Koen Verhoeven

Dr. Koen Verhoeven

Senior Researcher
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Visiting Address

Droevendaalsesteeg 10
6708 PB Wageningen

+31 (0) 317 47 34 00

The Netherlands

About

I am an ecological geneticist with a broad interest in plant adaptation. I study the genetic and epigenetic mechanisms by which plants cope with, and adapt to, a rapidly changing world.

Biography

Human activities have a massive impact on the environment. The majority of the earth's land surface has been transformed in the last few centuries, and climate change and biological invasions pose important challenges to ecosystems. Understanding the response of ecosystems to these challenges has an ecological and an evolutionary component: which species fit together in the modified environments, and how well do the individual species adapt and change their traits to fit the modified environments? My research focuses on the micro-evolutionary component. We use genetic and genomic tools to understand how plant populations respond to rapidly changing environments. One of my research interests is in ecological epigenetics: what role does epigenetic variation play in rapid responses and adaptation to changing environments? Other topics that I work on include urban evolution in plants, genetic and ecological aspects of plant invasions, the evolutionary ecology of asexually reproducing plants, and intraspecific variation in plant-microbiome interactions.

Research groups

CV

Employment

  • 2015–Present
    senior researcher, Netherlands Institute of Ecology
  • 2010–2015
    Tenure track researcher, Netherlands Institute of Ecology. Personal NWO-VIDI grant 2011-2016
  • 2009–2010
    Postdoc, Netherlands Institute of Ecology; and Laboratory of Nematology, Wageningen University
  • 2005–2009
    Postdoc, Netherlands Institute of Ecology. Personal NWO-VENI grant
  • 2003–2005
    Postdoc, Computational Genomics, Purdue University, Indiana USA

Education

1998–2003
PhD project, Utrecht University, in collaboration with Netherlands Institute of Ecology and Haifa University

Editorial board memberships

  • 2023–Present
    G3
  • 2020–Present
    Environmental Epigenetics

PhD students

  • Present
    Yvet Boele
    NIOO-KNAW, WUR
  • 2018–2023
    Cristian Peña Ponton
    NIOO-KNAW, WUR
    Promotors and Copromotors:
  • 2018–2023
    Morgane van Antro
    NIOO-KNAW, WUR
    Promotors and Copromotors:
  • 2019–2023
    Paola Rallo
    NIOO-KNAW, WUR
    Promotors and Copromotors:
  • 2013–2016
    Jun Shi
    Tübingen University
    Promotors and Copromotors:
  • 2011–2016
    Thomas van Gurp
    NIOO-KNAW, WUR
    Promotors and Copromotors:
  • 2011–2015
    Veronica Preite
    NIOO-KNAW, WUR
    Promotors and Copromotors:
  • 2011–2015
    Maartje Groot
    Radboud University Nijmegen
    Promotors and Copromotors:

Ancillary activities

Publications

Peer-reviewed publications

  • Evolutionary Applications
    13-03-2024

    Early developmental carry‐over effects on exploratory behaviour and DNA methylation in wild great tits (Parus major)

    Adverse, postnatal conditions experienced during development are known to induce lingering effects on morphology, behaviour, reproduction and survival. Despite the importance of early developmental stress for shaping the adult phenotype, it is largely unknown which molecular mechanisms allow for the induction and maintenance of such phenotypic effects once the early environmental conditions are released. Here we aimed to investigate whether lasting early developmental phenotypic changes are associated with post-developmental DNA methylation changes. We used a cross-foster and brood size experiment in great tit (Parus major) nestlings, which induced post-fledging effects on biometric measures and exploratory behaviour, a validated personality trait. We investigated whether these post-fledging effects are associated with DNA methylation levels of CpG sites in erythrocyte DNA. Individuals raised in enlarged broods caught up on their developmental delay after reaching independence and became more explorative as days since fledging passed, while the exploratory scores of individuals that were raised in reduced broods remained stable. Although we previously found that brood enlargement hardly affected the pre-fledging methylation levels, we found 420 CpG sites that were differentially methylated between fledged individuals that were raised in small versus large sized broods. A considerable number of the affected CpG sites were located in or near genes involved in metabolism, growth, behaviour and cognition. Since the biological functions of these genes line up with the observed post-fledging phenotypic effects of brood size, our results suggest that DNA methylation provides organisms the opportunity to modulate their condition once the environmental conditions allow it. In conclusion, this study shows that nutritional stress imposed by enlarged brood size during early development associates with variation in DNA methylation later in life. We propose that treatment-associated DNA methylation differences may arise in relation to pre- or post-fledging phenotypic changes, rather than that they are directly induced by the environment during early development.
    https://doi.org/10.1111/eva.13664
  • PLoS ONE
    08-09-2023

