Biology subjects

Bossdorf, O.

Publications and source records attributed to Bossdorf, O..

At least 19 recordsLinked to original sources

bioRxiv2026

Long-term stomatal and leaf trait dynamics in invasive knotweeds in Europe - insights from 160 years of herbarium records

O_LIStomata and leaf traits are key regulators of plant water use efficiency and are expected to have changed in response to rising atmospheric CO2 concentrations and climate warming over the past centuries. However, long-term data documenting such changes are rare. C_LIO_LIWe leveraged herbarium collections to track changes in stomatal characteristics and leaf traits in 656 individuals of invasive Japanese knotweed and its hybrid Bohemian knotweed collected across their European range and spanning 160 years of invasive spread. C_LIO_LIWe found that several functional traits including stomatal density and maximum anatomical stomatal conductance did not show significant changes over time but that plants adjusted their stomatal size and shape over time, and that these changes were associated with increased atmospheric CO2 levels. Interestingly, Reynoutria japonica showed increases in stomatal size and stomatal elongation, while the hybrid R. x bohemica showed a reduction in stomatal size. Traits also varied systematically with climates of origin. Plants from warmer origins with higher evaporative demands during the growing season had thicker leaves, lower SLA, smaller stomata and higher stomatal density, indicating more conservative water-use strategies. Stomatal density and gas exchange capacity co-varied with leaf structural traits, and there was a trade-off between stomatal size and number. Overall, "fast" leaf economic traits were associated with "slow" physiological traits. C_LIO_LIOur results suggest that stomatal anatomical plasticity may enhance climate resilience by maintaining a stable maximum gas exchange capacity across environmental gradients. Herbarium collections provide a unique resource for reconstructing plant responses to historical environmental changes and understanding intraspecific trait variation. C_LI

ecology↗

bioRxiv2026

Using herbarium genomics to understand the history of a global plant invasion

Invasive plants are dynamic eco-evolutionary systems characterized by rapid spread and evolutionary change. Herbarium genomics offers a powerful way to study these processes across broad spatial and temporal scales. We generated low-coverage shotgun-sequencing data from 152 herbarium specimens of the invasive Japanese knotweed species complex (Reynoutria), collected across its native range in Japan and China, and its introduced ranges in Europe and North America, spanning 200 years of global spread. Introduced populations of R. japonica, R. japonica var. compacta and R. sachalinensis showed reduced genetic diversity compared to native populations and were genetically most similar to Japanese specimens, indicating Japan as the source of all three introductions. European and North American R. japonica were genetically highly similar and closely related to local R. x bohemica hybrids, suggesting that these hybrids originated post-introduction, through hybridization and subsequent introgression from the R. japonica parent. A few R. x bohemica hybrids in the UK and France shared a multilocus lineage with R. sachalinensis, indicating an independent but ecologically less successful hybridization event involving introgression from R. sachalinensis. A genetically distinct R. x bohemica from Japan was closely related to a Japanese R. sachalinensis specimen, suggesting that hybridization also occurs in the native range. Introduced R. japonica has remained genetically uniform for [~]200 years reflecting long-term founder effects. The dominance of a single R. japonica lineage supports the general-purpose genotype hypothesis and the importance of vegetative reproduction in its spread. Herbarium genomics thus uncovers the origin and global spread of Japanese knotweed, providing direct molecular evidence of long-term plant invasions.

evolutionary biology↗

bioRxiv2026

Failure to invest below-ground may limit the Northern expansion of invasive knotweed: lessons from a two-phase transplant experiment

The ecological and evolutionary processes determining species range limits remain poorly understood. Ultimately, range limits depend on the species abilities to persist under heterogeneous conditions, by adaptive differentiation and phenotypic plasticity, including transgenerational effects. To investigate ecological differentiation and transgenerational effects in the clonal invasive knotweed, Reynoutria japonica, in Europe, we conducted a two-phase transplant experiment: plants sampled along the entire latitudinal gradient were planted in three sites located at the northern range margin, mid-range and near the southern range margin, and then re-transplanted among all three sites after two years. Biomass production and allocation were generally not associated with latitude of origin and previous growth at the same site did not promote performance. We therefore find no evidence that adaptive differentiation or transgenerational effects contribute to the wide distribution of R. japonica in Europe. However, at the northern site, with a 25% shorter season, knotweed plants invested much less biomass below-ground, and the pattern was further strengthened in plants that had grown in the northern site in the previous generation. Overwintering below-ground rhizomes are essential for survival and spread. We further explored limiting climate conditions in a species distribution model for the European range and found that mean annual temperature and temperature annual range are the main predictors of the European distribution of R. japonica. Taken together, our study suggests that low temperatures and associated short seasons may pose a limit to the broad environmental tolerance of R. japonica and restrict its northward spread by reducing below-ground biomass accumulation.

