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Lexer, C.

Publications and source records attributed to Lexer, C..

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Closely related facultative and constitutive CAM phenotypes show little transcriptomic overlap in the subgenus Tillandsia

Crassulacean acid metabolism (CAM) is a water-efficient photosynthetic strategy involving a coordinated suite of complex traits including metabolic, anatomical and regulatory aspects that shift across the diel cycle. While CAM has evolved repeatedly in land plants, the evolutionary routes enabling this convergence remain elusive. Whereas the same core CAM (de)carboxylation genes are consistently involved, a key question is whether distinct CAM phenotypes also depend on a shared set of auxiliary genes, reflecting a quantitative continuum of expression, or whether they can instead emerge through divergent or redundant peripheral solutions. The bromeliad subgenus Tillandsia, with diverse photosynthetic strategies, offers an ideal system to explore this question. Using physiological and transcriptomic analyses of well-watered and water-limited accessions of two closely related species, we characterized facultative and constitutive CAM. By comparing orthologous gene expression and orthogroup recruitment, we found that while both species performed CAM upon water-withholding, transcriptional shifts in pathways related to stomatal movement, sugar/malate transport, aquaporins and starch metabolism showed minimal overlap. Core enzymes involved in the CAM (de)carboxylation cycle exhibited broadly shared expression patterns, yet the facultative CAM species uniquely up-regulated PPC2 at night instead of the canonical CAM-related PEPC ortholog PPC1. Our study reveals that, while the expression of certain core CAM enzymes is conserved, the surrounding transcriptional architecture can differ substantially even between closely related species. This supports a model in which CAM evolves through a mosaic recruitment of functionally equivalent, yet non-orthologous genes - underscoring its flexible and modular genetic architecture. These insights advance our understanding of the mechanisms enabling the repeated evolution of CAM and its capacity to facilitate adaptive diversification.

evolutionary biology↗

The explosive radiation of the Neotropical Tillandsia subgenus Tillandsia (Bromeliaceae) has been facilitated by pervasive hybridization

The recent rapid radiation of Tillandsia subgenus Tillandsia (Bromeliaceae) provides an attractive system to study the drivers and constraints of species diversification. This species-rich Neotropical monocot clade includes predominantly epiphytic species displaying vast phenotypic diversity. Recent in-depth phylogenomic work revealed that the subgenus originated within the last 7 MY, with one major expansion from South into Central America within the last 5 MY. However, disagreements between phylogenies and lack of resolution at shallow nodes suggest that hybridization may have occurred throughout the radiation, together with frequent incomplete lineage sorting and rapid gene family evolution. We used whole-genome resequencing data to explore the evolutionary history of representative ingroup species employing both tree-based and network approaches. Our results indicate that lineage co-occurrence does not predict relatedness and confirm significant deviations from a tree-like structure, coupled with pervasive gene tree discordance. Focusing on hybridization, ABBA-BABA and related statistics were used to infer the rates and relative timing of events, while topology weighting uncovered high heterogeneity of the phylogenetic signal along the genome. High rates of hybridization within and among subclades suggest that, contrary to previous hypotheses, the expansion of subgenus Tillandsia into Central America proceeded through several dispersal events, punctuated by episodes of diversification and gene flow. Network analysis revealed reticulation as a plausible propeller during radiation and establishment across different ecological niches. This work contributes a plant example of prevalent hybridization during rapid species diversification, supporting the hypothesis that interspecific gene flow facilitates explosive diversification.

evolutionary biology↗

Short structural variation fuelled CAM evolution within an explosive bromeliad radiation

1.The subgenus Tillandsia (Bromeliaceae) belongs to one of the fastest radiating clades in the plant kingdom and is characterised by the repeated evolution of Crassulacean Acid Metabolism (CAM). Despite its complex genetic basis, this water-conserving trait has evolved independently across many plant families and is regarded as a key innovation trait and driver of ecological diversification in Bromeliaceae. By producing high-quality genome assemblies of a Tillandsia species pair displaying divergent photosynthetic phenotypes, and combining genome-wide investigations of synteny, TE dynamics, sequence evolution, gene family evolution and temporal differential expression, we were able to pinpoint the genomic drivers of CAM evolution in Tillandsia. Several large-scale rearrangements associated with karyotype changes between the two genomes and a highly dynamic TE landscape shaped the genomes of Tillandsia. However, our analyses show that rewiring of photosynthetic metabolism is mainly obtained through regulatory evolution rather than coding sequence evolution, as CAM-related genes are differentially expressed across a 24-hour cycle between the two species, but are no candidates of positive selection. Gene orthology analyses reveal that CAM-related gene families manifesting differential expression underwent accelerated gene family expansion in the constitutive CAM species, further supporting the view of gene family evolution as a driver of CAM evolution.

evolutionary biology↗

Conserved genomic landscapes of differentiation across Populus speciation continuum

