Adaptive sequence evolution is driven by biotic stress in a pair of orchid species (Dactylorhiza) with distinct ecological optima

Francisco Balao, Emiliano Trucchi, Thomas M. Wolfe, Bao Hai Hao, Maria Teresa Lorenzo, Juliane Baar, Laura Sedman, Carolin Kosiol, Fabian Amman, Mark W. Chase, Mikael Hedrén, Ovidiu Paun

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    Abstract

    The orchid family is the largest in the angiosperms, but little is known about the molecular basis of the significant variation they exhibit. We investigate here the transcriptomic divergence between two European terrestrial orchids, Dactylorhiza incarnata and Dactylorhiza fuchsii, and integrate these results in the context of their distinct ecologies that we also document. Clear signals of lineage-specific adaptive evolution of protein-coding sequences are identified, notably targeting elements of biotic defence, including both physical and chemical adaptations in the context of divergent pools of pathogens and herbivores. In turn, a substantial regulatory divergence between the two species appears linked to adaptation/acclimation to abiotic conditions. Several of the pathways affected by differential expression are also targeted by deviating post-transcriptional regulation via sRNAs. Finally, D. incarnata appears to suffer from insufficient sRNA control over the activity of RNA-dependent DNA polymerase, resulting in increased activity of class I transposable elements and, over time, in larger genome size than that of D. fuchsii. The extensive molecular divergence between the two species suggests significant genomic and transcriptomic shock in their hybrids and offers insights into the difficulty of coexistence at the homoploid level. Altogether, biological response to selection, accumulated during the history of these orchids, appears governed by their microenvironmental context, in which biotic and abiotic pressures act synergistically to shape transcriptome structure, expression and regulation.

    Original languageEnglish
    Pages (from-to)3649-3662
    Number of pages14
    JournalMolecular Ecology
    Volume26
    Issue number14
    Early online date27 Apr 2017
    DOIs
    Publication statusPublished - 1 Jul 2017

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    Balao, F., Trucchi, E., Wolfe, T. M., Hao, B. H., Lorenzo, M. T., Baar, J., ... Paun, O. (2017). Adaptive sequence evolution is driven by biotic stress in a pair of orchid species (Dactylorhiza) with distinct ecological optima. Molecular Ecology, 26(14), 3649-3662. https://doi.org/10.1111/mec.14123