Most cited article - PubMed ID 33363550
Parallel Alpine Differentiation in Arabidopsis arenosa
Cuticle function can be pivotal to plant success in different environments. Yet, the occurrence of intraspecific adjustments in cuticle traits resulting from acclimation or adaptation to different habitats remains poorly understood. Here, we used genetically well-characterised populations of Arabidopsis arenosa to investigate whether cuticle traits were adjusted as part of the parallel evolution from a foothill to an alpine ecotype. Six alpine and six foothill populations, representing at least three independent evolutionary origins of an alpine ecotype, were used in reciprocal transplantation experiments, to investigate cuticle traits at the eco-physiological, biochemical and structural levels. The genetic basis behind these traits was assessed by combining selection scans and differential gene expression analysis. Overall, alpine populations showed reduced cuticular transpiration in conjunction with consistently altered cuticular wax composition, with higher accumulation of two fatty alcohols and two iso-alkanes. Genomic analysis unravelled nine genes associated with cuticular wax metabolism showing allelic differentiation in alpine compared to lowland populations. In silico gene expression analysis revealed differences between ecotypes for several genes related to cuticle metabolism. Repeated ecotypic differentiation in cuticle traits together with the genetic architecture of the alpine ecotype points at an adaptive value of cuticle adjustments for the colonisation of alpine habitats.
- Keywords
- Alpine habitat, Arabidopsis arenosa, adaptation, cuticle, cuticular wax composition, ecotype, parallel evolution,
- MeSH
- Arabidopsis * genetics physiology MeSH
- Ecosystem * MeSH
- Ecotype MeSH
- Plant Epidermis * physiology genetics MeSH
- Phenotype MeSH
- Quantitative Trait, Heritable * MeSH
- Plant Leaves * physiology genetics anatomy & histology MeSH
- Gene Expression Regulation, Plant MeSH
- Genes, Plant MeSH
- Waxes metabolism MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Waxes MeSH
The role of endemic species in global biodiversity is pivotal, and understanding their biology and ecology is imperative for their fitness and long-term survival, particularly in the face of ongoing climatic oscillations. Our primary goal was to investigate the sexual reproduction level of the endangered Western Carpathian endemic Daphne arbuscula (Thymelaeaceae), which inhabits extreme rocky habitats, and to comprehend the influence of specific factors on its reproductive success. We conducted the research across four populations, varying in size and environmental conditions. Over two years, we monitored flower and fruit production, analyzed genetic variability within and among populations, and studied pollination mechanisms. Daphne arbuscula proved to be strictly self-incompatible, with significant variations in flower and fruit production among populations and seasons. The average fruit production percentage consistently remained below 50% across populations, indicating challenges in sexual reproduction. Cold and harsh weather during the reproductive phase had a substantial negative impact on sexual reproduction efficacy, leading to decreased fruit production. Nevertheless, several individuals in sheltered microhabitats displayed significantly higher fruit production, ranging from 60% to 83%, emphasizing the critical role of microhabitat heterogeneity in sustaining sexual reproduction in this species. We found no pronounced differences in genetic diversity within or among populations, suggesting that genetic factors may not critically influence the reproductive success of this endemic species. The implications of our findings might be of paramount importance for the long-term survival of D. arbuscula and offer valuable insights for the development of effective conservation strategies for this species.
Functional and structural adjustments of plants in response to environmental factors, including those occurring in alpine habitats, can result in transient acclimation, plastic phenotypic adjustments and/or heritable adaptation. To unravel repeatedly selected traits with potential adaptive advantage, we studied parallel (ecotypic) and non-parallel (regional) differentiation in leaf traits in alpine and foothill ecotypes of Arabidopsis arenosa. Leaves of plants from eight alpine and eight foothill populations, representing three independent alpine colonization events in different mountain ranges, were investigated by microscopy techniques after reciprocal transplantation. Most traits clearly differed between the foothill and the alpine ecotype, with plastic adjustments to the local environment. In alpine populations, leaves were thicker, with altered proportions of palisade and spongy parenchyma, and had fewer trichomes, and chloroplasts contained large starch grains with less stacked grana thylakoids compared to foothill populations. Geographical origin had no impact on most traits except for trichome and stomatal density on abaxial leaf surfaces. The strong parallel, heritable ecotypic differentiation in various leaf traits and the absence of regional effects suggests that most of the observed leaf traits are adaptive. These trait shifts may reflect general trends in the adaptation of leaf anatomy associated with the colonization of alpine habitats.