ecology↗

bioRxiv2025

Phenotypic plasticity of invasive knotweed across Europe: a distributed common garden experiment

O_LIBiological invasions expose populations of introduced species to strong selection forces in abiotic and biotic factors, which is expected to lead to adaptive differentiation of populations, particularly for large-scale invaders. C_LIO_LITo better understand population differentiation and phenotypic plasticity of invasive Japanese knotweed (Reynoutria japonica) in Europe, we compared the performance of 45 European knotweed populations, collected across a 2000 km latitudinal transect, in three common gardens with contrasting climatic conditions, one at the southern edge, one in the center, and one at the northern edge of the species European distribution. C_LIO_LIThe plants exhibited strong phenotypic plasticity across the three gardens, with a more acquisitive growth strategy in the southern garden, and a more conservative strategy and change of architecture in the climatically unfavorable north. Although we observed phenotypic selection on several leaf traits, and on the plasticity of leaf thickness, with some selection differences between the gardens, there was little evidence of population differentiation, and none for local adaptation. Only for plant architecture (shrubbiness), we detected heritable population variation in trait means and plasticity. However, variation in plasticity was unrelated to climatic variability of origin, and to plant fitness. C_LIO_LISynthesis. Our results suggest that evolutionary processes - local adaptation and evolution of plasticity - did not play a key role in the success of Japanese knotweed in Europe. Instead, its high baseline plasticity appears to be the key factor that makes it such a strong invader across a broad range of environments. C_LI

ecology↗

bioRxiv2025

Dissolved inorganic carbon driven dynamics of calcite shell formation in 12 strains of the freshwater algae Phacotus lenticularis (Chlorophyta)

This article explores the close relationship between dissolved inorganic carbonate ion concentration (DIC) and the calcification state of Phacotus lenticularis, a globally abundant freshwater phytoplankton that is responsible for a significant part of modern lake carbonate production during bloom formation. We cultured 12 freshly isolated P. lenticularis strains under an ecologically relevant range of DIC (0.2 to 12 mmol l-1 total scale) for 14 days. From this experiment we gained information on responses in shell formation and growth that highlight strong lower boundaries in morphometric calcite shell variables with regards to DIC. All P. lenticularis strains showed reduced shell thickness by up to 60 % and dissolved calcite crystals structures at declining DIC < 4 mmol l-1. Increasing DIC > 4 mmol l-1 had no significant effect on shell thickness and crystal length in the culture experiments. We found a significant preadaptation of all 12 strains to ambient DIC concentrations measured in their lake of origin, but no dependence of growth rates up to a lethal DIC of > 10 mmol l-1. The simulation experiments illustrate the close relationship between shell function and dissolved inorganic carbonate ion concentration in lakes and highlight the need of continued research of important roles in biogenic carbon transformation and storage in a future world.

ecology↗

bioRxiv2025

Plant age and genotype explain variation in the microbiome of natural Lotus corniculatus populations