    Herbivory induced methylation changes in the Lombardy poplar

    A. Niloya Troyee, Cristian Peňa, Mónica Medrano, Koen Verhoeven, Conchita Alonso

    DNA cytosine methylation is an epigenetic mechanism involved in regulation of plant responses to biotic and abiotic stress and its ability to change can vary with the sequence context in which a cytosine appears (CpG, CHG, CHH, where H = Adenine, Thymine, Cytosine). Quantification of DNA methylation in model plant species is frequently addressed by Whole Genome Bisulfite Sequencing (WGBS), which requires a good-quality reference genome. Reduced Representation Bisulfite Sequencing (RRBS) is a cost-effective potential alternative for ecological research with limited genomic resources and large experimental designs. In this study, we provide for the first time a comprehensive comparison between the outputs of RRBS and WGBS to characterize DNA methylation changes in response to a given environmental factor. In particular, we used epiGBS (recently optimized RRBS) and WGBS to assess global and sequence-specific differential methylation after insect and artificial herbivory in clones of Populus nigra cv. 'italica'. We found that, after any of the two herbivory treatments, global methylation percentage increased in CHH, and the shift was detected as statistically significant only by epiGBS. As regards to loci-specific differential methylation induced by herbivory (cytosines in epiGBS and regions in WGBS), both techniques indicated the specificity of the response elicited by insect and artificial herbivory, together with higher frequency of hypo-methylation in CpG and hyper-methylation in CHH. Methylation changes were mainly found in gene bodies and intergenic regions when present at CpG and CHG and in transposable elements and intergenic regions at CHH context. Thus, epiGBS succeeded to characterize global, genome-wide methylation changes in response to herbivory in the Lombardy poplar. Our results support that epiGBS could be particularly useful in large experimental designs aimed to explore epigenetic changes of non-model plant species in response to multiple environmental factors.

    https://doi.org/10.1371/journal.pone.0291202
  • Biological Invasions
    24-06-2023

    Metabolomic profiling reveals shifts in defenses of an invasive plant

    Jun Shi, Mark Stahl, Ric C.H De Vos, Katja Tielbörger, Koen Verhoeven, Mirka Macel
    Post-introduction evolution of plant defense traits is fundamental to several important theories for plant invasiveness. Research on chemical defense traits of invasive plants has focused mostly on targeted chemical analysis, however, such analyses restrict novel insights to known compounds. Here, we provide an untargeted metabolomic analysis of native and invasive Purple Loosestrife populations and we experimentally test if admixture between introduced populations provides a basis for rapid defense chemistry evolution. Invasive populations showed improved growth and generalist herbivore resistance, but lower resistance to a specialist weevil, consistent with the Shifting Defense Hypothesis of plant invasions. Metabolomic profiling revealed large shifts in chemistry between native and invasive populations, including differences in alkaloids and flavonoids. Experimental admixture increased chemical diversity and plant growth in the native populations, indicating its potential to fuel rapid evolution, but admixture did not affect generalist and specialist herbivory. Our untargeted metabolomics analysis provides novel insights in the evolutionary changes in the chemistry of invasive plants, and reveals the chemical associations of a shift from defenses against specialist to generalist herbivores in invasive populations.
    https://doi.org/10.1007/s10530-023-03109-0
  • Frontiers in Plant Science
    21-06-2023

    Phylogenomic analysis provides insights into MADS-box and TCP gene diversification and floral development of the Asteraceae, supported by de novo genome and transcriptome sequences from dandelion (Taraxacum officinale)

