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Cross-tissue and cross-species analysis of gene expression in skeletal muscle and electric organ of African weakly-electric fish (Teleostei; Mormyridae).

Lamanna F, Kirschbaum F, Waurick I, Dieterich C, Tiedemann R - BMC Genomics (2015)

Bottom Line: In silico cross-tissue DE-analysis allowed us to identify 271 shared differentially expressed genes between EO and SM in C. compressirostris and C.tshokwe.Many of these genes correspond to myogenic factors, ion channels and pumps, and genes involved in several metabolic pathways.Cross-species analysis has revealed that the electric organ transcriptome is more variable in terms of gene expression levels across species than the skeletal muscle transcriptome.

View Article: PubMed Central - PubMed

Affiliation: Unit of Evolutionary Biology/Systematic Zoology, Institute of Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Strasse 24-25, Potsdam, Germany. lamanna@uni-potsdam.de.

ABSTRACT

Background: African weakly-electric fishes of the family Mormyridae are able to produce and perceive weak electric signals (typically less than one volt in amplitude) owing to the presence of a specialized, muscle-derived electric organ (EO) in their tail region. Such electric signals, also known as Electric Organ Discharges (EODs), are used for objects/prey localization, for the identification of conspecifics, and in social and reproductive behaviour. This feature might have promoted the adaptive radiation of this family by acting as an effective pre-zygotic isolation mechanism. Despite the physiological and evolutionary importance of this trait, the investigation of the genetic basis of its function and modification has so far remained limited. In this study, we aim at: i) identifying constitutive differences in terms of gene expression between electric organ and skeletal muscle (SM) in two mormyrid species of the genus Campylomormyrus: C. compressirostris and C. tshokwe, and ii) exploring cross-specific patterns of gene expression within the two tissues among C. compressirostris, C. tshokwe, and the outgroup species Gnathonemus petersii.

Results: Twelve paired-end (100 bp) strand-specific RNA-seq Illumina libraries were sequenced, producing circa 330 M quality-filtered short read pairs. The obtained reads were assembled de novo into four reference transcriptomes. In silico cross-tissue DE-analysis allowed us to identify 271 shared differentially expressed genes between EO and SM in C. compressirostris and C.tshokwe. Many of these genes correspond to myogenic factors, ion channels and pumps, and genes involved in several metabolic pathways. Cross-species analysis has revealed that the electric organ transcriptome is more variable in terms of gene expression levels across species than the skeletal muscle transcriptome.

Conclusions: The data obtained indicate that: i) the loss of contractile activity and the decoupling of the excitation-contraction processes are reflected by the down-regulation of the corresponding genes in the electric organ's transcriptome; ii) the metabolic activity of the EO might be specialized towards the production and turn-over of membrane structures; iii) several ion channels are highly expressed in the EO in order to increase excitability; iv) several myogenic factors might be down-regulated by transcription repressors in the EO.

No MeSH data available.


Related in: MedlinePlus

Distribution of length coverage between Campylomormyrus Trinity transcripts and corresponding top-blast hits (D. rerio proteome). Histogram showing the distribution of the percent in length of the sequences in the D. rerio proteome that aligns to the assembled Trinity contigs. Numbers on the x-axis indicate the upper limit of the binned interval (e.g., 100 is the upper value of the interval 100–91). a Cross-tissue comparison. b Cross-species comparison
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Fig2: Distribution of length coverage between Campylomormyrus Trinity transcripts and corresponding top-blast hits (D. rerio proteome). Histogram showing the distribution of the percent in length of the sequences in the D. rerio proteome that aligns to the assembled Trinity contigs. Numbers on the x-axis indicate the upper limit of the binned interval (e.g., 100 is the upper value of the interval 100–91). a Cross-tissue comparison. b Cross-species comparison

Mentions: Sequencing of the twelve cDNA libraries produced a total amount of 371,043,357raw read pairs, resulting in 330,595,546 quality-filtered read pairs (89.1 %); see Additional file 1 for per library sequencing statistics. Trinity assembly resulted in 260,598 and 369,030 contigs for C. compressirostris and C.tshokwe cross-tissue transcriptomes respectively (Table 1); 357,832 and 399,878 contigs were obtained for the SM and EO cross-species assemblies respectively (Table 2). Contigs were then compared to the Danio rerio proteome, retrieving 18,458 and 19,363 unique proteins for C. compressirostris and C.tshokwe respectively; of these retrieved matches, 7971 (43.1 %) and 8993 (46.4 %) hits corresponded to full or nearly full-length coding sequences (Fig. 2a). For the cross-species assemblies, 20,023 and 20,352 contigs, for the SM and EO respectively, matched unique proteins in the D. rerio proteome, with 8662 (43.3 %) and 8768 (43.1 %) hits corresponding to full or nearly full-length coding sequences (Fig. 2b).Table 1


Cross-tissue and cross-species analysis of gene expression in skeletal muscle and electric organ of African weakly-electric fish (Teleostei; Mormyridae).

