Abstract

In most electric fish species, the electric organ (EO) derives from striated muscle cells that suppress many muscle properties. In the gymnotiform Sternopygus macrurus, mature electrocytes, the current-producing cells of the EO, do not contain sarcomeres, yet they continue to make some cytoskeletal and sarcomeric proteins and the muscle transcription factors (MTFs) that induce their expression. In order to more comprehensively examine the transcriptional regulation of genes associated with the formation and maintenance of the contractile sarcomere complex, results from expression analysis using qRT-PCR were informed by deep RNA sequencing of transcriptomes and miRNA compositions of muscle and EO tissues from adult S. macrurus. Our data show that: (1) components associated with the homeostasis of the sarcomere and sarcomere-sarcolemma linkage were transcribed in EO at levels similar to those in muscle; (2) MTF families associated with activation of the skeletal muscle program were not differentially expressed between these tissues; and (3) a set of microRNAs that are implicated in regulation of the muscle phenotype are enriched in EO. These data support the development of a unique and highly specialized non-contractile electrogenic cell that emerges from a striated phenotype and further differentiates with little modification in its transcript composition. This comprehensive analysis of parallel mRNA and miRNA profiles is not only a foundation for functional studies aimed at identifying mechanisms underlying the transcription-independent myogenic program in S. macrurus EO, but also has important implications to many vertebrate cell types that independently activate or suppress specific features of the skeletal muscle program.

Highlights

  • Skeletal muscles are crucial for animals to perform behaviors that are necessary for survival in a changeable environment

  • In the present study we extended our analyses of the regulation of sarcomere gene expression in S. macrurus electrocytes to include sets of genes associated with different regions of the sarcomere, i.e., the costamere, Z-disk and I-A-M band, protein degradation pathways including the ubiquitin-proteasome system (UPS) and the autophagy pathway, and transcription factors known to regulate the myogenic phenotype other than the MyoD family

  • Transcript levels of genes associated with different regions of the sarcomere were characterized in skeletal muscle and electric organ (EO) of adult S. macrurus

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Summary

Introduction

Skeletal muscles are crucial for animals to perform behaviors that are necessary for survival in a changeable environment. Cell signaling pathways and key regulatory factors associated with inducing the skeletal muscle phenotype, but specific muscle fiber type properties have been discovered (Buckingham & Rigby, 2014; Schiaffino & Reggiani, 2011; McCarthy, 2011). Together, data from these studies have led to our current understanding that changes in environmental and intrinsic factors can affect gene transcription, or expression of genes, including turning genes completely on or off, or adjusting the levels of transcripts produced, and as a result influence muscle cell fate decisions throughout the life of the organism. Studies on vertebrates wherein regulation of subsets of muscle genes are independently activated or repressed, and can be studied with high precision, are likely to further our understanding of some of these basic processes in muscle biology

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