Bioinformatic analyses of zona pellucida genes in vertebrates and their expression in Nile tilapia

Abstract

Zona pellucida (ZP) genes encode ZP glycoproteins which constitute the coat surrounding oocytes and early embryos. Genome-wide identification of ZP genes is still lacking in vertebrates, especially in fish species. Herein, we conducted bioinformatic analyses of the ZP genes of the Nile tilapia and other vertebrates. Totally 16, 9, 17, 27, 21, 20, 26, 19, 14,11, 24, 17, 9, 18, 8, 11, 9, 8, 5, and 4 ZP genes belonging to 5 subfamilies (ZPA, ZPB, ZPC, ZPD, and ZPAX) were found in the sea lamprey, elephant shark, coelacanth, spotted gar, zebrafish, medaka, stickleback, Nile tilapia, Amazon molly, platyfish, seahorse, Northern snakehead, cavefish, tetraodon, clawed frog, turtle, chicken, platypus, kangaroo rat, and human genomes, respectively. The expansion of ZP genes in basal vertebrates was mainly achieved by gene duplication of ZPB, ZPC, and ZPAX subfamilies, while the shrink of ZP gene number in viviparous mammals was achieved by keeping only one copy of the ZP genes in each subfamily or even secondary loss of some subfamilies. The number of ZP gene is related to the environment where the eggs are fertilized and the embryos develop in vertebrates. Transcriptomic analysis showed that 14 ZP genes were expressed in the ovary of Nile tilapia, while two (ZPB2b and ZPC2) were highly expressed in the liver. On the other hand, ZPB1a and ZPB2c were not found to be expressed in any tissue or at any developmental stage of the gonads examined. In the ovary, the expression of ZP genes started from 30 dah (days after hatching), significantly upregulated at 90 dah and maintained this level at 180 dah. The expression of ZPC2 in the liver and ZPC5-2 and ZPAX1 in the ovary was confirmed by in situ hybridization. The ovary- and liver-expressed ZP genes are expressed coordinately with oocyte growth in tilapia.

Antarctic blackfin icefish genome reveals adaptations to extreme environments

“…9). The ovaries and liver express zona pellucida genes in vertebrates 44 , and most C. aceratus zona pellucida genes were strongly expressed in the ovaries, similar to three other Antarctic fish 12 ( Supplementary Fig. 10), although transcription of several zona pellucida genes was detected in other C. aceratus organs.…”

Comparative transcriptome analysis of the ovary and testis of the lacustrine goby (Gobiopterus lacustris)

“…On the zona pellucida (ZP), sperm receptor activity is associated with glycoproteins ZP3 and ZP2 [58]. In fish, zps are mainly expressed in the ovary, and we found higher expression levels for zp2, zp3, and zp4 in the ovary (Table S3), suggesting that these zps may also play important roles in oocyte development and fertilization [14,59,60]. As a member of the TGF-β family, inhibins (inha and inhb) play important roles in the development of vertebrate, especially mammalian gametes [61].…”

Evolution and multiple origins of zona pellucida genes in vertebrates

“…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. Based on gene structure and organization and synteny analyses, the ZP genes in vertebrates are thought to have been derived from a common ancestral gene that generated the ZP3 gene subfamily in one branch and the ZPD, ZPAX, ZP2, ZP1 and ZP4 gene subfamilies on the other branch through an ancient gene duplication event ( Claw and Swanson, 2012 ; Litscher and Wassarman, 2014 ; Spargo and Hope, 2003 ).…”