available, and this accumulation of data provides excellent 1 Department of Pathogenic Biology, School of Medicine, Jianghan University, opportunities for addressing the evolution of the egg-coat ZP Wuhan, Hubei Province 430056, China. 2Department of Aquaculture and Genetics Breeding, Yangtze River Fisheries Research Institute, Chinese Academy of Fishery genes. In the present study, a comprehensive taxa-wide investigation Sciences, Wuhan 430223, Hubei Province, China. of egg-coat ZP genes was implemented to analyse their *These authors contributed equally to this work phylogenetic distributions in metazoans. Moreover, phylogenetic ‡Author for correspondence ([email protected]) and synteny analyses were conducted to explore the origin and evolution of egg-coat ZP genes. Our results showed that vertebrate H.-B.X., 0000-0002-6389-8204 egg-coat ZP genes should be classified into eight subfamilies This is an Open Access article distributed under the terms of the Creative Commons Attribution contained within the last common ancestor of vertebrates. In License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. addition, these subfamilies could be further traced back to three ancestral ZP genes during the evolution of early vertebrates, but Received 29 May 2018; Accepted 18 September 2018 these three ancestral vertebrate ZP genes do not appear to have been Biology Open 1 RESEARCH ARTICLE Biology Open (2018) 7, bio036137. doi:10.1242/bio.036137 directly inherited from the few invertebrate egg-coat ZP genes. This be products of the same genomic locus (Table S2). The number of work provides a basis for studying these reproductive genes in ZP genes found in each species ranged from three in mammals to 33 different disciplines and performing functional analyses. in Actinopterygii (Table 1), and our search did not find any putative ZP gene in the other 45 species. RESULTS Phylogenetic analyses of these characterized putative ZP genes Phylogenetic distribution of egg-coat ZP genes and were performed to evaluate the definition of ZP gene subfamilies in modification of the ZP gene subfamily definition vertebrates and explore the distributions of ZP members in each After performing the hmm searches and additional confirmations, representative vertebrate species. A total of 410 ZP module regions a total of 446 ZP genes (smart00241: ZP module) were found in (SMART00241, more than 130 amino acids) were obtained and the genome of the 52 investigated representative species, which aligned. To explore the potential origin of these identified vertebrate included 47 vertebrates and five invertebrates. All the identified ZP ZP genes, previously characterized ZP genes of invertebrates genes (with accession numbers, characteristic domains, genomic (Aagaard et al., 2006; Kürn et al., 2007) as well as those data sources and taxonomic information of the studied species) characterized in this work, were included in the phylogenetic are listed in Table S1. The obtained putative ZP genes are non- analyses. The two phylogenetic trees reconstructed using FastTree redundant, and even the 21 ZP genes from four species that showed and PhyML showed similar topologies, and the ML tree (Fig. 1; high identities (no less than 93%) with each other did not appear to Fig. S1) reconstructed using FastTree is shown here. We found six Table 1. Phylogenetic distribution of the ZP genes in vertebrates Number of Evolutionary lineages Species full name ZP genes Vertebrate; Gnathostomata; Tetrapoda; Amniota; Mammalia; Theria; Eutheria; Boreoeutheria Homo sapiens 4 Pan troglodytes 4 Pongo abelii 4 Gorilla gorilla 4 Nomascus leucogenys 4 Macaca mulatta 4 Callithrix jacchus 4 Tarsius (Carlito) syrichta 4 Microcebus murinus 3 Otolemur garnettii 4 Oryctolagus cuniculus 4 Rattus norvegicus 4 Mus musculus 3 Ictidomys tridecemlineatus 4 Cavia porcellus 3 Ailuropoda melanoleuca 4 Canis lupus familiaris 4 Mustela putorius furo 4 Felis catus 4 Equus caballus 4 Sus scrofa 3 Bos taurus 3 Myotis lucifugus 3 Vertebrate; Gnathostomata; Tetrapoda; Amniota; Mammalia; Theria; Eutheria; Afrotheria Loxodonta africana 5 Vertebrate; Gnathostomata; Tetrapoda; Amniota; Mammalia; Theria; Metatheria Monodelphis domestica 4 Macropuseugenii 4 Sarcophilus harrisii 6 Vertebrate; Gnathostomata; Tetrapoda; Amniota;Monotremata Ornithorhynchus anatinus 13 Vertebrate; Gnathostomata; Tetrapoda; Amniota; Sauria Toxicofera Anolis carolinensis 13 Python bivittatus 6 Archosauria Pelodiscus sinensis 16 Gallus gallus 10 Taeniopygia guttata 6 Alligator sinensis 11 Alligator mississippiensis 11 Vertebrate; Gnathostomata; Tetrapoda; Batrachia Anura; Xenopus Xenopus laevis 13
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