    Wei Xiong, Judith Risse, Lidija Berke, Tao Zhao, Henri C. Van de Geest, Carla Oplaat, Marco Busscher, Julie Ferreira de Carvalho, Ingrid M. van der Meer, Koen Verhoeven, M. Eric Schranz, Kitty Vijverberg
    The Asteraceae is the largest angiosperm family with more than 25,000 species. Individual studies have shown that MADS-box and TCP transcription factors are regulators of the development and symmetry of flowers, contributing to their iconic flower-head (capitulum) and floret. However, a systematic study of MADS-box and TCP genes across the Asteraceae is lacking. We performed a comparative analysis of genome sequences of 33 angiosperm species including our de novo assembly of diploid sexual dandelion (Taraxacum officinale) and 11 other Asteraceae to investigate the lineage-specific evolution of MADS-box and TCP genes in the Asteraceae. We compared the phylogenomic results of MADS-box and TCP genes with their expression in T. officinale floral tissues at different developmental stages to demonstrate the regulation of genes with Asteraceae-specific attributes. Here, we show that MADS-box MIKCc and TCP-CYCLOIDEA (CYC) genes have expanded in the Asteraceae. The phylogenomic analysis identified AGAMOUS-like (AG-like: SEEDSTICK [STK]-like), SEPALATA-like (SEP3-like), and TCP-PROLIFERATING CELL FACTOR (PCF)-like copies with lineage-specific genomic contexts in the Asteraceae, Cichorioideae, or dandelion. Different expression patterns of some of these gene copies suggest functional divergence. We also confirm the presence and revisit the evolutionary history of previously named “Asteraceae-Specific MADS-box genes (AS-MADS).” Specifically, we identify non-Asteraceae homologs, indicating a more ancient origin of this gene clade. Syntenic relationships support that AS-MADS is paralogous to FLOWERING LOCUS C (FLC) as demonstrated by the shared ancient duplication of FLC and SEP3.
    https://doi.org/10.3389/fpls.2023.1198909
  • Molecular Ecology
    08-05-2023

    Developmental stress does not induce genome‐wide DNA methylation changes in wild great tit (Parus major) nestlings

    The environment experienced during early life is a crucial factor in the life of many organisms. This early life environment has been shown to have profound effects on morphology, physiology and fitness. However, the molecular mechanisms that mediate these effects are largely unknown, even though they are essential for our understanding of the processes that induce phenotypic variation in natural populations. DNA methylation is an epigenetic mechanism that has been suggested to explain such environmentally induced phenotypic changes early in life. To investigate whether DNA methylation changes are associated with experimentally induced early developmental effects, we cross-fostered great tit (Parus major) nestlings and manipulated their brood sizes in a natural study population. We assessed experimental brood size effects on pre-fledging biometry and behaviour. We linked this to genome-wide DNA methylation levels of CpG sites in erythrocyte DNA, using 122 individuals and an improved epiGBS2 laboratory protocol. Brood enlargement caused developmental stress and negatively affected nestling condition, predominantly during the second half of the breeding season, when conditions are harsher. Brood enlargement, however, affected nestling DNA methylation in only one CpG site and only if the hatch date was taken into account. In conclusion, this study shows that nutritional stress in enlarged broods does not associate with direct effects on genome-wide DNA methylation. Future studies should assess whether genome-wide DNA methylation variation may arise later in life as a consequence of phenotypic changes during early development.
    https://doi.org/10.1111/mec.16973
  • Ecology and Evolution
    01-05-2023

    Adaptive plasticity and fitness costs of endangered, nonendangered, and invasive plants in response to variation in nitrogen and phosphorus availabilities

