Dataset Information

The Genome and Adult Somatic Transcriptome of the Mormyrid Electric Fish Paramormyrops kingsleyae.

ABSTRACT: Several studies have begun to elucidate the genetic and developmental processes underlying major vertebrate traits. Few of these traits have evolved repeatedly in vertebrates, preventing the analysis of molecular mechanisms underlying these traits comparatively. Electric organs have evolved multiple times among vertebrates, presenting a unique opportunity to understand the degree of constraint and repeatability of the evolutionary processes underlying novel vertebrate traits. As there is now a completed genome sequence representing South American electric eels, we were motivated to obtain genomic sequence from a linage that independently evolved electric organs to facilitate future comparative analyses of the evolution and development of electric organs. We report here the sequencing and de novo assembly of the genome of the mormyrid Paramormyrops kingsleyae using short-read sequencing. In addition, we have completed a somatic transcriptome from 11 tissues to construct a gene expression atlas of predicted genes from this assembly, enabling us to identify candidate housekeeping genes as well as genes differentially expressed in the major somatic tissues of the mormyrid electric fish. We anticipate that this resource will greatly facilitate comparative studies on the evolution and development of electric organs and electroreceptors.

SUBMITTER: Gallant JR

PROVIDER: S-EPMC5751062 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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The Genome and Adult Somatic Transcriptome of the Mormyrid Electric Fish Paramormyrops kingsleyae.

Gallant Jason R JR Losilla Mauricio M Tomlinson Chad C Warren Wesley C WC

Genome biology and evolution 20171201 12

Several studies have begun to elucidate the genetic and developmental processes underlying major vertebrate traits. Few of these traits have evolved repeatedly in vertebrates, preventing the analysis of molecular mechanisms underlying these traits comparatively. Electric organs have evolved multiple times among vertebrates, presenting a unique opportunity to understand the degree of constraint and repeatability of the evolutionary processes underlying novel vertebrate traits. As there is now a c ...[more]

PMID: 29240929

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Project description:Electric fishes have independently evolved six times. Most of these fish are weakly electric and they use their discharge mainly for orientation and communication. In the African weakly electric fish genus Campylomormyrus, electric organ discharge (EOD) signals are strikingly different in shape and duration among closely related species, they contribute to pre-zygotic isolation and may have triggered an adaptive radiation. We performed mRNA sequencing on electric organs (EOs) and skeletal muscle (SMs; from which the EOs derive) from three species with short (0.4 ms), medium (5 ms), and long (40 ms) EODs and two different cross-species hybrids. Using pairwise comparison of differential gene expression between EOs and SMs, we identified 1,444 up regulated genes in EO shared by all five species/hybrids cohorts, rendering them candidate genes for EO-specific properties in Campylomormyrus. To understand how gene expression contributes to the variation in EOD duration, we made cross species comparisons among species and tissue. We identified three types of EOD-duration-related expression patterns and several candidate genes, including KCNJ2, KLF5 and SLC24a2, their upregulation may contribute to increased EOD duration, along with a down-regulated gene KCNK6. Hybrids between a short (C. compressirostris) and a long (C. rhynchophorus) discharging species exhibit EODs of intermediate duration and showed imbalanced expression of KCNJ2 alleles. The preferential expression of the C. rhynchophorus allele is in line with a higher expression level in that parental species and points towards a cis-regulatory difference at this locus, relative to EOD duration. A further candidate gene, KLF5, is a transcription factor potentially balancing potassium channel gene expression, a crucial process for the formation of an EOD. Unraveling the genetic basis of the species-specific modulation of the EOD in Campylomormyrus is crucial for understanding the adaptive radiation of this emerging model taxon of ecological (perhaps even sympatric) speciation.