In natural populations, plants are associated with a huge diversity of bacteria, fungi and other microbes. There is usually substantial microbiome variation between different plant individuals and populations, and the drivers of this variation are still poorly understood, particularly in wild plants. Here, we were interested in the potential of plant genotype and plant age to explain intraspecific variation in the plant microbiome of Lotus corniculatus. In seven natural populations, we genotyped a total of 168 individuals over four years, determined their ages through growth ring analysis, and then sequenced their root, shoot, flower and seed microbiomes. We found that plant genotypes differed both in the diversity and composition of microbes, and that some microbial taxa were associated with particular plant genotypes. The genotype effects tended to be strongest and most consistent for plant-associated bacteria, with the largest plant genotype differences in the microbiome diversity of flowers and seeds. We found less evidence for an effect of plant age on microbiome diversity: the age of plants explained variation in fungi diversity, and it was associated with the abundance of several microbial taxa. Our study indicates that the genotype of a plant and - to a lesser degree its age - influences the diversity and composition of plant-associated microbiota, even in complex natural environments. ImportanceThe plant microbiome plays a key role in important plant functions such as pathogen resistance, nutrient uptake, and stress tolerance. To fully understand these processes, it is essential to identify the factors that drive microbiome variation. Most research to date has focused on model or crop species under controlled conditions, leaving open questions about the drivers of microbiome diversity and composition in natural populations. In this multi-year field study, we examined how plant genotype and age shape the microbiomes of Lotus corniculatus. We show that the plant genotype strongly influences microbial diversity and composition, while plant age has subtler but still important effects, particularly on fungal communities. To our knowledge, this is the first study to link plant age with microbiome variation in natural populations. These findings demonstrate that plant traits can shape the microbiome even in complex natural environments.

microbiology↗

bioRxiv2025

Organ-specific filtering by abiotic and biotic environmental factors shapes distinct yet overlapping microbial communities across Lotus corniculatus roots, shoots, flowers, and seeds

Plant microbiome assembly is modulated via filtering by the host plant and local environment as well as stochastic processes like microbial dispersal. Lotus corniculatus in natural populations that are continuously exposed to natural perturbations and microbial sources is an ideal plant model system to study the ecological processes that structure the distinct yet overlapping microbial communities in plant organs. We observed spatial and temporal variation in microbiomes associated with L. corniculatus roots, shoots, flowers, and seeds across seven grassland sites for four years. In this study we examined how abiotic and biotic factors in the local environment throughout multiple years contribute to the structure of microbiomes associated with L. corniculatus populations. We show that plant microbiomes are shaped by a set of environmental factors that are distinct to each plant compartment. These environmental factors either directly influence the plant microbiomes or by indirectly affecting them via other biotic factors. The environmental factors soil temperature seasonality, soil microbiome composition, air temperature seasonality, plant community richness, and grazing are found to influence the structure and microbial interactions in the plant organs, and are different in relationships with microbiomes with each compartment, possibly influencing dispersal decisions of microorganisms and consequently contribute in shaping distinct yet overlapping microbiomes across plant organs. Burkholderia and Sulfuritalea, plant-associated microbes that are highly correlated with environmental variables across all plant organs, respond to environmental variables differently depending on their organ microhabitat. This organ-dependent environmental perception is also observed in biomarker microbes in roots, shoots, and flowers, such as the rhizobial symbiont Mesorhizobium, leaf pathogen Setosphaeria, and necrotroph Botryotinia, respectively. Our knowledge about the organ-specific response of plant microbiomes to abiotic and biotic perturbations will equip us with a framework to understand and engineer plant microbiomes in the context of global climate change. The observed patterns on dispersal decisions or habitat choice based on organ-dependent environmental cues and microbial interactions in plant microbiomes also advance our insights on how beneficial microbes or pathogens survive and persist on specific plant microhabitat and environmental conditions.

microbiology↗

bioRxiv2025

Organ-specific microbiomes in natural Lotus corniculatus populations: Metacommunity dynamics in the plant endosphere

The structure of plant microbial communities vary due to a broad range of factors such as host and environmental factors, abiotic and biotic perturbations, and various assembly processes occurring at multiple tempo-spatial scales. In natural environments plant microbial communities are constantly exposed to such perturbations and processes. Thus, to attain a systemic understanding of the ecology of plant microbiomes, it is essential to study assembly processes that influence patterns of microbial community structures in natural environments. In this study we examined bacterial, fungal, and eukaryotic communities in plant organs of Lotus corniculatus in natural populations at seven grassland sites for four years. We used the framework of metacommunity theory of ecology to understand assembly processes that shape community structures and variations by defining microbial communities associated with the roots, shoots, flowers, and seeds as distinct communities linked by dispersal. In this study we show the organ-specificity of plant endophytic communities. Our findings suggest that selective filtering by plant organs, microbial interactions, as well as abiotic and biotic factors at tempo-spatial scales result in distinct core microbiomes of plant organs. In addition, transmission of microorganisms from within and outside the plant hosts accounts for the distinct yet overlapping organ microbiomes. We could provide a comprehensive knowledge of the stochastic and deterministic assembly processes that shape plant microbial communities in natural conditions. Understanding these ecological processes is essential for harnessing beneficial effects of plant-associated microbial communities on plant productivity, resilience, and pathogen defense.