- Keywords
- adaptation, alpine environment, ecotype, leaf anatomy, parallel evolution,
- Publication type
- Journal Article MeSH
Success or failure of plants to cope with freezing temperatures can critically influence plant distribution and adaptation to new habitats. Especially in alpine environments, frost is a likely major selective force driving adaptation. In Arabidopsis arenosa (L.) Lawalrée, alpine populations have evolved independently in different mountain ranges, enabling studying mechanisms of acclimation and adaptation to alpine environments. We tested for heritable, parallel differentiation in freezing resistance, cold acclimation potential and ice management strategies using eight alpine and eight foothill populations. Plants from three European mountain ranges (Niedere Tauern, Făgăraș and Tatra Mountains) were grown from seeds of tetraploid populations in four common gardens, together with diploid populations from the Tatra Mountains. Freezing resistance was assessed using controlled freezing treatments and measuring effective quantum yield of photosystem II, and ice management strategies by infrared video thermography and cryomicroscopy. The alpine ecotype had a higher cold acclimation potential than the foothill ecotype, whereby this differentiation was more pronounced in tetraploid than diploid populations. However, no ecotypic differentiation was found in one region (Făgăraș), where the ancient lineage had a different evolutionary history. Upon freezing, an ice lens within a lacuna between the palisade and spongy parenchyma tissues was formed by separation of leaf tissues, a mechanism not previously reported for herbaceous species. The dynamic adjustment of freezing resistance to temperature conditions may be particularly important in alpine environments characterized by large temperature fluctuations. Furthermore, the formation of an extracellular ice lens may be a useful strategy to avoid tissue damage during freezing.
- Keywords
- Adaptation, cold acclimation, freezing resistance, ice nucleation, parallel evolution, polyploidization,
- MeSH
- Acclimatization MeSH
- Arabidopsis * genetics MeSH
- Ecosystem MeSH
- Photosystem II Protein Complex MeSH
- Ice MeSH
- Plants MeSH
- Tetraploidy MeSH
- Freezing MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Photosystem II Protein Complex MeSH
- Ice MeSH
Parallel adaptation provides valuable insight into the predictability of evolutionary change through replicated natural experiments. A steadily increasing number of studies have demonstrated genomic parallelism, yet the magnitude of this parallelism varies depending on whether populations, species, or genera are compared. This led us to hypothesize that the magnitude of genomic parallelism scales with genetic divergence between lineages, but whether this is the case and the underlying evolutionary processes remain unknown. Here, we resequenced seven parallel lineages of two Arabidopsis species, which repeatedly adapted to challenging alpine environments. By combining genome-wide divergence scans with model-based approaches, we detected a suite of 151 genes that show parallel signatures of positive selection associated with alpine colonization, involved in response to cold, high radiation, short season, herbivores, and pathogens. We complemented these parallel candidates with published gene lists from five additional alpine Brassicaceae and tested our hypothesis on a broad scale spanning ∼0.02 to 18 My of divergence. Indeed, we found quantitatively variable genomic parallelism whose extent significantly decreased with increasing divergence between the compared lineages. We further modeled parallel evolution over the Arabidopsis candidate genes and showed that a decreasing probability of repeated selection on the same standing or introgressed alleles drives the observed pattern of divergence-dependent parallelism. We therefore conclude that genetic divergence between populations, species, and genera, affecting the pool of shared variants, is an important factor in the predictability of genome evolution.