Speciation, the continuous process by which new species form, is often investigated by looking at the variation of nucleotide diversity and differentiation across the genome (hereafter genomic landscapes). A key challenge lies in how to determine the main evolutionary forces at play shaping these patterns. One promising strategy, albeit little used to date, is to comparatively investigate these genomic landscapes as a progression through time by using a series of species pairs along a divergence gradient. Here, we resequenced 201 whole-genomes from eight closely related Populus species, with pairs of species at different stages along the divergence gradient to learn more about speciation processes. Using population structure and ancestry analyses, we document extensive introgression between some species pairs, especially those with parapatric distributions. We further investigate genomic landscapes, focusing on within-species (nucleotide diversity and recombination rate) and among-species (relative and absolute divergence) summary statistics of diversity and divergence. We observe highly conserved patterns of genomic divergence across species pairs. Independent of the stage across the divergence gradient, we find support for signatures of linked selection (i.e., the interaction between natural selection and genetic linkage) in shaping these genomic landscapes, along with gene flow and standing genetic variation. We highlight the importance of investigating genomic patterns on multiple species across a divergence gradient and discuss prospects to better understand the evolutionary forces shaping the genomic landscapes of diversity and differentiation.

evolutionary biology↗

Taxon-specific or universal? Using target capture to study the evolutionary history of a rapid radiation

Target capture has emerged as an important tool for phylogenetics and population genetics in non-model taxa. Whereas developing taxon-specific capture probes requires sustained efforts, available universal kits may have a lower power to reconstruct relationships at shallow phylogenetic scales and within rapidly radiating clades. We present here a newly-developed target capture set for Bromeliaceae, a large and ecologically-diverse plant family with highly variable diversification rates. The set targets 1,776 coding regions, including genes putatively involved in key innovations, with the aim to empower testing of a wide range of evolutionary hypotheses. We compare the relative power of this taxon-specific set, Bromeliad1776, to the universal Angiosperms353 kit. The taxon-specific set results in higher enrichment success across the entire family, however, the overall performance of both kits to reconstruct phylogenetic trees is relatively comparable, highlighting the vast potential of universal kits for resolving evolutionary relationships. For more detailed phylogenetic or population genetic analyses, e.g. the exploration of gene tree concordance, nucleotide diversity or population structure, the taxon-specific capture set presents clear benefits. We discuss the potential lessons that this comparative study provides for future phylogenetic and population genetic investigations, in particular for the study of evolutionary radiations.

evolutionary biology↗

Spatial and ecological drivers of population structure in Alkanna tinctoria (Boraginaceae), a polyploid medicinal herb

Background and AimsQuantifying genetic variation is fundamental to understand a species demographic trajectory and its ability to adapt to future changes. In comparison to diploids, however, genetic variation and factors fostering genetic divergence remains poorly studied in polyploids due to analytical challenges. Here, by employing a ploidy-aware framework, we investigated the genetic structure and its determinants in polyploid Alkanna tinctoria (Boraginaceae), an ancient medicinal herb that is the source of bioactive compounds known as alkannin and shikonin (A/S). From a practical perspective, such investigation can inform biodiversity management strategies. MethodsWe collected 14 populations of A. tinctoria within its main distribution range in Greece and genotyped them using restriction site-associated DNA sequencing (RAD-seq). As an outgroup, we included two populations of A. sieberi. By using a ploidy-aware genotype calling based on likelihoods, we generated a dataset of 16,107 high quality SNPs. Classical and model-based analysis was done to characterize the genetic structure within and between the sampled populations. Finally, to reveal the drivers of genetic structure, we searched for associations between allele frequencies and spatial and climatic variables. Key ResultsWe found support for a marked regional structure in A. tinctoria along a latitudinal gradient in line with phytogeographic divisions. Several analyses identified interspecific admixture affecting both mainland and island populations. Modelling of spatial and climatic variables further demonstrated a larger contribution of neutral processes and a lesser albeit significant role of selection in shaping the observed genetic structure in A. tinctoria. ConclusionsCurrent findings provide evidence of strong genetic structure in A. tinctoria mainly driven by neutral processes. The revealed natural genomic variation in Greek Alkanna can be used to further predict variation in A/S production, whereas our bioinformatics approach should prove useful for the study of other non-model polyploid species.

genomics↗

Adaptive introgression and standing genetic variation, two facilitators of adaptation to high latitudes in European aspen (Populus tremula L.)

