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July 17th, 2025
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University of Vienna
evolutionary biology
biorxiv

Small RNAs regulation and genomic harmony: insights into allopolyploid evolution in marsh orchids (Dactylorhiza)

Eriksson, M. C.Open in Google Scholar•Thornton, M.Open in Google Scholar•Trucchi, E.Open in Google Scholar•Wolfe, T. M.Open in Google Scholar•Balao, F.Open in Google Scholar•Hedren, M.Open in Google Scholar•Paun, O.Open in Google Scholar

Hybridization and polyploidy are major drivers of plant diversification, often leading to novel ecological traits through changes in gene regulation. Among these, small RNAs (smRNAs) play a key role, particularly through their interactions with transposable elements (TEs). Using a common garden setup, we comparatively investigated how smRNAs, including those targeting TEs, contribute to post-allopolyploid genome stabilization and ecological divergence in two sibling allotetraploid marsh orchids (Dactylorhiza majalis and D. traunsteineri) and their diploid progenitors. Despite independent origins, both allopolyploids exhibited substantial overlap in smRNA targeting, including transgressive overexpression around genes linked to stress response, cell division and transcriptional regulation. TE-targeting 24 nt smRNAs followed patterns consistent with subgenome size and origin, while shorter 20-23 nt smRNAs displayed greater divergence. The older allotetraploid D. majalis exhibited enhanced smRNA-mediated fine-tuning of gene copy number regulation, while its younger sibling D. traunsteineri showed more pronounced non-additive expression patterns, suggesting ongoing resolution of post-polyploid meiotic and mitotic instability. These findings reveal a two-phase smRNA response to allopolyploidy: early genome stabilization followed by regulatory fine-tuning. Our study highlights the central role of smRNAs in resolving genomic conflict, enabling functional divergence, and driving ecological innovation during polyploid evolution.

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