Hedren, M. | Search bioRxiv

bioRxiv2024

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

O_LIHybridization and polyploidy are major drivers of plant diversification, often accompanied by shifts in gene expression and genome composition. Small RNAs (smRNAs) are thought to influence such genomic changes, particularly through their interactions with transposable elements (TEs). C_LIO_LIWe comparatively quantified smRNAs in established sibling allopolyploids Dactylorhiza majalis and D. traunsteineri and their diploid progenitors to assess how independent allopolyploidization events shaped smRNA landscapes. C_LIO_LIDespite independent origins, the allotetraploids exhibited substantial overlap in smRNA composition, including transgressive accumulation of smRNA near genes related to transcriptional regulation, cell division and stress response. Consistently, TE-associated 24 nt smRNAs more closely resembled the paternal and larger genome, while shorter smRNAs typically reflected the maternal and smaller genome. Nevertheless, distinct patterns were also evident: the older D. majalis showed greater accumulation of smRNAs near genes involved in transcriptional and translational regulation, while the younger D. traunsteineri displayed stronger non-additive patterns, suggesting ongoing resolution of post-polyploid meiotic and mitotic instability. C_LIO_LIOur results reveal both convergence and divergence in smRNA landscapes among independently formed allopolyploids. Our study highlights the central role of smRNAs in resolving genomic conflict, with possible implications for functional divergence and ecological innovation during polyploid evolution. C_LI Plain-language summaryWe studied two sibling marsh orchid species that arose through hybridization and genome doubling. By comparing their small RNA molecules and how these associate with genes, we found both shared and species-specific patterns. These differences reflect how the orchids genomes have changed since formation, and may explain how repeated polyploidy events contribute to genetic and ecological diversity in plants.

evolutionary biology↗

bioRxiv2021

Recurrent allopolyploidization events diversify eco-physiological traits in marsh orchids

Whole-genome duplication, in particular allopolyploidy, has shaped the evolution of angiosperms and other organisms. Structural reorganization of chromosomes and repatterning of gene expression is frequently observed in early generation allopolyploids, with potential ecological consequences. The relative contributions of environmental and intrinsic drivers to these changes are unknown. We show here that in marsh orchids (Dactylorhiza, Orchidaceae), recurrently-formed allopolyploids are characterized by distinct eco-physiologies matching their respective environments, providing us with an excellent study system to address this question. Here we integrate eco-physiological and transcriptomic comparative studies to reveal a complex suite of intertwined, pronounced differences between sibling allopolyploids. We show that Dactylorhiza majalis that is distributed in Central and Southern Europe favors meadows with mesic soils. Its sibling allopolyploid D. traunsteineri occurs in fens, characterized by soils depleted by macro- and micronutrients, mainly in previously glaciated European areas. We further uncover distinct features in their nutrient transport, leaf elemental chemistry, light-harvesting, photoprotection, and stomata activity, that appear all linked to their distinct ecologies, in particular soil chemistry differences at their native sites. Recurrent polyploidization hence enriches biodiversity through eco-physiological diversification, providing the opportunity for sibling allopolyploids to evolve as distinct evolutionary units, despite pervasive interspecific gene flow. Significance StatementWhole-genome duplication resulting in polyploidy has underpinned the evolution of flowering plants and other organisms, and is important for many crops. However, the ecological implications of polyploidy remain little understood. Here, we demonstrate that two sibling allopolyploid marsh orchid species prefer distinct habitats, and have evolved a suite of distinctive ecophysiological characters (e.g. nutrient transport, energy harvesting and photoprotection). We argue that the divergence of these characters in the nascent polyploids drove adaptation into distinct ecological niches (low nutrient fens versus meadows with mesic soils), generating ecological barriers that maintains distinct, independent lineages, even in the presence of interspecific gene flow.

evolutionary biology↗