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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.

SUBMITTER: Balao F

PROVIDER: S-EPMC5518283 | biostudies-literature | 2017 Jul

REPOSITORIES: biostudies-literature

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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 F Trucchi Emiliano E Wolfe Thomas M TM Hao Bao-Hai BH Lorenzo Maria Teresa MT Baar Juliane J Sedman Laura L Kosiol Carolin C Amman Fabian F Chase Mark W MW Hedrén Mikael M Paun Ovidiu O

Molecular ecology 20170427 14

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 ...[more]

PMID: 28370647

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Project description:Orchidaceae is the 3rd largest family of angiosperms, an evolved young branch of monocotyledons. This family contains a number of economically-important horticulture and flowering plants. However, the limited availability of genomic information largely hindered the study of molecular evolution and phylogeny of Orchidaceae. In this study, we determined the evolutionary characteristics of whole chloroplast (cp) genomes and the phylogenetic relationships of the family Orchidaceae. We firstly characterized the cp genomes of four orchid species: Cremastra appendiculata, Calanthe davidii, Epipactis mairei, and Platanthera japonica. The size of the chloroplast genome ranged from 153,629 bp (C. davidi) to 160,427 bp (E. mairei). The gene order, GC content, and gene compositions are similar to those of other previously-reported angiosperms. We identified that the genes of ndhC, ndhI, and ndhK were lost in C. appendiculata, in that the ndh I gene was lost in P. japonica and E. mairei. In addition, the four types of repeats (forward, palindromic, reverse, and complement repeats) were examined in orchid species. E. mairei had the highest number of repeats (81), while C. davidii had the lowest number (57). The total number of Simple Sequence Repeats is at least 50 in C. davidii, and, at most, 78 in P. japonica. Interestingly, we identified 16 genes with positive selection sites (the psbH, petD, petL, rpl22, rpl32, rpoC1, rpoC2, rps12, rps15, rps16, accD, ccsA, rbcL, ycf1, ycf2, and ycf4 genes), which might play an important role in the orchid species' adaptation to diverse environments. Additionally, 11 mutational hotspot regions were determined, including five non-coding regions (ndhB intron, ccsA-ndhD, rpl33-rps18, ndhE-ndhG, and ndhF-rpl32) and six coding regions (rps16, ndhC, rpl32, ndhI, ndhK, and ndhF). The phylogenetic analysis based on whole cp genomes showed that C. appendiculata was closely related to C. striata var. vreelandii, while C. davidii and C. triplicate formed a small monophyletic evolutionary clade with a high bootstrap support. In addition, five subfamilies of Orchidaceae, Apostasioideae, Cypripedioideae, Epidendroideae, Orchidoideae, and Vanilloideae, formed a nested evolutionary relationship in the phylogenetic tree. These results provide important insights into the adaptive evolution and phylogeny of Orchidaceae.

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Project description:Deciphering the genomic variation that represents microevolutionary processes toward species divergence is key to understanding microbial speciation, which has long been under debate. Streptomycetes are filamentous bacteria that are ubiquitous in nature and the richest source of antibiotics; however, their speciation processes remain unknown. To tackle this issue, we performed a comprehensive population genomics analysis on Streptomyces albidoflavus residing in different habitats and with a worldwide distribution and identified and characterized the foundational changes within the species. We detected three well-defined phylogenomic clades, of which clades I and III mainly contained free-living (soil/marine) and insect-associated strains, respectively, and clade II had a mixed origin. By performing genome-wide association studies (GWAS), we identified a number of genetic variants associated with free-living or entomic (denoting or relating to insects) habitats in both the accessory and core genomes. These variants contributed collectively to the population structure and had annotated or confirmed functions that likely facilitate differential adaptation of the species. In addition, we detected higher levels of homologous recombination within each clade and in the free-living group than within the whole species and in the entomic group. A subset of the insect-associated strains (clade III) showed a relatively independent evolutionary trajectory with more symbiosis-favorable genes but little genetic interchange with the other lineages. Our results demonstrate that ecological adaptation promotes genetic differentiation in S. albidoflavus, suggesting a model of ecological speciation with gene flow in streptomycetes.IMPORTANCE Species are the fundamental units of ecology and evolution, and speciation leads to the astounding diversity of life on Earth. Studying speciation is thus of great significance to understand, protect, and exploit biodiversity, but it is a challenge in the microbial world. In this study, using population genomics, we placed Streptomyces albidoflavus strains in a spectrum of speciation and showed that the genetic differences between phylogenomic clusters evolved mainly by environmental selection and gene-specific sweeps. These findings highlight the role of ecology in structuring recombining bacterial species, making a step toward a deeper understanding of microbial speciation. Our results also raise concerns of an underrated microbial diversity at the intraspecies level, which can be utilized for mining of ecologically relevant natural products.

Dataset Information

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

Publications

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

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