Neofunctionalization of zona pellucida proteins enhances freeze-prevention in the eggs of Antarctic notothenioids

Nat Commun. 2016 Oct 4:7:12987. doi: 10.1038/ncomms12987.

Abstract

The mechanisms by which the eggs of the Antarctic notothenioid fishes avoid freezing are not fully understood. Zona pellucida proteins (ZPs) are constituents of the chorion which forms a protective matrix surrounding the egg. Here we report occurrence of freezing temperature-related gene expansion and acquisition of unusual ice melting-promoting (IMP) activity in a family of Antarctic notothenioid ZPs (AnnotoZPs). Members of AnnotoZPs are shown to bind with ice and non-colligatively depress the melting point of a solution in a range of 0.26 to 0.65 °C at a moderate concentration. Eggs of zebrafishes expressing an AnnotoZP transgene show improved melting point depression and enhanced survival in freezing conditions. Mutational analyses in a representative AnnotoZP indicate the ZP domain and patches of acidic residues are essential structures for the IMP activity. AnnotoZPs, therefore, represent a group of macromolecules that prevent freezing by a unique ZP-ice interaction mechanism distinct from the known antifreeze proteins.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological*
  • Animals
  • Antarctic Regions
  • Antifreeze Proteins / physiology*
  • Cold Temperature
  • DNA Mutational Analysis
  • Expressed Sequence Tags
  • Freezing*
  • Genome
  • Models, Molecular
  • Oocytes / physiology*
  • Phylogeny
  • Protein Conformation
  • Recombinant Proteins / metabolism
  • Temperature
  • Transgenes
  • Zebrafish / genetics
  • Zebrafish / physiology*
  • Zona Pellucida / physiology*

Substances

  • Antifreeze Proteins
  • Recombinant Proteins