Understanding local adaptation in plants from a genomic perspective has become a key research area given the ongoing climate challenge and the concomitant requirement to conserve genetic resources. Perennial plants, such as forest trees, are good models to study local adaptation given their wide geographic distribution, largely outcrossing mating systems and demographic histories. We evaluated signatures of local adaptation in European aspen (Populus tremula) across Europe by means of whole genome re-sequencing of a collection of 411 individual trees. We dissected admixture patterns between aspen lineages and observed a strong genomic mosaicism in Scandinavian trees, evidencing different colonization trajectories into the peninsula from Russia, Central and Western Europe. As a consequence of the secondary contacts between populations after the last glacial maximum (LGM), we detected an adaptive introgression event in a genome region of [~]500kb in chromosome 10, harboring a large-effect locus that has previously been shown to contribute to adaptation to the short growing seasons characteristic of northern Scandinavia. Demographic simulations and ancestry inference suggest an Eastern origin - probably Russian - of the adaptive Nordic allele which nowadays is present in a homozygous state at the north of Scandinavia. The strength of introgression and positive selection signatures in this region is a unique feature in the genome. Furthermore, we detected signals of balancing selection, shared across regional populations, that highlight the importance of standing variation as a primary source of alleles that facilitate local adaptation. Our results therefore emphasize the importance of migration-selection balance underlying the genetic architecture of key adaptive quantitative traits.

evolutionary biology↗

Estimating and accounting for genotyping errors in RAD-seq experiments

In non-model organisms, evolutionary questions are frequently addressed using reduced representation sequencing techniques due to their low cost, ease of use, and because they do not require genomic resources such as a reference genome. However, evidence is accumulating that such techniques may be affected by specific biases, questioning the accuracy of obtained genotypes, and as a consequence, their usefulness in evolutionary studies. Here we introduce three strategies to estimate genotyping error rates from such data: through the comparison to high quality genotypes obtained with a different technique, from individual replicates, or from a population sample when assuming Hardy-Weinberg equilibrium. Applying these strategies to data obtained with Restriction site Associated DNA sequencing (RAD-seq), arguably the most popular reduced representation sequencing technique, revealed per-allele genotyping error rates that were much higher than sequencing error rates, particularly at heterozygous sites that were wrongly inferred as homozygous. As we exemplify through the inference of genome-wide and local ancestry of well characterized hybrids of two Eurasian poplar (Populus) species, such high error rates may lead to wrong biological conclusions. By properly accounting for these error rates in downstream analyses, either by incorporating genotyping errors directly or by recalibrating genotype likelihoods, we were nevertheless able to use the RAD-seq data to support biologically meaningful and robust inferences of ancestry among Populus hybrids. Based on these findings, we strongly recommend carefully assessing genotyping error rates in reduced representation sequencing experiments, and to properly account for these in downstream analyses, for instance using the tools presented here.

evolutionary biology↗

Admixture mapping in interspecific Populus hybrids identifies classes of genomic architectures for phytochemical, morphological and growth traits

The genomic architecture of functionally important traits is key to understanding the maintenance of reproductive barriers and trait differences when divergent populations or species hybridize. We conducted a Genome-Wide Association Study (GWAS) to study trait architecture in natural hybrids of two ecologically divergent Populus species. We genotyped 472 seedlings from a natural hybrid zone of Populus alba and P. tremula for genome-wide markers from reduced representation sequencing, phenotyped the plants in common gardens for 46 phytochemical (phenylpropanoid), morphological, and growth traits, and used a Bayesian polygenic model for mapping. We detected three classes of genomic architectures: (1) traits with finite, detectable associations of genetic loci with phenotypic variation in addition to highly polygenic heritability, (2) traits with indications for polygenic heritability only, (3) traits with no detectable heritability. For class (1), we identified genome regions with plausible candidate genes for phenylpropanoid biosynthesis or its regulation, including MYB transcription factors and glycosyl transferases. GWAS in natural, recombinant hybrids represents a promising step towards resolving the genomic architecture of phenotypic traits in long-lived species. This facilitates the fine-mapping and subsequent functional characterization of genes and networks causing differences in hybrid performance and fitness.

evolutionary biology↗

Genomic footprints of repeated evolution of CAM photosynthesis in tillandsioid bromeliads

The adaptive radiation of Bromeliaceae (pineapple family) is one of the most diverse among Neotropical flowering plants. Diversification in this group was facilitated by several key innovations including the transition from C3 to CAM photosynthesis. We used a phylogenomic approach complemented by differential gene expression (RNA-seq) and targeted metabolite profiling to address the patterns and mechanisms of C3/CAM evolution in the extremely species-rich bromeliad genus Tillandsia and related taxa. Evolutionary analyses at a range of different levels (selection on protein-coding genes, gene duplication and loss, regulatory evolution) revealed three common themes driving the evolution of CAM: response to heat and drought, alterations to basic carbohydrate metabolism, and regulation of organic acid storage. At the level of genes and their products, CAM/C3 shifts were accompanied by gene expansion of a circadian regulator, re-programming of ABA-related gene expression, and adaptive sequence evolution of an enolase, effectively linking carbohydrate metabolism to ABA-mediated stress response. These changes include several pleiotropic regulators, which facilitated the evolution of correlated adaptive traits during a textbook adaptive radiation.

genomics↗