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

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.

Speciation across the Earth driven by global cooling in terrestrial Orchids

“…Major changes in genome size and GC content are associated with orchidoid diversification (51, 52). Recent work has highlighted a role for stress in generating diverse orchidoid lineages with distinct ecological optima (53). The orchidoids also show evidence of recent allotetraploidy (54), suggesting that new species formed during global cooling as a consequence of alterations in meiosis.…”

A Phylogenomic Analysis of the Floral Transcriptomes of Sexually Deceptive and Rewarding European Orchids, Ophrys and Gymnadenia

“…OrthoMCL v2.0.9 (Li et al, 2003) was used under the MySQL v14.14 server to identify orthologous groups based on annotated coding sequences (CDS) (where no annotated CDS were available, they were derived by TransDecoder as above) of 15 members of the Orchidaceae family including the above described Ophrys and the four Gymnadenia single-species transcriptome assemblies together with the transcriptomes/genomes of Apostasia shenzhenica and Phalaenopsis equesteris (Zhang et al, 2017) , Dactylorhiza fuchsii (Balao et al, 2017) , Chiloglottis trapeziformis (Wong et al, 2017) , Dendrobium catenatum (Zhang et al, 2016), and Platanthera clavellata and Goodyera pubescens (retrieved from the 1KP project; ). Following the TranslatorX pipeline (Abascal et al, 2010), sequences were aligned using Mafft v7.407 (Katoh and Standley, 2013).…”

Molecular phylogenomics of the tribe Shoreeae (Dipterocarpaceae) using whole plastid genomes

“…Turner et al , 2016; M. Y. Zhang et al , 2017; Lu et al , 2018; Tosso et al , 2018), only substitution information has been retained in the final vcf file using the -selectType SNP option in GATK following Balao et al (2017). Finally, the FastaAlternateReferenceMaker tool in GATK was used to replace the SNP information in the reference, resulting in a fasta file for a synthetic sequence of the plastid genome of each accession.…”