Epigenetic variation mediated by lncRNAs accounts for adaptive genomic differentiation of the endemic blue mussel Mytiluschilensis

Abstract

Epigenetic variation affects gene expression without altering the underlying DNA sequence of genes controlling ecologically relevant phenotypes through different mechanisms, one of which is long non-coding RNAs (lncRNAs). This study identified and evaluated the gene expression of lncRNAs in the gill and mantle tissues of Mytilus chilensis individuals from two ecologically different sites: Cochamó (41°S) and Yaldad (43°S), southern Chile, both impacted by climatic-related conditions and by mussel farming given their use as seedbeds. Sequences identified as lncRNAs exhibited tissue-specific differences, mapping to 3.54 % of the gill transcriptome and 1.96 % of the mantle transcriptome, representing an average of 2.76 % of the whole transcriptome. Using a high fold change value (≥|100|), we identified 43 and 47 differentially expressed lncRNAs (DE-lncRNAs) in the gill and mantle tissue of individuals sampled from Cochamó and 21 and 17 in the gill and mantle tissue of individuals sampled from Yaldad. Location-specific DE-lncRNAs were also detected in Cochamó (65) and Yaldad (94) samples. Via analysis of the differential expression of neighboring protein-coding genes, we identified enriched GO terms related to metabolic, genetic, and environmental information processing and immune system functions, reflecting how the impact of local ecological conditions may influence the M. chilensis (epi)genome expression. These DE-lncRNAs represent complementary biomarkers to DNA sequence variation for maintaining adaptive differences and phenotypic plasticity to cope with natural and human-driven perturbations.

Keywords: Differential gene expression; Epigenetics; Genome functioning; Mytilus chilensis; lncRNAs.

Fig. 1

Map of sampling locations. Map (a) with the geographic location of the sampled natural seedbeds of Mytilus chilensis, Cochamó (north), and Yaldad (south) of Chiloé Island. Mean seawater temperature (colored background) between June 2017 and May 2018. (b) Mean seawater of salinity, age of seawater, and currents for each sampling location. The scaling of the parameters is different between locations.

Fig. 2

Differential expression of lncRNAs in Mytilus chilensis. Heatmap (a) illustrating expression variations patterns among samples grouped by tissue and location, constructed using cut-offs of fold change (FCvalue) > |4| and FDR p_value <0.05. Exploring the magnitude of expression differences in lncRNAs from analyzed samples are highlighted in the PCA and volcano plots (b and c, respectively). Red points in (c) denote Bonferroni p_value filtered outcomes. These last were selected and enumerated using (d) Venn diagram, where the numbers represent the count (exclusive and shared) of differentially expressed lncRNAs (FCvalue>4; Bonferroni p_value<0.05) for each comparison. Labels: LCo_g/m (Cochamó gills/mantle), LYa_g/m (Yaldad gills/mantle). (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

Fig. 3

Mapping significant DE lncRNAs on chromosomes of Mytilus chilensis. Figure showing the mapping of the significant detected differential expressed lncRNAs (DE-lncRNAs) on chromosome sequences for both comparisons, by tissue (a) for Cochamó gill (LCo_g) and mantle (LCo_m) samples; likewise, for (b) Yaldad gills (LYa_g) and mantle (LYa_m) samples. Mapping location comparison is shown in (c). The little vertical lines on the chromosomes represent the DE-lncRNAs loci, with their height indicating the proximity between one lncRNA locus and another.

Fig. 4

GO annotations of lncRNA-neighboring genes. Semantic visualization of GO ID term distribution, depicting functional annotations of differentially expressed neighboring protein-coding genes linked with differentially expressed lncRNAs within mantle samples from individuals in Cochamó (dark colors) and Yaldad (light colors). (a) and (b) indicate biological processes for samples from Cochamó and Yaldad, respectively, shown in blue. Cellular components are illustrated in brown for Cochamó (c) and Yaldad (d), while molecular functions are represented in green (e) for Cochamó and (f) for Yaldad. The size of each sphere represents the level of enrichment resulting from GO analysis. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

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