Molecular characterization of the cDNAs of two zona pellucida genes in the Chinese sturgeon,Acipenser sinensisGray, 1835

Abstract

SummaryThe Chinese sturgeon, Acipenser sinensis, is a large-sized panadromous cartilagous fish and requires more than ten years to reach sexual maturity. An understanding of the reproductive organs and fertilization process is a precondition for controlled reproduction of this endangered species. The developing oocyte is surrounded by an extracellular matrix composed of the zona pellucide (ZP) protein in several isoforms, all of which play important roles in fertilization and embryo protection. The present study reports the identification of two ZP genes, AsZPAX and AsZPB, in this fish. The full-length cDNAs of AsZPAX and AsZPB were 2950 base pairs (bp) and 1832 bp, predicting proteins of 946 and 592 amino acid residues, respectively. Both proteins have a conserved ZP domain. In a gene tree, AsZPAX and AsZPB were respectively clustered with their counterparts in other vertebrates. Tissue distribution analysis demonstrated that the AsZPAX RNA was transcribed in both the ovary and the liver, while AsZPB was transcribed exclusively in the ovary. RNA in situ hybridization revealed apparent RNA expression of both AsZPAX and AsZPB in growing oocytes of the 4-year-old ovary.

Previtellogenic and vitellogenic oocytes in ovarian follicles of cultured siberian sturgeon Acipenser baerii (Chondrostei, Acipenseriformes)

“…Transcripts of boule and dazl , and germ cell‐specific RNA‐binding proteins Boule and Dazl represent similar localization in ovaries of A. sinensis (Ye et al, ). In this species, in previtellogenic oocytes in ovaries of 4‐year‐old specimens AsZPAX and AsZPB , the zona pellucida RNAs are detected in the oocyte nucleus, ooplasm, egg envelopes and in peripheries of ovarian follicles (Yue et al, ). In specimens of A. gueldenstaedtii and of A. baerii cultured in indoor tanks and in aquaria, the oocyte nucleus, perinuclear ooplasm and granules located in the ooplasm stain with anti‐proliferating cell nuclear antigen (PCNA) antibody that recognizes a PCNA (Rzepkowska and Ostaszewska, ).…”

“…Meiosis in oocytes proceeds until the diplotene stage and is arrested for an extended period of time (Raikova, ; Dettlaff et al, ; Le Menn et al, ). During this stage, termed dictyotene oocytes grow and accumulate organelles and macromolecules (Le Menn and Pelissero, ; Le Menn et al, ; Lyman‐Gingerich and Pelegri, ; Zelazowska et al, ; Lubzens et al, ; Ye et al, ; Yue et al, ; Yang et al, ). Three phases of oocyte development are distinguished: previtellogenesis, vitellogenesis (accumulation of yolk) and choriogenesis (deposition of egg envelopes; Raikova, ; Selman and Wallace, ; Le Menn and Pelissero, ; Le Menn et al, ; Zelazowska et al, ; Lubzens et al, ; Żelazowska, ).…”

Previtellogenic oocytes of South African largemouth bass Micropterus salmoides Lacépède 1802 (Actinopterygii, Perciformes) ‐ the Balbiani body, cortical alveoli and developing eggshell

“…It has also been investigated in teleost fish, for example, in zebrafish Danio rerio (Elkouby, ; Elkouby et al, ; Elkouby & Mullins, ; Lyman‐Gingerich & Pelegri, ; Marlow & Mullins, ), rainbow trout Salmo gairdneri (Beams & Kessel, ), golden grey mullet Mugil (Liza) auratus (Bruslé, ), medaka Oryzias latipes (Iwamatsu & Nakashima, ; Kobayashi & Iwamatsu, ; Nakamura et al, ), and in the Atlantic salmon Salmo salar (Škugor, Tveiten, Johnsen, & Andersen, ). It is also present in oocytes of several species of sturgeons and paddlefish (Chondrostei, Acipenseriformes); for example, in the Russian sturgeon, Acipenser gueldenstaedtii (Zelazowska et al, ; Żelazowska, Jankowska, Plewniak, & Rajek, ), Siberian sturgeon, A. baerii (Żelazowska & Fopp‐Bayat, , ), Chinese, A. sinensis , Dabry's, A. dabryanus sturgeons (Yang, Yue, Ye, Li, & Wei, ; Ye et al, ; Ye, Li, Yue, Yang, & Wei, ; Ye, Yue, Yang, Li, & Wei, ; Yue et al, ), the North American paddlefish, Polyodon spathula (Żelazowska et al, ; Żelazowska & Kilarski, ) as well as in numerous species of invertebrates (e.g., Bilinski et al, ; Kloc, Jedrzejowska, Tworzydlo, & Bilinski, ). In all species investigated, the Balbiani body is involved in the development of ooplasm polarity and marks the future vegetal region or vegetal pole in the oocytes.…”

Evolution and multiple origins of zona pellucida genes in vertebrates

“…All such characterized glycoproteins possess a common ZP module with approximately 260 amino acids ( Litscher and Wassarman, 2014 ; Wilburn and Swanson, 2017 ) and are thus 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 ). The systematic distribution of ZP genes in vertebrates was recently reviewed ( Litscher and Wassarman, 2014 ; Shu et al, 2015 ; Wu et al, 2018 ), although the evolutionary relationships among these ZP gene subfamilies remain unresolved.…”