Developmental transcriptomic analyses for mechanistic insights into critical pathways involved in embryogenesis of pelagic mahi-mahi (Coryphaena hippurus)

PLoS One. 2017 Jul 10;12(7):e0180454. doi: 10.1371/journal.pone.0180454. eCollection 2017.

Abstract

Mahi-mahi (Coryphaena hippurus) is a commercially and ecologically important species of fish occurring in tropical and temperate waters worldwide. Understanding early life events is crucial for predicting effects of environmental stress, which is largely restricted by a lack of genetic resources regarding expression of early developmental genes and regulation of pathways. The need for anchoring developmental stages to transcriptional activities is highlighted by increasing evidence on the impacts of recurrent worldwide oil spills in this sensitive species during early development. By means of high throughput sequencing, we characterized the developmental transcriptome of mahi-mahi at three critical developmental stages, from pharyngula embryonic stage (24 hpf) to 48 hpf yolk-sac larva (transition 1), and to 96 hpf free-swimming larva (transition 2). With comparative analysis by multiple bioinformatic tools, a larger number of significantly altered genes and more diverse gene ontology terms were observed during transition 2 than transition 1. Cellular and tissue development terms were more significantly enriched in transition 1, while metabolism related terms were more enriched in transition 2, indicating a switch progressing from general embryonic development to metabolism during the two transitions. Special focus was given on the most significant common canonical pathways (e.g. calcium signaling, glutamate receptor signaling, cAMP response element-binding protein signaling, cardiac β-adrenergic signaling, etc.) and expression of developmental genes (e.g. collagens, myosin, notch, glutamate metabotropic receptor etc.), which were associated with morphological changes of nervous, muscular, and cardiovascular system. These data will provide an important basis for understanding embryonic development and identifying molecular mechanisms of abnormal development in fish species.

MeSH terms

  • Animals
  • Ecosystem*
  • Embryo, Nonmammalian / metabolism
  • Embryonic Development / genetics*
  • Gene Expression Profiling / methods*
  • Gene Expression Regulation, Developmental
  • Gene Ontology
  • Larva / genetics
  • Perciformes / embryology*
  • Perciformes / genetics*
  • Sequence Analysis, RNA
  • Signal Transduction / genetics*
  • Takifugu / embryology
  • Takifugu / genetics

Grants and funding

This research was made possible by a grant from The Gulf of Mexico Research Initiative, Grant No: SA-1520; Name: Relationship of Effects of Cardiac Outcomes in fish for Validation of Ecological Risk (RECOVER). The authors are grateful to the Gulf of Mexico Research Initiative Information and Data Cooperative (GRIIDC) for supporting data management system to store the data generated. GRIIDC doi:10.7266/N7GX48ND. GH acknowledges the Medical University of South Carolina College of Medicine for start-up funds. This research was supported in part by the Genomics Shared Resource, Hollings Cancer Center. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.