    Vanessa Minden, Koen Verhoeven, Harry Olde Venterink
    Global change drivers such as eutrophication and plant invasions will create novel environments for many plant species. Through adaptive trait plasticity plants may maintain their performance under these novel conditions and may outcompete those showing low-adaptive trait plasticity. In a greenhouse study, we determined if plasticity in traits is adaptive or maladaptive in endangered, nonendangered, and invasive plant species in response to variation of nitrogen (N) and phosphorus (P) availability (N:P ratios 1.7, 15, and 135) and whether plastic trait responses are adaptive and/or costly for fitness (i.e., biomass). Species choice comprised 17 species from three functional groups (legumes, nonlegume forbs, and grasses), either classified as endangered, nonendangered, or invasive. After 2 months, plants were harvested and nine traits related to carbon assimilation and nutrient uptake were measured (leaf area, SLA, LDMC, SPAD, RMR, root length, SRL, root surface area, and PME activity). We found more traits responding plastically to variation in P than in N. Plasticity only created costs when P was varied. Plasticity in traits was mostly adaptively neutral toward fitness, with plasticity in three traits being similarly adaptive across all species groups: SPAD (as a measure of chlorophyll content, adaptive to N and P limitation), leaf area, and root surface area (adaptive to P limitation). We found little differences in trait plasticity between endangered, nonendangered, and invasive species. Synthesis. Along a gradient from N limitation, balanced N:P supply, and P limitation, we found that the type of fluctuating nutrient (i.e., if N or P is varied) is decisive for the adaptive value of a trait. Variation in P availability (from balanced supply to P limitation) created both a stronger reduction in fitness as well as created plasticity costs in more traits than variation in N availability (from balanced supply to N limitation). However, the patterns observed in our study may change if nutrient availability is altered, either by nutrient inputs or by a shift in nutrient availabilities, for example, by decreasing N input as foreseen by European Legislation, but without simultaneously decreasing P input.
    https://doi.org/10.1002/ece3.10075
  • Plant and Soil
    05-2023

    Inter- and intraspecific plant-soil feedbacks of grass species

    Paola Rallo, Freddy ten Hooven, Koen Verhoeven, Jan E. Kammenga, Wim H. van der Putten

    Background and aims: Plants continuously interact with soil microbiota. These plant-soil feedbacks (PSFs) are considered a driving force in plant community dynamics. However, most PSF information comes from inter-family studies, with limited information on possible causes. We studied the variation of PSFs between and within grass species and identified the soil microbes that are associated with the observed PSFs effects. Methods: We grew monocultures of ten cultivars of three grass species (Lolium perenne, Poa pratensis, Schedonorus arundinaceus) using a two-phase PSF experiment. We measured plant total biomass to determine PSFs between and within species and correlated it with sequenced rhizosphere bacteria and fungi. Results: In the soil conditioning phase, grass species developed microbial legacies that affected the performance of other grass species in the feedback phase. We detected overall negative interspecific PSFs. While we show that L. perenne and P. pratensis increased their performance respectively in conspecific and heterospecific soils, S. arundinaceus was not strongly affected by the legacies of the previous plant species. Contrary to our expectation, we found no evidence for intraspecific variation in PSFs. Bacterial taxa associated with PSFs included members of Proteobacteria, Firmicutes, Verrucomicrobia and Planctomycetes whereas fungal taxa included members of Ascomycota. Conclusion: Our results suggest differences in PSF effects between grass species, but not between cultivars within species. Thus, in the studied grass species, there might be limited potential for breeding on plant traits mediated by PSFs. Furthermore, we point out potential microbial candidates that might be driving the observed PSF effects that could be further explored.

    https://doi.org/10.1007/s11104-023-05893-z
  • Molecular Biology and Evolution
    01-04-2023

    Variation in DNA methylation in avian nestlings is largely determined by genetic effects

    Bernice Sepers, Rebecca Shuhua Chen, Michelle Memelink, Koen Verhoeven, Kees van Oers
    As environmental fluctuations are becoming more common, organisms need to rapidly adapt to anthropogenic, climatic, and ecological changes. Epigenetic modifications and DNA methylation in particular provide organisms with a mechanism to shape their phenotypic responses during development. Studies suggest that environmentally induced DNA methylation might allow for adaptive phenotypic plasticity that could last throughout an organism's lifetime. Despite a number of studies demonstrating environmentally induced DNA methylation changes, we know relatively little about what proportion of the epigenome is affected by environmental factors, rather than being a consequence of genetic variation. In the current study, we use a partial cross-foster design in a natural great tit (Parus major) population to disentangle the effects of common origin from common rearing environment on DNA methylation. We found that variance in DNA methylation in 8,315 CpG sites was explained by a common origin and only in 101 by a common rearing environment. Subsequently, we mapped quantitative trait loci for the brood of origin CpG sites and detected 754 cis and 4,202 trans methylation quantitative trait loci, involving 24% of the CpG sites. Our results indicate that the scope for environmentally induced methylation marks independent of the genotype is limited and that the majority of variation in DNA methylation early in life is determined by genetic factors instead. These findings suggest that there may be little opportunity for selection to act on variation in DNA methylation. This implies that most DNA methylation variation likely does not evolve independently of genomic changes.
    https://doi.org/10.1093/molbev/msad086
  • Journal of Evolutionary Biology
    22-02-2023

