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

Elvis Genbo Xu,Daniel Schlenk,Edward M Mager,John D Stieglitz,E Starr Hazard,Gary Hardiman,Martin Grosell

doi:10.1371/journal.pone.0180454

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.

Highlights

Spatial and temporal dynamics of patterns of gene expression during development provides important insights into mechanisms linking genotype with phenotype [1]
During the embryo-to-larval phase, the mechanisms of organogenesis depend on the regulation of genes involved in multiple cellular processes, such as cell proliferation, differentiation, migration, as well as other biological pathways such as protein biosynthesis, and RNA processing [32]
The liver plays a central role in lipid metabolism, carbohydrate metabolism, and urological function [33], and all of these functions were more significantly enriched in transition 2 over transition 1 (Fig 4), consistent with terminal differentiation of the liver during later larval stages

Summary

Introduction

Spatial and temporal dynamics of patterns of gene expression during development provides important insights into mechanisms linking genotype with phenotype [1]. Understanding the early development of susceptible non-model fish is a prerequisite for predicting impacts of contaminants or environmental stress. The Deepwater Horizon (DWH) incident in 2010, the largest marine oil spill in U.S history, resulted in exposure of embryonic and larval life stages of pelagic fish species [4,5,6]. Our previous study demonstrated that crude oil exposure resulted in altered regulation of genes involved in metabolism, steroid biosynthesis, cardiac development, and vision [9]. Since previous studies only evaluated differential expression of the transcriptome comparing oil-treated animals with controls, it is necessary to characterize molecular pathways of normal developmental stages to better understand the impacts of oil

Methods

Results

Conclusion