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

Balao, Francisco; Trucchi, Emiliano; Wolfe, Thomas M.; Hao, Bao Hai; Lorenzo, Maria Teresa; Baar, Juliane; Sedman, Laura; Kosiol, Carolin; Amman, Fabian and Chase, Mark W., et al. (2017) In Molecular Ecology 26(14). p.3649-3662
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... (More)

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.

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publication status
published
subject
keywords
Abiotic stress, Defence, Ecological divergence, Positive selection, Small RNAs, Transcriptomics
in
Molecular Ecology
volume
26
issue
14
pages
3649 - 3662
publisher
Wiley-Blackwell
external identifiers
  • scopus:85018991642
  • wos:000404618000007
ISSN
0962-1083
DOI
10.1111/mec.14123
language
English
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yes
id
87f434c7-fcee-45b9-a69c-be2bb97991d9
date added to LUP
2017-06-08 08:03:45
date last changed
2018-02-18 23:29:08
@article{87f434c7-fcee-45b9-a69c-be2bb97991d9,
  abstract     = {<p>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.</p>},
  author       = {Balao, Francisco and Trucchi, Emiliano and Wolfe, Thomas M. and Hao, Bao Hai and Lorenzo, Maria Teresa and Baar, Juliane and Sedman, Laura and Kosiol, Carolin and Amman, Fabian and Chase, Mark W. and Hedrén, Mikael and Paun, Ovidiu},
  issn         = {0962-1083},
  keyword      = {Abiotic stress,Defence,Ecological divergence,Positive selection,Small RNAs,Transcriptomics},
  language     = {eng},
  number       = {14},
  pages        = {3649--3662},
  publisher    = {Wiley-Blackwell},
  series       = {Molecular Ecology},
  title        = {Adaptive sequence evolution is driven by biotic stress in a pair of orchid species (Dactylorhiza) with distinct ecological optima},
  url          = {http://dx.doi.org/10.1111/mec.14123},
  volume       = {26},
  year         = {2017},
}