Inferring the Evolution of Teleostean zp Genes Based on Their Sites of Expression

Abstract

Fish egg envelopes consist of several glycoproteins, called zona pellucida (ZP) proteins, which are conserved among chordates. Euteleosts synthesize ZP proteins in the liver, while elopomorphs synthesize them in the ovaries. In Cypriniformes, zp genes are expressed in the ovaries. We investigated the zp genes of two Otocephalan orders: Clupeiformes (Pacific herring and Japanese anchovy) and Gonorynchiformes (milkfish), which diverged earlier than Cypriniformes. cDNA cloning of zp gene homologs revealed that Pacific herring and Japanese anchovy possessed both ovary- and liver-expressed zp genes; however, the zp genes of milkfish were only expressed in the ovaries. Molecular phylogenetic analysis showed that ovary- and liver-expressed zpc genes of two the Clupeiformes formed independent clades. Based on this, we hypothesized the evolution of teleostean zp genes, focusing on the organ expressing zp gene. As in other chordates, the original site of expression of zp genes was likely the ovary. In the early stage of teleostean evolution, the ancestral zp genes acquired the ability to express in the liver. Later, one of the two expression sites became dominant. The liver-expressed zp genes are component proteins of the egg envelope in the Euteleostei. In Otocephala, Clupeiformes possess both ovary- and liver-expressed genes that presumably participate in egg envelope formation, whereas the Gonorynchiformes and Cypriniformes have primarily preserved ovary expressed zp genes.

Comparison of Egg Envelope Thickness in Teleosts and its Relationship to the Sites of ZP Protein Synthesis

“…Subsequently, liver‐expressed ZP genes were produced by duplication and diversification in a common ancestor of Euteleostei and Otocephala (Kawaguchi et al., , ). All euteleost fish and Clupeiformes, which is diverged early from Otocephala, have both ovarian‐ and liver‐expressing ZP genes (Sano et al., ). The liver‐expressing ZP genes in Otocephala have lost the evolutionary process to Ostariophysi, and the egg envelopes of Ostariophysi, such as milkfish, zebrafish, carp, and goldfish, are composed of ovarian‐synthesized ZP proteins (Chang et al., , ; Sano et al., , ; Wang et al., ).…”

“…All euteleost fish and Clupeiformes, which is diverged early from Otocephala, have both ovarian‐ and liver‐expressing ZP genes (Sano et al., ). The liver‐expressing ZP genes in Otocephala have lost the evolutionary process to Ostariophysi, and the egg envelopes of Ostariophysi, such as milkfish, zebrafish, carp, and goldfish, are composed of ovarian‐synthesized ZP proteins (Chang et al., , ; Sano et al., , ; Wang et al., ). The egg envelopes of euteleost species have been particularly well studied, and their egg envelopes are principally composed of liver‐synthesized ZP proteins (Hamazaki et al., , Murata et al., ).…”

“…We recently cloned ZP genes from two species of Clupeiformes (Pacific herring [ Clupea pallasii ] and Japanese anchovy [ Engraulis japonicas ]). We discovered that these species possess both ovarian‐expressed and liver‐expressed ZP genes, and that the expression levels of the liver‐expressed ZP genes are much stronger than those of ovarian‐expressed ZP genes (Sano et al., ). In this study, we analyzed the amino acid sequences of the egg envelope proteins extracted from unfertilized egg envelopes of Japanese anchovy and revealed that the major components of the egg envelope proteins were liver‐synthesized ZP proteins.…”

“…Thus, we chose Pacific herring as another clupeiform species to investigate in the present study. We have already reported the sequences and expression of the ZP genes (Sano et al., ); however, no protein level analysis has been performed, so we conducted biochemical and immunohistochemical experiments. Furthermore, in our previous study, we documented that the inner layer of the Pacific herring egg envelope consists of two distinct layers (Sano et al., ), unlike many teleost egg envelopes, which are constructed of a single lamellar layer structure (Yamamoto and Yamagami, ; Sano et al., ; Kawaguchi et al., , ).…”

Male parental assistance in embryo hatching of barred‐chin blenny Rhabdoblennius nitidus

“…Teleostean ZP proteins categorized the glycoproteins, ZPB and ZPC. In euteleosts, ZPB is derived from either choriogenin H (ChgH) or H minor (ChgHm), and ZPC is derived from choriogenin L (ChgL; Fujita, Fukuda, Shimizu, Hiramatsu, & Hara, 2008;Sano et al, 2013;Sano, Kawaguchi, Yoshikawa, Iuchi, & Yasumasu, 2010). At the time of hatching, an embryo secretes hatching enzymes to digest the egg envelope.…”