- Keywords
- Arabidopsis, alpine adaptation, evolution, genomics, parallelism,
- MeSH
- Molecular Sequence Annotation MeSH
- Arabidopsis classification genetics metabolism radiation effects MeSH
- Biological Evolution * MeSH
- Herbivory physiology MeSH
- Adaptation, Physiological genetics MeSH
- Stress, Physiological MeSH
- Genetic Variation * MeSH
- Genetic Drift MeSH
- Genome, Plant * MeSH
- Genetic Introgression MeSH
- Gene Ontology MeSH
- Radiation, Ionizing MeSH
- Models, Genetic MeSH
- Cold Temperature MeSH
- Plant Proteins genetics metabolism MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Plant Proteins MeSH
BACKGROUND: Plant genomes can respond rapidly to environmental changes and transposable elements (TEs) arise as important drivers contributing to genome dynamics. Although some elements were reported to be induced by various abiotic or biotic factors, there is a lack of general understanding on how environment influences the activity and diversity of TEs. Here, we combined common garden experiment with short-read sequencing to investigate genomic abundance and expression of 2245 consensus TE sequences (containing retrotransposons and DNA transposons) in an alpine environment in Arabidopsis arenosa. To disentangle general trends from local differentiation, we leveraged four foothill-alpine population pairs from different mountain regions. Seeds of each of the eight populations were raised under four treatments that differed in temperature and irradiance, two factors varying with elevation. RNA-seq analysis was performed on leaves of young plants to test for the effect of elevation and subsequently of temperature and irradiance on expression of TE sequences. RESULTS: Genomic abundance of the 2245 consensus TE sequences varied greatly between the mountain regions in line with neutral divergence among the regions, representing distinct genetic lineages of A. arenosa. Accounting for intraspecific variation in abundance, we found consistent transcriptomic response for some TE sequences across the different pairs of foothill-alpine populations suggesting parallelism in TE expression. In particular expression of retrotransposon LTR Copia (e.g. Ivana and Ale clades) and LTR Gypsy (e.g. Athila and CRM clades) but also non-LTR LINE or DNA transposon TIR MuDR consistently varied with elevation of origin. TE sequences responding specifically to temperature and irradiance belonged to the same classes as well as additional TE clades containing potentially stress-responsive elements (e.g. LTR Copia Sire and Tar, LTR Gypsy Reina). CONCLUSIONS: Our study demonstrated that the A. arenosa genome harbours a considerable diversity of TE sequences whose abundance and expression response varies across its native range. Some TE clades may contain transcriptionally active elements responding to a natural environmental gradient. This may further contribute to genetic variation between populations and may ultimately provide new regulatory mechanisms to face environmental challenges.
- Keywords
- Alpine environment, Arabidopsis arenosa, Common garden experiment, Parallelism, RNA-seq, Transposable elements,
- Publication type
- Journal Article MeSH
Parallel evolution provides powerful natural experiments for studying repeatability of evolution and genomic basis of adaptation. Well-documented examples from plants are, however, still rare, as are inquiries of mechanisms driving convergence in some traits while divergence in others. Arabidopsis arenosa, a predominantly foothill species with scattered morphologically distinct alpine occurrences is a promising candidate. Yet, the hypothesis of parallelism remained untested. We sampled foothill and alpine populations in all regions known to harbor the alpine ecotype and used SNP genotyping to test for repeated alpine colonization. Then, we combined field surveys and a common garden experiment to quantify phenotypic parallelism. Genetic clustering by region but not elevation and coalescent simulations demonstrated parallel origin of alpine ecotype in four mountain regions. Alpine populations exhibited parallelism in height and floral traits which persisted after two generations in cultivation. In contrast, leaf traits were distinctive only in certain region(s), reflecting a mixture of plasticity and genetically determined non-parallelism. We demonstrate varying degrees and causes of parallelism and non-parallelism across populations and traits within a plant species. Parallel divergence along a sharp elevation gradient makes A. arenosa a promising candidate for studying genomic basis of adaptation.
- Keywords
- Arabidopsis, adaptation, alpine environments, convergence, parallel evolution, phenotypic parallelism,
- Publication type
- Journal Article MeSH