Lamanna F, Kirschbaum F, Waurick I, Dieterich C, Tiedemann R - BMC Genomics (2015)

Distribution of length coverage between Campylomormyrus Trinity transcripts and corresponding top-blast hits (D. rerio proteome). Histogram showing the distribution of the percent in length of the sequences in the D. rerio proteome that aligns to the assembled Trinity contigs. Numbers on the x-axis indicate the upper limit of the binned interval (e.g., 100 is the upper value of the interval 100–91). a Cross-tissue comparison. b Cross-species comparison
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4558960&req=5

Fig2: Distribution of length coverage between Campylomormyrus Trinity transcripts and corresponding top-blast hits (D. rerio proteome). Histogram showing the distribution of the percent in length of the sequences in the D. rerio proteome that aligns to the assembled Trinity contigs. Numbers on the x-axis indicate the upper limit of the binned interval (e.g., 100 is the upper value of the interval 100–91). a Cross-tissue comparison. b Cross-species comparison
Mentions: Sequencing of the twelve cDNA libraries produced a total amount of 371,043,357raw read pairs, resulting in 330,595,546 quality-filtered read pairs (89.1 %); see Additional file 1 for per library sequencing statistics. Trinity assembly resulted in 260,598 and 369,030 contigs for C. compressirostris and C.tshokwe cross-tissue transcriptomes respectively (Table 1); 357,832 and 399,878 contigs were obtained for the SM and EO cross-species assemblies respectively (Table 2). Contigs were then compared to the Danio rerio proteome, retrieving 18,458 and 19,363 unique proteins for C. compressirostris and C.tshokwe respectively; of these retrieved matches, 7971 (43.1 %) and 8993 (46.4 %) hits corresponded to full or nearly full-length coding sequences (Fig. 2a). For the cross-species assemblies, 20,023 and 20,352 contigs, for the SM and EO respectively, matched unique proteins in the D. rerio proteome, with 8662 (43.3 %) and 8768 (43.1 %) hits corresponding to full or nearly full-length coding sequences (Fig. 2b).Table 1

Bottom Line: In silico cross-tissue DE-analysis allowed us to identify 271 shared differentially expressed genes between EO and SM in C. compressirostris and C.tshokwe.Many of these genes correspond to myogenic factors, ion channels and pumps, and genes involved in several metabolic pathways.Cross-species analysis has revealed that the electric organ transcriptome is more variable in terms of gene expression levels across species than the skeletal muscle transcriptome.

View Article: PubMed Central - PubMed

Affiliation: Unit of Evolutionary Biology/Systematic Zoology, Institute of Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Strasse 24-25, Potsdam, Germany. lamanna@uni-potsdam.de.

ABSTRACT

Background: African weakly-electric fishes of the family Mormyridae are able to produce and perceive weak electric signals (typically less than one volt in amplitude) owing to the presence of a specialized, muscle-derived electric organ (EO) in their tail region. Such electric signals, also known as Electric Organ Discharges (EODs), are used for objects/prey localization, for the identification of conspecifics, and in social and reproductive behaviour. This feature might have promoted the adaptive radiation of this family by acting as an effective pre-zygotic isolation mechanism. Despite the physiological and evolutionary importance of this trait, the investigation of the genetic basis of its function and modification has so far remained limited. In this study, we aim at: i) identifying constitutive differences in terms of gene expression between electric organ and skeletal muscle (SM) in two mormyrid species of the genus Campylomormyrus: C. compressirostris and C. tshokwe, and ii) exploring cross-specific patterns of gene expression within the two tissues among C. compressirostris, C. tshokwe, and the outgroup species Gnathonemus petersii.

Results: Twelve paired-end (100 bp) strand-specific RNA-seq Illumina libraries were sequenced, producing circa 330 M quality-filtered short read pairs. The obtained reads were assembled de novo into four reference transcriptomes. In silico cross-tissue DE-analysis allowed us to identify 271 shared differentially expressed genes between EO and SM in C. compressirostris and C.tshokwe. Many of these genes correspond to myogenic factors, ion channels and pumps, and genes involved in several metabolic pathways. Cross-species analysis has revealed that the electric organ transcriptome is more variable in terms of gene expression levels across species than the skeletal muscle transcriptome.

Conclusions: The data obtained indicate that: i) the loss of contractile activity and the decoupling of the excitation-contraction processes are reflected by the down-regulation of the corresponding genes in the electric organ's transcriptome; ii) the metabolic activity of the EO might be specialized towards the production and turn-over of membrane structures; iii) several ion channels are highly expressed in the EO in order to increase excitability; iv) several myogenic factors might be down-regulated by transcription repressors in the EO.

No MeSH data available.


Related in: MedlinePlus