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BMC Genomics
2021 Mar 23;221:204. doi: 10.1186/s12864-021-07517-1.
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Transcriptomic analysis of the trade-off between endurance and burst-performance in the frog Xenopus allofraseri.
Ducret V
,
Richards AJ
,
Videlier M
,
Scalvenzi T
,
Moore KA
,
Paszkiewicz K
,
Bonneaud C
,
Pollet N
,
Herrel A
.
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BACKGROUND: Variation in locomotor capacity among animals often reflects adaptations to different environments. Despite evidence that physical performance is heritable, the molecular basis of locomotor performance and performance trade-offs remains poorly understood. In this study we identify the genes, signaling pathways, and regulatory processes possibly responsible for the trade-off between burst performance and endurance observed in Xenopus allofraseri, using a transcriptomic approach.
RESULTS: We obtained a total of about 121 million paired-end reads from Illumina RNA sequencing and analyzed 218,541 transcripts obtained from a de novo assembly. We identified 109 transcripts with a significant differential expression between endurant and burst performant individuals (FDR ≤ 0.05 and logFC ≥2), and blast searches resulted in 103 protein-coding genes. We found major differences between endurant and burst-performant individuals in the expression of genes involved in the polymerization and ATPase activity of actin filaments, cellular trafficking, proteoglycans and extracellular proteins secreted, lipid metabolism, mitochondrial activity and regulators of signaling cascades. Remarkably, we revealed transcript isoforms of key genes with functions in metabolism, apoptosis, nuclear export and as a transcriptional corepressor, expressed in either burst-performant or endurant individuals. Lastly, we find two up-regulated transcripts in burst-performant individuals that correspond to the expression of myosin-binding protein C fast-type (mybpc2). This suggests the presence of mybpc2 homoeologs and may have been favored by selection to permit fast and powerful locomotion.
CONCLUSION: These results suggest that the differential expression of genes belonging to the pathways of calcium signaling, endoplasmic reticulum stress responses and striated muscle contraction, in addition to the use of alternative splicing and effectors of cellular activity underlie locomotor performance trade-offs. Ultimately, our transcriptomic analysis offers new perspectives for future analyses of the role of single nucleotide variants, homoeology and alternative splicing in the evolution of locomotor performance trade-offs.
09-PEXT-003 Agence Nationale de la Recherche, MR/M008924/1 Medical Research Council (UK), WT097835MF Wellcome Trust (GB), WT101650MA Wellcome Trust (GB), BB/K003240/1 Biotechnology and Biological Sciences Research Council (GB), MR/M008924/1 Medical Research Council , Wellcome Trust
Fig. 1. Principal Component Analysis (PCA) and agglomerative hierarchical clustering of the four locomotor performance traits in eight males Xenopus allofraseri (named sample A to H): distance (total distance jumped until exhaustion), time (maximum time spent moving until exhaustion), acceleration (maximal instantaneous acceleration during an escape locomotor burst), velocity (maximal instantaneous speed during an escape locomotor burst)
Fig. 2. Geographic range of some Xenopus species in Africa and maximum-likelihood phylogenetic tree of the eight studied Xenopus males captured in Cameroon in 2009 (represented by a red cross). Geographic ranges were downloaded from the IUCN 2020 red list [29] and the map was created with QGIS v.3.14 (https://www.qgis.org/). The unrooted tree shows the phylogeny built with PhyML [30] based on mitogenomes assembled de novo (Sample A to H correspond to the reconstructed mitochondrial sequence based on each individual data whereas Sample ABCDEFGH corresponds to the reconstructed mitochondrial sequence from all individual data combined) and from mitogenomes of other Xenopus species previously published (corresponding GenBank accession numbers are presented in Table S2). The phylogenetic tree was designed using Figtree v.1.4.4 (http://tree.bio.ed.ac.uk/software/figtree/). The branch lengths are proportional to the number of substitutions per site with the scale indicated under the tree. The Shimoidara-Hasegawa (SH)-like branch support test is represented by node colors (p-value >â0.95 in green, p-value >â0.80 in orange, p-value <â0.80 in red)
Fig. 3. a Heatmap representation of the regularized log-transformed counts for the de novo assembly. All transcripts (n =â109) shown had significance levels with (FDR)ââ¤â0.05. The expression values are plotted in log2 space and mean-centered, and show up- and down-regulated expression as yellow and blue, respectively. b Volcano plot of all de novo transcripts and the red data points corresponding to the significantly differentially expressed transcripts. Gene symbol of the top 10 most differentially expressed transcripts in endurant and in burst-performant groups are plotted
Fig. 4. Gene interaction networks that contain 46/109 differentially expressed transcripts between endurant and burst-performant individuals. Differentially expressed transcripts were analyzed using STRING [31] using gene symbols of human orthologous genes for analysis (see the supplementary table to find corresponding X. allofraseri annotated transcripts), and visual inspection was finalized using Cytoscape [32]. The node color is based on the log2FC of expression data, with negative (blue) and positive (yellow) values representing up-regulated transcript expression in endurant and burst-performant individuals, respectively (grey color correspond to gene with transcript isoforms expressed in both groups). Node size represents the number of interactions with other protein-coding genes and allows to rapidly visualize central genes
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