    Environmental and genealogical effects on DNA methylation in a widespread apomictic dandelion lineage

    Verónica Noé Ibañez, Morgane Van Antro, Cristian Peňa, Slavica Milanovic-Ivanovic, Niels C. A. M. Wagemaker, F. Gawehns, Koen Verhoeven
    DNA methylation in plant genomes occurs in different sequences and genomic contexts that have very different properties. DNA methylation that occurs in CG (mCG) sequence context shows transgenerational stability and high epimutation rate, and can thus provide genealogical information at short time scales. However, due to meta-stability and because mCG variants may arise due to other factors than epimutation, such as environmental stress exposure, it is not clear how well mCG captures genealogical information at micro-evolutionary time scales. Here, we analysed DNA methylation variation between accessions from a geographically widespread, apomictic common dandelion (Taraxacum officinale) lineage when grown experimentally under different light conditions. Using a reduced-representation bisulphite sequencing approach, we show that the light treatment induced differentially methylated cytosines (DMCs) in all sequence contexts, with a bias towards transposable elements. Accession differences were associated mainly with DMCs in CG context. Hierarchical clustering of samples based on total mCG profiles revealed a perfect clustering of samples by accession identity, irrespective of light conditions. Using microsatellite information as a benchmark of genetic divergence within the clonal lineage, we show that genetic divergence between accessions correlates strongly with overall mCG profiles. However, our results suggest that environmental effects that do occur in CG context may produce a heritable signal that partly dilutes the genealogical signal. Our study shows that methylation information in plants can be used to reconstruct micro-evolutionary genealogy, providing a useful tool in systems that lack genetic variation such as clonal and vegetatively propagated plants.
    https://doi.org/10.1111/jeb.14162
  • Molecular Ecology
    20-11-2022

    DNA methylation in clonal Duckweed lineages ( Lemna minor L.) reflects current and historical environmental exposures

    Morgane Van Antro, Stella Prelovsek, Slavica Milanovic-Ivanovic, F. Gawehns, Niels C. A. M. Wagemaker, Mohamed Mysara, Nele Horemans, Philippine Vergeer, Koen Verhoeven

    Environmentally induced DNA methylation variants may mediate gene expression responses to environmental changes. If such induced variants are transgenerationally stable, there is potential for expression responses to persist over multiple generations. Our current knowledge in plants, however, is almost exclusively based on studies conducted in sexually reproducing species where the majority of DNA methylation changes are subject to resetting in germlines, limiting the potential for transgenerational epigenetics stress memory. Asexual reproduction circumvents germlines, and may therefore be more conducive to long-term inheritance of epigenetic marks. Taking advantage of the rapid clonal reproduction of the common duckweed Lemna minor, we hypothesize that long-term, transgenerational stress memory from exposure to high temperature can be detected in DNA methylation profiles. Using a reduced representation bisulphite sequencing approach (epiGBS), we show that temperature stress induces DNA hypermethylation at many CG and CHG cytosine contexts but not CHH. Additionally, differential methylation in CHG context that was observed was still detected in a subset of cytosines, even after 3–12 generations of culturing in a common environment. This demonstrates a memory effect of stress reflected in the methylome and that persists over multiple clonal generations. Structural annotation revealed that this memory effect in CHG methylation was enriched in transposable elements. The observed epigenetic stress memory is probably caused by stable transgenerational persistence of temperature-induced DNA methylation variants across clonal generations. To the extent that such epigenetic memory has functional consequences for gene expression and phenotypes, this result suggests potential for long-term modulation of stress responses in asexual plants.

