Monsen Øystein, Grønvold Lars, Datsomor Alex, Harvey Thomas, Kijas James, Suh Alexander, Hvidsten Torgeir R, Sandve Simen Rød
Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, 1432 Ås, Norway.
Aquaculture Programme, Commonwealth Scientific and Industrial Research Organisation, St. Lucia, Queensland 4067, Australia.
Genome Res. 2025 Mar 18;35(3):475-488. doi: 10.1101/gr.278931.124.
Whole-genome duplications (WGDs) and transposable element (TE) activity can act synergistically in genome evolution. WGDs can increase TE activity directly through cellular stress or indirectly by relaxing selection against TE insertions in functionally redundant, duplicated regions. Because TEs can function as, or evolve into, TE-derived -regulatory elements (TE-CREs), bursts of TE activity following WGD are therefore likely to impact evolution of gene regulation. Yet, the role of TEs in genome regulatory evolution after WGDs is not well understood. Here we used Atlantic salmon as a model system to explore how TE activity after the salmonid WGD ∼100 MYA shaped CRE evolution. We identified 55,080 putative TE-CREs using chromatin accessibility data from the liver and brain. Retroelements were both the dominant source of TE-CREs and had higher regulatory activity in MPRA experiments compared with DNA elements. A minority of TE subfamilies (16%) accounted for 46% of TE-CREs, but these "CRE superspreaders" were mostly active prior to the WGD. Analysis of individual TE insertions, however, revealed enrichment of TE-CREs originating from WGD-associated TE activity, particularly for the DTT (Tc1-Mariner) DNA elements. Furthermore, coexpression analyses supported the presence of TE-driven gene regulatory network evolution, including DTT elements active at the time of WGD. In conclusion, our study supports a scenario in which TE activity has been important in genome regulatory evolution, either through relaxed selective constraints or through strong selection to recalibrate optimal gene expression phenotypes, during a transient period following genome doubling.
全基因组复制（WGDs）和转座元件（TE）活性在基因组进化中可协同作用。WGDs可通过细胞应激直接增加TE活性，或通过放松对功能冗余的复制区域中TE插入的选择间接增加TE活性。由于TE可作为TE衍生的调控元件（TE-CREs）发挥作用或进化为TE-CREs，因此WGD后TE活性的爆发可能会影响基因调控的进化。然而，TE在WGD后基因组调控进化中的作用尚未得到充分理解。在这里，我们以大西洋鲑为模型系统，探讨了约1亿年前鲑科鱼类WGD后TE活性如何塑造CRE进化。我们利用肝脏和大脑的染色质可及性数据鉴定出55080个推定的TE-CREs。逆转录元件既是TE-CREs的主要来源，并且与DNA元件相比，在MPRA实验中具有更高的调控活性。少数TE亚家族（16%）占TE-CREs的46%，但这些“CRE超级传播者”大多在WGD之前就活跃。然而，对单个TE插入的分析揭示了源自与WGD相关的TE活性的TE-CREs的富集，特别是对于DTT（Tc1-Mariner）DNA元件。此外，共表达分析支持了TE驱动的基因调控网络进化的存在，包括在WGD时活跃的DTT元件。总之，我们的研究支持这样一种情况，即在基因组加倍后的短暂时期内，TE活性通过放松选择限制或通过强烈选择来重新校准最佳基因表达表型，在基因组调控进化中发挥了重要作用。