microbiology↗

bioRxiv2024

General purpose genotypes and evolution of higher plasticity in clonality underlie knotweed invasion

Many widespread invasive plant species express high phenotypic variation across novel environments, providing a unique opportunity to examine ecological and evolutionary dynamics under global change. However, biogeographical studies often lack information about the origin of introduced populations, limiting our understanding of post-introduction evolution of introduced species in the new range. Here, we assessed the responses of Reynoutria japonica from 128 populations spanning three latitudinal transects in the native ranges of China and Japan, and the introduced ranges of North America and Europe. When grown in two common gardens in the native range, plants from introduced populations in North America and Europe differed in almost all traits from those from native Chinese populations, but were similar to plants from native Japanese populations. Compared to Chinese populations, North American, European and Japanese populations expressed lower trait values and plasticity in most traits. However, plants from both introduced ranges and from Japanese populations expressed higher clonality and plasticity in clonality than plants from Chinese populations. In addition, introduced populations expressed higher plasticity in clonality but lower plasticity in basal diameter compared to Japanese populations. Our study showed heritable differences in phenotypes between plants from the native ranges of Japan and China, and those from the introduced ranges were similar to the putative source of origin in Japan. However, we found that introduced populations may have evolved higher plasticity in clonal growth. Our findings emphasize the critical role of clonality and plasticity in invasion success, demonstrating the importance of discriminating between source and non-source native populations to identify ecological and evolutionary responses of invasive plants to novel environments.

ecology↗

bioRxiv2024

Global heterogeneity of latitudinal patterns in herbivory between native and exotic plants

Latitudinal gradient of herbivory that differs between native and exotic plants has been an open issue. It is expected that a latitudinal gradient of herbivory will be evident for native plants; this gradient in exotic plants may lag behind native plants in terms of co-evolution with local abiotic and biotic factors in introduced area. Our study aims to elucidate the difference in latitudinal gradient of herbivory between native and exotic plants globally, while exploring the underlying mechanisms driving the latitudinal gradient of herbivory with biotic and abiotic factors. To achieve this, we analyzed herbivory data from 94 studies and calculated 862 herbivory effect sizes (zr) to quantitatively characterize the intensity of latitudinal herbivory gradient. For each herbivory data, we matched the corresponding plant identity (native/exotic), herbivore feeding guilds and climate data to reveal the contribution of these factors to zr. Our findings demonstrate a significant decrease in the latitudinal gradients of with increasing latitude for native plants, a pattern not observed for exotic plants. The heterogeneity in latitudinal gradients of herbivory between native and exotic plants is mediated by herbivore feeding guilds. There is a significant influence of climatic factors on the latitudinal gradient of herbivory for native plants, but not for exotic plants. Overall, our results underscore a general heterogeneity in global macroecological herbivory patterns between native and exotic plants, and highlight the role of biotic and abiotic factors in explaining these global-scale differences.

ecology↗

bioRxiv2023

Divergence in herbivore resistance during the invasion of a global plant invader

O_LISuccessful plant invasions are often explained with adaptation to novel environments. However, invasive species often occupy broad niches within their native and introduced ranges, and a true understanding of microevolution during invasion therefore requires broad sampling of ranges, ideally with a knowledge of introduction history. C_LIO_LIWe tested for genetic differentiation in herbivore resistance among 128 introduced (Europe, North America) and native (China, Japan) populations of the invasive Japanese knotweed (Reynoutria japonica) in two common gardens in the native range. C_LIO_LIIn both common gardens we found that resistance traits of introduced populations differed from most Chinese native populations, but not from populations in Japan, the putative sources of introduction. Compared to Chinese populations, introduced European populations had thicker leaves with a lower C:N ratio but higher flavonoids contents. In the native range, variation in herbivore resistance was much more strongly associated with climate of origin than in introduced populations. C_LIO_LIOur results support the idea that founder effects played a key role in the invasion of knotweed into Europe and North America, with introduction of particular resistance phenotypes from Japan. Our study also demonstrates how knowledge of introduction history can avoid drawing wrong conclusions from observed biogeographic divergence. C_LI

ecology↗

bioRxiv2023

Discarded sequencing reads uncover natural variation in pest resistance in Thlaspi arvense

