Analysis of fish ZP1/ZPB homologous genes--evidence for both genome duplication and species-specific amplification models of evolution

Abstract

The vertebrate egg envelope is composed of a family of related proteins, the zona pellucida (ZP) proteins, which are characterized by the presence of a conserved zona pellucida domain. Analysis of teleost fish ZP gene sequences has demonstrated that there are no direct orthologues of the mammalian ZPB and ZP1 genes, but that teleost fish contain multiple copies of two classes of genes (ZPXa and ZPXb) that are equally related to ZPB and ZP1. The two classes of genes are further distinguished by expression in liver or ovary, respectively, indicating there was probably an initial duplication event, followed by a switch to hepatic expression of one of the paralogues. This switch was followed in some species by additional amplification of one of the paralogues with the subsequent loss of the other. It is proposed that the expansion of the number of ZPXa and ZPXb genes and the acquisition of dual sites of synthesis are the result of an ancient polyploidization event, followed by additional species-specific gene amplifications.

Zona pellucida protein ZP2 is expressed in the oocyte of Japanese quail (Coturnix japonica)

“…In addition to the oocytes-restricted expression, the follicular granulosa cells also contribute to the synthesis of ZP3 in rabbits (Lee & Dunbar 1993) and in cynomolgus monkeys (Martinez et al 1996). On the other hand, glycoproteins homologous to ZP glycoproteins in chorion, the fish egg envelope, are produced in the liver and transported to the ovary by the blood circulation, like vitellogenin (Hamazaki et al 1985(Hamazaki et al , 1989, whereas the egg envelope glycoproteins of carp (Cyprinus carpio), goldfish (Carassius auratus), and zebrafish (Danio rerio) appear to be derived from an ovarian source (Conner & Hughes 2003). Our experimental evidence strongly suggests that female germ cells (i.e., the oocyte) also participate in producing the ZP glycoprotein in addition to the ovarian granulosa cells (ZP3 and ZPD) and the liver (ZP1) in avian species.…”

Gamete interactions in teleost fish: the egg envelope. Basic studies and perspectives as environmental biomonitor

“…The ancestral condition for vertebrates is ovary expression (Conner and Hughes, 2003). It has been hypothesized that teleostean fi sh experience a duplication event followed by a switch to hepatic expression of one of the paralogue genes and that the acquisition of dual sites of synthesis is the result of an ancient polyploidization event plus additional species-specifi c gene amplifi cations (Conner and Hughes, 2003). Probably the fi rst step in ZP gene evolution was a gene duplication that might have originated both the ancestral ZPC gene and the precursor of the ZPA, ZPB and ZPX subfamilies.…”

Cracking the egg: increased complexity in the zona pellucida

“…This lack of thoroughness over the genetics of the ZP genes was a major factor in the late discovery of the fourth human ZP gene. The subject of a simplified naming system has been raised by ourselves and others in two recent publications (Conner and Hughes, 2003;Spargo and Hope, 2003). Additionally the nomenclature committee at the National Center for Biotechnology Information (NCBI) have re-categorized the ZP genes.…”

“…Paralogues usually evolve different or more specialized functions], and can be seen to be structurally more closely related than the other ZP proteins, both having a trefoil domain. ZP1 and ZP4 have evolved from a common ancestor as a result of gene duplication (Conner and Hughes, 2003;Spargo and Hope, 2003).…”