Project description:Electric organs (EOs) have evolved independently in vertebrates six times from skeletal muscle (SM). The transcriptional changes accompanying this developmental transformation are not presently well understood. Mormyrids and gymnotiforms are two highly convergent groups of weakly electric fish that have independently evolved EOs: while much is known about development and gene expression in gymnotiforms, very little is known about development and gene expression in mormyrids. This lack of data limits prospects for comparative work. We report here on the characterization of 28 differentially expressed genes between SM and EO tissues in the mormyrid Brienomyrus brachyistius, which were identified using suppressive subtractive hybridization (SSH). Forward and reverse SSH was performed on tissue samples of EO and SM resulting in one cDNA library enriched with mRNAs expressed in EO, and a second library representing mRNAs unique to SM. Nineteen expressed sequence tags (ESTs) were identified in EO and nine were identified in SM using BLAST searching of Danio rerio sequences available in NCBI databases. We confirmed differential expression of all 28 ESTs using RT-PCR. In EO, these ESTs represent four classes of proteins: (1) ion pumps, including the ?- and ?-subunits of Na(+)/K(+)-ATPase, and a plasma membrane Ca(2+)-ATPase; (2) Ca(2+)-binding protein S100, several parvalbumin paralogs, calcyclin-binding protein and neurogranin; (3) sarcomeric proteins troponin I, myosin heavy chain and actin-related protein complex subunit 3 (Arcp3); and (4) the transcription factors enhancer of rudimentary homolog (ERH) and myocyte enhancer factor 2A (MEF2A). Immunohistochemistry and western blotting were used to demonstrate the translation of seven proteins (myosin heavy chain, Na(+)/K(+)-ATPase, plasma membrane Ca(2+)-ATPase, MEF2, troponin and parvalbumin) and their cellular localization in EO and SM. Our findings suggest that mormyrids express several paralogs of muscle-specific genes and the proteins they encode in EOs, unlike gymnotiforms, which may post-transcriptionally repress several sarcomeric proteins. In spite of the similarity in the physiology and function of EOs in mormyrids and gymnotiforms, this study indicates that the mechanisms of development in the two groups may be considerably different.

Project description:African weakly electric fish of the mormyrid genus Campylomormyrus generate pulse-type electric organ discharges (EODs) for orientation and communication. Their pulse durations are species-specific and elongated EODs are a derived trait. So far, differential gene expression among tissue-specific transcriptomes across species with different pulses and point mutations in single ion channel genes indicate a relation of pulse duration and electrocyte geometry/excitability. However, a comprehensive assessment of expressed Single Nucleotide Polymorphisms (SNPs) throughout the entire transcriptome of African weakly electric fish, with the potential to identify further genes influencing EOD duration, is still lacking. This is of particular value, as discharge duration is likely based on multiple cellular mechanisms and various genes. Here we provide the first transcriptome-wide SNP analysis of African weakly electric fish species (genus Campylomormyrus) differing by EOD duration to identify candidate genes and cellular mechanisms potentially involved in the determination of an elongated discharge of C. tshokwe. Non-synonymous substitutions specific to C. tshokwe were found in 27 candidate genes with inferred positive selection among Campylomormyrus species. These candidate genes had mainly functions linked to transcriptional regulation, cell proliferation and cell differentiation. Further, by comparing gene annotations between C. compressirostris (ancestral short EOD) and C. tshokwe (derived elongated EOD), we identified 27 GO terms and 2 KEGG pathway categories for which C. tshokwe significantly more frequently exhibited a species-specific expressed substitution than C. compressirostris. The results indicate that transcriptional regulation as well cell proliferation and differentiation take part in the determination of elongated pulse durations in C. tshokwe. Those cellular processes are pivotal for tissue morphogenesis and might determine the shape of electric organs supporting the observed correlation between electrocyte geometry/tissue structure and discharge duration. The inferred expressed SNPs and their functional implications are a valuable resource for future investigations on EOD durations.

Dataset Information

The Genome and Adult Somatic Transcriptome of the Mormyrid Electric Fish Paramormyrops kingsleyae.

Publications

The Genome and Adult Somatic Transcriptome of the Mormyrid Electric Fish Paramormyrops kingsleyae.

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