Understanding the genomic basis of natural variation in plant pest resistance is an important goal in plant science, but it usually requires large and labour-intensive phenotyping experiments. Here, we explored the possibility that non-target reads from plant DNA sequencing can serve as phenotyping proxies for addressing such questions. We used data from a whole-genome and -epigenome sequencing study of 207 natural lines of field pennycress (Thlaspi arvense) that were grown in a common environment and spontaneously colonized by aphids, mildew and other microbes. We found that the numbers of non-target reads assigned to the pest species differed between populations, had significant SNP-based heritability, and were associated with climate of origin and baseline glucosinolates content. Specifically, pennycress lines from cold and thermally fluctuating habitats, presumably less favorable to aphids, showed higher aphid DNA load, i.e. decreased aphid resistance. Genome-wide association analyses identified genetic variants at known defense genes but also novel genomic regions associated with variation in aphid and mildew DNA load. Moreover, we found several differentially methylated regions associated with pathogen loads, in particular differential methylation at transposons and hypomethylation in the promoter of a gene involved in stomatal closure, likely induced by pathogens. Our study provides first insights into the defense mechanisms of Thlaspi arvense, a rising crop and model species, and demonstrates that non-target whole genome sequencing reads, usually discarded, can be leveraged to estimate intensities of plant biotic interactions. With rapidly increasing numbers of large sequencing datasets worldwide, this approach should have broad application in fundamental and applied research.

evolutionary biology↗

bioRxiv2023

Transposon dynamics in the emerging oilseed crop Thlaspi arvense

Genome evolution is partly driven by the mobility of transposable elements (TEs) which often leads to deleterious effects, but their activity can also facilitate genetic novelty and catalyze local adaptation. We explored how the intraspecific diversity of TE polymorphisms is shaping the broad geographic success and adaptation capacity of the emerging oil crop Thlaspi arvense. We achieved this by classifying the TE inventory of this species based on a high-quality genome assembly, age estimation of retrotransposon TE families and a comprehensive assessment of their mobilization potential. Our survey of TE insertion polymorphisms (TIPs) captured 280 accessions from 12 regions across the Northern hemisphere. We quantified over 90,000 TIPs, with their distribution mirroring genetic differentiation as measured by single nucleotide polymorphisms (SNPs). The number and types of mobile TE families vary substantially across populations, but there are also shared patterns common to all accessions. We found that Ty3/Athila elements are the main drivers of TE diversity in T. arvense populations, while a single Ty1/Alesia lineage might be particularly important for molding transcriptome divergence. We further observed that the number of retrotransposon TIPs is associated with variation at genes related to epigenetic regulation while DNA transposons are associated with variation at a Heat Shock Protein (HSP19). We propose that the high rate of mobilization activity can be harnessed for targeted gene expression diversification, which may ultimately present a toolbox for the potential use of transposition in breeding and domestication of T. arvense.

genomics↗

bioRxiv2023

Recent evolution of flowering time across multiple European plant species correlates with changes in aridity

Ongoing global warming and increasing drought frequencies impact plant populations and potentially drive rapid evolutionary adaptations. Historical comparisons, where plants grown from seeds collected in the past are compared to plants grown from freshly collected seeds from populations of the same sites, are a powerful method to investigate recent evolutionary changes across many taxa. We used 21-38 year-old seeds of 13 European plant species, stored in seed banks and originating from Mediterranean and temperate regions, together with recently collected seeds from the same sites for a greenhouse experiment to investigate shifts in flowering phenology as a potential result of adaptive evolution to changes in drought intensities over the last decades. We further used single nucleotide polymorphism (SNP) markers to quantify relatedness and levels of genetic variation. We found that, across species, current populations grew faster and advanced their flowering. These shifts were correlated with changes in aridity at the population origins, suggesting that increased drought induced evolution of earlier flowering, whereas decreased drought lead to weak or inverse shifts in flowering phenology. In five out of the 13 species, however, the SNP markers detected strong differences in genetic variation and relatedness between the past and current populations collected, indicating that other evolutionary processes may have contributed to changes in phenotypes. Our results suggest that changes in aridity may have influenced the evolutionary trajectories of many plant species in different regions of Europe, and that flowering phenology may be one of the key traits that is rapidly evolving. Highlighted student paperWe demonstrated that accurately sampled and stored seed collections from conventional seed banks can, with some limitations, be used in a similar way as the increasingly popular resurrection approach sensu stricto. Given the vast availability of seeds stored in seed banks, this opens up a large potential for future research on rapid evolutionary adaptation to changing environmental conditions across a wide variety of taxa suitable for resurrection. Furthermore, this work is unique and novel, as we combine greenhouse experiments with molecular and climatic data to disentangle potential drivers for the observed phenotypic evolution, which, to our knowledge, was never done in resurrection studies.

