The myogenic electric organ of Sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptome

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...

Full description

Bibliographic Details
Main Authors: Matthew Pinch, Robert Güth, Manoj P. Samanta, Alexander Chaidez, Graciela A. Unguez
Format: Article
Language:English
Published: PeerJ Inc. 2016-04-01
Series:PeerJ
Subjects:
Online Access:https://peerj.com/articles/1828.pdf
id doaj-eca2631cae7843cb9bc52c6b409734fc
record_format Article
spelling doaj-eca2631cae7843cb9bc52c6b409734fc2020-11-25T02:29:36ZengPeerJ Inc.PeerJ2167-83592016-04-014e182810.7717/peerj.1828The myogenic electric organ of Sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptomeMatthew Pinch0Robert Güth1Manoj P. Samanta2Alexander Chaidez3Graciela A. Unguez4Department of Biology, New Mexico State University, Las Cruces, NM, United StatesDepartment of Biology, New Mexico State University, Las Cruces, NM, United StatesSystemix Institute, Redmond, WA, United StatesDepartment of Biology, New Mexico State University, Las Cruces, NM, United StatesDepartment of Biology, New Mexico State University, Las Cruces, NM, United StatesIn 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.https://peerj.com/articles/1828.pdfTranscriptomeSkeletal muscleElectric organElectric fishMyogenic regulatory factorsMyogenic transcriptome
collection DOAJ
language English
format Article
sources DOAJ
author Matthew Pinch
Robert Güth
Manoj P. Samanta
Alexander Chaidez
Graciela A. Unguez
spellingShingle Matthew Pinch
Robert Güth
Manoj P. Samanta
Alexander Chaidez
Graciela A. Unguez
The myogenic electric organ of Sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptome
PeerJ
Transcriptome
Skeletal muscle
Electric organ
Electric fish
Myogenic regulatory factors
Myogenic transcriptome
author_facet Matthew Pinch
Robert Güth
Manoj P. Samanta
Alexander Chaidez
Graciela A. Unguez
author_sort Matthew Pinch
title The myogenic electric organ of Sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptome
title_short The myogenic electric organ of Sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptome
title_full The myogenic electric organ of Sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptome
title_fullStr The myogenic electric organ of Sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptome
title_full_unstemmed The myogenic electric organ of Sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptome
title_sort myogenic electric organ of sternopygus macrurus: a non-contractile tissue with a skeletal muscle transcriptome
publisher PeerJ Inc.
series PeerJ
issn 2167-8359
publishDate 2016-04-01
description 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.
topic Transcriptome
Skeletal muscle
Electric organ
Electric fish
Myogenic regulatory factors
Myogenic transcriptome
url https://peerj.com/articles/1828.pdf
work_keys_str_mv AT matthewpinch themyogenicelectricorganofsternopygusmacrurusanoncontractiletissuewithaskeletalmuscletranscriptome
AT robertguth themyogenicelectricorganofsternopygusmacrurusanoncontractiletissuewithaskeletalmuscletranscriptome
AT manojpsamanta themyogenicelectricorganofsternopygusmacrurusanoncontractiletissuewithaskeletalmuscletranscriptome
AT alexanderchaidez themyogenicelectricorganofsternopygusmacrurusanoncontractiletissuewithaskeletalmuscletranscriptome
AT gracielaaunguez themyogenicelectricorganofsternopygusmacrurusanoncontractiletissuewithaskeletalmuscletranscriptome
AT matthewpinch myogenicelectricorganofsternopygusmacrurusanoncontractiletissuewithaskeletalmuscletranscriptome
AT robertguth myogenicelectricorganofsternopygusmacrurusanoncontractiletissuewithaskeletalmuscletranscriptome
AT manojpsamanta myogenicelectricorganofsternopygusmacrurusanoncontractiletissuewithaskeletalmuscletranscriptome
AT alexanderchaidez myogenicelectricorganofsternopygusmacrurusanoncontractiletissuewithaskeletalmuscletranscriptome
AT gracielaaunguez myogenicelectricorganofsternopygusmacrurusanoncontractiletissuewithaskeletalmuscletranscriptome
_version_ 1724832111217606656