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Molecular architecture of adaptive diffusion in sibling allopolyploid lineages (Dactylorhiza, Orchidaceae)

Final Report Summary - TRANSADAPTATION (Molecular architecture of adaptive diffusion in sibling allopolyploid lineages (Dactylorhiza, Orchidaceae))

Hybridization and whole genome doubling (WGD, or polyploidization) have been central to the evolution of flowering plants, starting with their origin. Immediately following a WGD and/or a hybridization event, a genome suffers adjustments in organization and function at the genetic and epigenetic level, thereby shaping the adaptive success and the evolutionary fate of resulting lineages. Recurrent origins of polyploids are frequent phenomena but the full evolutionary significance of the highly iterative polyploid evolution in plants is not yet known. It is intriguing for example that polyploid derivatives of the same progenitor pair can exhibit contrasting morphological, ecological and range properties. Using ecologically-divergent, sibling European orchid allopolyploids of different ages and taking advantage of state-of-the-art genomic methods, the TransAdaptation project (http://www.botanik.univie.ac.at/systematik/projects/dactylorhiza/research_6.html) investigates gene expression alterations triggered by recurrent WGD with the aim to better understand their importance on the ecological properties of polyploids.
We have focused on a samples originating from 25 different populations across five countries and five species (the polyploids Dactylorhiza majalis, D. traunsteineri and D. ebudensis and their diploid parents: D. fuchsii and D. incarnata). We have performed a large-scale experiment to investigate gene expression in multiple individuals, after they have been grown in uniform conditions for at least one season, in order to eliminate local and momentary effects on expression patterns.
As preparatory steps of our research, the genetic constitution of each individual has been confirmed by sequencing various parts of their genome. By doing so, we could also apply population genetics specific inferences to demonstrate a frequent gene flow between the different polyploidy species especially in the Alps, where geographic barriers between them are absent or weak. The presence of frequent gene flow between the allopolyploids points toward a very strong natural selection required in order to maintain their ecological and morphological differences.
For the gene expression analyses we have first assembled and annotated a reference based on representatives of the diploid parents, by using state-of-the-art bioinformatics methods. Within our high-throughput experiment we have read in total close to 1,000 billion nucleotides, across the 27 individuals analyzed. Looking at differentially expressed genes between pairs of species we observe a trend of increased overexpression of genes in the younger D. traunsteineri in comparison to D. majalis, whose transcriptome generally resembles more closely those of the diploid parents. Our results point to a bidirectional dominance of patterns inherited from either parents in the polyploids as the main mechanism of differential expression, with only few hundred transcripts exhibiting novel expression patterns. Significantly overexpressed genes in D. traunsteineri as compared to D. majalis include some of ecological relevance.
Overall, there is strong evidence that recurrent allopolyploidizations modify transcript architecture in sibling allopolyploid lineages in different ways, progressing according to the evolutionary age of the polyploids. The massive expression differences among diploid parents became reconciled in siblings polyploids in different ways, thereby producing a panoply of different ecological and morphological properties which set the stage for species-specific patterns to form rapidly, most probably in response to selection and/or drift. Our results from TransAdaptation come to improve our understanding of the mechanisms underlying natural variation and adaptive strategies.