evolutionary biology↗

bioRxiv2023

Plants cultivated for ecosystem restoration can evolve towards a domestication syndrome

The UN Decade on Ecosystem Restoration calls for upscaling restoration efforts, but many terrestrial restoration projects are constrained by seed availability. To overcome these constraints, wild plants are increasingly propagated on farms to produce seeds for restoration projects. During on-farm propagation, the plants face non-natural conditions with different selection pressures, and they might evolve adaptations to cultivation that parallel those of agricultural crops, which could be detrimental to restoration efforts. To test this, we compared traits of 19 species grown from wild-collected seeds to those from their farm-propagated offspring of up to four cultivation generations, produced by two European seed growers, in a common garden experiment. We found that some plants rapidly evolved across cultivated generations towards increased size and reproduction, lower within-species variability, and more synchronized flowering. In one species, we found evolution towards less seed shattering. These trait changes are typical signs of the crop domestication syndrome, and our study demonstrates that it can also occur during cultivation of wild plants, within only few cultivated generations. However, there was large variability between cultivation lineages, and the observed effect sizes were generally rather moderate, which suggests that the detected evolutionary changes are unlikely to compromise farm-propagated seeds for ecosystem restoration. To mitigate the potential negative effects of unintended selection, we recommend to limit the maximum number of generations the plants can be cultivated without replenishing the seed stock from new wild collections. Significance StatementGlobally upscaling demands for native seeds for ecosystem restoration can be covered by agricultural seed propagation. Yet, agricultural practice can unintentionally select for specific traits and reduce adaptive variability, which could affect plant performance once sown back to the wild. We show, across 19 wild species, two seed producers and up to four consecutive cultivated generations, that some plants under cultivation evolved higher vigor, reduced adaptive variability, synchronized flowering and in one case, reduced seed shattering. Yet, there were substantial differences among cultivation lineages, with negligible changes in most, and large changes only in a few cases. Substantial unintended evolution in cultivation is thus rather an exception than the rule.

ecology↗

bioRxiv2023

Sustainable seed harvesting in wild plant populations

Seed harvesting from wild plant populations is key for ecological restoration, but may threaten the persistence of source populations. Consequently, several countries have set guidelines limiting the proportions of harvestable seeds. However, these guidelines are so far inconsistent, and they lack a solid empirical basis. Here, we use high-resolution data from 298 plant species to model the demographic consequences of seed harvesting. We find that the current guidelines do not protect populations of annuals and short-lived perennials, while they are overly restrictive for long-lived plants. We show that the maximum possible fraction of seed production - what can be harvested without compromising the long-term persistence of populations - is strongly related to the generation time of the target species. When harvesting every year, this safe seed fraction ranges from 80% in long-lived species to 2% in most annuals. Less frequent seed harvesting substantially increases the safe seed fraction: In the most vulnerable annual species, it is safe to harvest 5%, 10% or 30% of population seed production when harvesting every two, five or ten years, respectively. Our results provide a quantitative basis for seed harvesting legislations worldwide, based on species generation time and harvesting regime. SignificanceThe UN Decade on Ecosystem Restoration, 2021-2030, foresees upscaling restoration, and the demand for native seed is skyrocketing. Seeds for restoring native vegetation are often harvested in wild, but too intensive harvest can threaten the donor populations. Existing guidelines that set limits to wild seed harvest are mostly based on expert opinions, yet they commonly lack empirical basis and vary among regions in one order of magnitude. We show that the current guidelines urgently need to be reformulated, because they are overly restrictive in long-lived species, while they do not protect annual plants from extinction. Using matrix population models of nearly 300 plant species, we provide a quantitative basis for a new seed harvesting legislation world-wide.

