Effects of hatching enzymes on egg envelope digestion in the male‐brooding seahorse

In the present study, we aimed to evaluate the effects of hatching enzymes on the egg envelope digestion during the hatching period in the male brooding seahorse. The complementary DNAs encoding two hatching‐enzyme genes, high choriolytic enzyme (HCE) and low choriolytic enzyme (LCE), were cloned and functionally characterized from the lined seahorse (Hippocampus erectus). The genomic‐synteny analysis confirmed that teleosts shared LCE gene synteny. In contrast, the genomic location of HCE was found to be conserved with pipefish, but not other teleosts, suggesting that translocation into a novel genomic location occurred. Whole‐mount in situ hybridization showed that HCE and LCE mRNAs were expressed in hatching gland cells. To determine the digestion mechanisms of HCE and LCE in hatching, recombinant HCE and LCE were generated and their enzyme activities were examined using fertilized egg envelopes and synthetic peptides. Seahorse HCE and LCE independently digested and softened the egg envelopes of the lined seahorse. Although the egg envelope was digested more following HCE and LCE co‐treatment, envelope solubilization was not observed. Indeed, both HCE and LCE showed similar substrate specificities toward four different synthetic peptides designed from the cleavage sites of egg envelope proteins. HCE and LCE proteins from other euteleostean fishes showed different specificities, and the egg envelope was solubilized by the cooperative action of HCE and LCE. These results suggest that the function of LCE was degenerated in the lined seahorse. Our results imply a digestion mechanism for evolutionary adaptation in ovoviviparous fish with male pregnancy.

• Publication year

  2021

• Venue

  Molecular Reproduction and Development

• Publication date

  2021-05-07

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1002/mrd.23474PMID 33960059
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Effects of food, salinity, and ammonia-nitrogen on the physiology of juvenile seahorse (Hippocampus erectus) in two typical culture models in China

  2020influential reference
• Translocation of promoter-conserved hatching enzyme genes with intron-loss provides a new insight in the role of retrocopy during teleostean evolution

  2019influential reference
• Male parental assistance in embryo hatching of barred-chin blenny Rhabdoblennius nitidus.

  2019cited by this paper
• Comparison of Egg Envelope Thickness in Teleosts and its Relationship to the Sites of ZP Protein Synthesis

  2017cited by this paper
• Draft genome of the lined seahorse, Hippocampus erectus

  2017cited by this paper
• An evolutionary insight into the hatching strategies of pipefish and seahorse embryos.

  2016cited by this paper
• Fishes of the World: Nelson/Fishes of the World

  2016cited by this paper
• Molecular events in adaptive evolution of the hatching strategy of ovoviviparous fishes.

  2015cited by this paper
• Molecular co-evolution of a protease and its substrate elucidated by analysis of the activity of predicted ancestral hatching enzyme

  2013cited by this paper
• MEGA6: Molecular Evolutionary Genetics Analysis version 6.0.

  2013influential reference
• Sub-functionalization of duplicated genes in the evolution of nine-spined stickleback hatching enzyme.

  2013cited by this paper
• Mechanism of egg envelope digestion by hatching enzymes, HCE and LCE in medaka, Oryzias latipes.

  2010cited by this paper
• Conservation of the egg envelope digestion mechanism of hatching enzyme in euteleostean fishes

  2010cited by this paper
• Breeding and juvenile culture of the lined seahorse, Hippocampus erectus Perry,1810

  2008cited by this paper
• Hatching enzyme of the ovoviviparous black rockfish Sebastes schlegelii– environmental adaptation of the hatching enzyme and evolutionary aspects of formation of the pseudogene

  2008influential reference
• Clustal W and Clustal X version 2.0

  2007cited by this paper
• Male pregnancy in seahorses and pipefish: beyond the mammalian model

  2007cited by this paper
• Analysis of the exon-intron structures of fish, amphibian, bird and mammalian hatching enzyme genes, with special reference to the intron loss evolution of hatching enzyme genes in Teleostei.

  2007cited by this paper
• Evolution of teleostean hatching enzyme genes and their paralogous genes

  2006cited by this paper
• Purification and gene cloning of Fundulus heteroclitus hatching enzyme

  2005cited by this paper
• Structure and developmental expression of hatching enzyme genes of the Japanese eel Anguilla japonica: an aspect of the evolution of fish hatching enzyme gene

  2004cited by this paper
• Cloning and expression of high choriolytic enzyme, a component of the hatching enzyme system, during embryonic development of the marine ornamental fish Chrysiptera parasema

  2004cited by this paper
• Male pregnancy in seahorses and pipefishes (family Syngnathidae): rapid diversification of paternal brood pouch morphology inferred from a molecular phylogeny.

  2001cited by this paper
• Species-dependent migration of fish hatching gland cells that express astacin-like proteases in common [corrected].

  1997cited by this paper
• Studies on the Hatching Enzyme (Choriolysin) and Its Substrate, Egg Envelope, Constructed of the Precursors (Choriogenins) in Oryzias latipes: A Sequel to the Information in 1991/1992

  1996cited by this paper
• cDNAs and the Genes of HCE and LCE, Two Constituents of the Medaka Hatching Enzyme

  1994cited by this paper
• [Hatching enzyme].

  1992cited by this paper
• Isolation and some properties of low choriolytic enzyme (LCE), a component of the hatching enzyme of the teleost, Oryzias latipes.

  1989cited by this paper
• Purification and partial characterization of high choriolytic enzyme (HCE), a component of the hatching enzyme of the teleost, Oryzias latipes.

  1989cited by this paper
• Viviparity: The Maternal-Fetal Relationship in Fishes

  1981cited by this paper
• Isolation of a choriolytic enzyme (hatching enzyme) of the teleost, Oryzias latipes.

  1972cited by this paper

• QNZ exposure induces development toxicity and mechanisms of hatching inhibition in large-scale loach (Paramisgurnus dabryanus) embryos.

  2023cites this paper
• Molecular cloning, characterization, and expression patterns of the hatching enzyme genes during embryonic development of pikeperch (Sander lucioperca)

  2022cites this paper