ecology↗

bioRxiv2022

Genetic and environmental drivers of large-scale epigenetic variation in Thlaspi arvense

Natural plant populations often harbour substantial heritable variation in DNA methylation. However, a thorough understanding of the genetic and environmental drivers of this epigenetic variation requires large-scale and high-resolution data, which currently exist only for a few model species. Here, we studied 207 lines of the annual weed Thlaspi arvense (field pennycress), collected across a large latitudinal gradient in Europe and propagated in a common environment. By screening for variation in DNA sequence and DNA methylation using whole-genome (bisulfite) sequencing, we found significant epigenetic population structure across Europe. Average levels of DNA methylation were strongly context-dependent, with highest DNA methylation in CG context, particularly in transposable elements and in intergenic regions. Residual DNA methylation variation within all contexts was associated with genetic variants, which often co-localized with annotated methylation machinery genes but also with new candidates. Variation in DNA methylation was also significantly associated with climate of origin, with methylation levels being higher in warmer regions and lower in more variable climates. Finally, we used variance decomposition to assess genetic versus environmental associations with differentially methylation regions (DMRs). We found that while genetic variation was generally the strongest predictor of DMRs, the strength of environmental associations increased from CG to CHG and CHH, with climate-of-origin as the strongest predictor in about one third of the CHH DMRs. In summary, our data show that natural epigenetic variation in Thlaspi arvense is significantly associated with both DNA sequence and environment of origin, and that the relative importance of the two factors strongly depends on the sequence context of DNA methylation. T. arvense is an emerging biofuel and winter cover crop; our results may hence be relevant for breeding efforts and agricultural practices in the context of rapidly changing environmental conditions. Author SummaryVariation within species is an important level of biodiversity, and it is key for future adaptation. Besides variation in DNA sequence, plants also harbour heritable variation in DNA methylation, and we want to understand the evolutionary significance of this epigenetic variation, in particular how much of it is under genetic control, and how much is associated with the environment. We addressed these questions in a high-resolution molecular analysis of 207 lines of the common plant field pennycress (Thlaspi arvense), which we collected across Europe, propagated under standardized conditions, and sequenced for their genetic and epigenetic variation. We found large geographic variation in DNA methylation, associated with both DNA sequence and climate of origin. Genetic variation was generally the stronger predictor of DNA methylation variation, but the strength of environmental association varied between different sequence contexts. Climate-of-origin was the strongest predictor in about one third of the differentially methylated regions in the CHH context, which suggests that epigenetic variation may play a role in the short-term climate adaptation of pennycress. As pennycress is currently being domesticated as a new biofuel and winter cover crop, our results may be relevant also for agriculture, particularly in changing environments.

evolutionary biology↗

bioRxiv2021

Evolution during seed production for ecological restoration? A molecular analysis of 19 species finds only minor genomic changes

A growing number of restoration projects require large amounts of seeds. As harvesting natural populations cannot cover the demand, wild plants are often propagated in large-scale monocultures. There are concerns that this cultivation process may cause genetic drift and unintended selection, which would alter the genetic properties of the cultivated populations and reduce their genetic diversity. Such changes could reduce the pre-existing adaptation of restored populations, and limit their adaptability to environmental change. We used single nucleotide polymorphism (SNP) markers and a pool-sequencing approach to test for genetic differentiation and changes in gene diversity during cultivation in 19 wild grassland species, comparing the source populations and up to four consecutive cultivation generations grown from these sources. We then linked the magnitudes of genetic changes to the species breeding systems and seed dormancy, to understand the roles of these traits in genetic change. The propagation of native seeds for ecosystem restoration changed the genetic composition of the cultivated generations only moderately. The genetic differentiation we observed as a consequence of cultivation was much lower than the natural genetic differentiation between different source regions, and the propagated generations harbored even higher gene diversity than wild-collected seeds. Genetic change was stronger in self-compatible species, probably as a result of increased outcrossing in the monocultures. Synthesis and applicationsOur study indicates that large-scale seed production maintains the genetic integrity of natural populations. Increased genetic diversity may even increase the adaptive potential of propagated seeds, which makes them especially suitable for ecological restoration. However, we have been working with seeds from Germany and Austria, where the seed production is regulated and certified. Whether other seed production systems perform equally well remains to be tested.

ecology↗