    https://doi.org/10.1111/mec.16757
  • Molecular Ecology
    11-2022

    Adapting to climate with limited genetic diversity

    Anne Aagaard, Shenglin Liu, Tom Tregenza, Marie Braad Lund, Andreas Schramm, Koen Verhoeven, Jesper Bechsgaard, Trine Bilde

    Understanding the role of genetic and nongenetic variants in modulating phenotypes is central to our knowledge of adaptive responses to local conditions and environmental change, particularly in species with such low population genetic diversity that it is likely to limit their evolutionary potential. A first step towards uncovering the molecular mechanisms underlying population-specific responses to the environment is to carry out environmental association studies. We associated climatic variation with genetic, epigenetic and microbiome variation in populations of a social spider with extremely low standing genetic diversity. We identified genetic variants that are associated strongly with environmental variation, particularly with average temperature, a pattern consistent with local adaptation. Variation in DNA methylation in many genes was strongly correlated with a wide set of climate parameters, thereby revealing a different pattern of associations than that of genetic variants, which show strong correlations to a more restricted range of climate parameters. DNA methylation levels were largely independent of cis-genetic variation and of overall genetic population structure, suggesting that DNA methylation can work as an independent mechanism. Microbiome composition also correlated with environmental variation, but most strong associations were with precipitation-related climatic factors. Our results suggest a role for both genetic and nongenetic mechanisms in shaping phenotypic responses to local environments.

    https://doi.org/10.1111/mec.16696
  • Frontiers in Ecology and Evolution
    12-05-2022

    Genetic and Epigenetic Differentiation Across Intertidal Gradients in the Foundation Plant Spartina alterniflora

    Jeannie M. Mounger, Isolde van Riemsdijk, M. Teresa Boquete, Niels C. A. M. Wagemaker, Samar Fatma, Marta H. Robertson, Sandy A. Voors, Jenna Oberstaller, F. Gawehns, Torrance C. Hanley, Ivo Grosse, Koen Verhoeven, Erik E. Sotka, Catherine A. Gehring, A. Randall Hughes, David B. Lewis, Marc W. Schmid, Christina L. Richards

    Ecological genomics approaches have informed us about the structure of genetic diversity in natural populations that might underlie patterns in trait variation. However, we still know surprisingly little about the mechanisms that permit organisms to adapt to variable environmental conditions. The salt marsh foundation plant Spartina alterniflora exhibits a dramatic range in phenotype that is associated with a pronounced intertidal environmental gradient across a narrow spatial scale. Both genetic and non-genetic molecular mechanisms might underlie this phenotypic variation. To investigate both, we used epigenotyping-by-sequencing (epiGBS) to evaluate the make-up of natural populations across the intertidal environmental gradient. Based on recent findings, we expected that both DNA sequence and DNA methylation diversity would be explained by source population and habitat within populations. However, we predicted that epigenetic variation might be more strongly associated with habitat since similar epigenetic modifications could be rapidly elicited across different genetic backgrounds by similar environmental conditions. Overall, with PERMANOVA we found that population of origin explained a significant amount of the genetic (8.6%) and epigenetic (3.2%) variance. In addition, we found that a small but significant amount of genetic and epigenetic variance (<1%) was explained by habitat within populations. The interaction of population and habitat explained an additional 2.9% of the genetic variance and 1.4% of the epigenetic variance. By examining genetic and epigenetic variation within the same fragments (variation in close-cis), we found that population explained epigenetic variation in 9.2% of 8,960 tested loci, even after accounting for differences in the DNA sequence of the fragment. Habitat alone explained very little (<0.1%) of the variation in these close-cis comparisons, but the interaction of population and habitat explained 2.1% of the epigenetic variation in these loci. Using multiple matrix regression with randomization (MMRR) we found that phenotypic differences in natural populations were correlated with epigenetic and environmental differences even when accounting for genetic differences. Our results support the contention that sequence variation explains most of the variation in DNA methylation, but we have provided evidence that DNA methylation distinctly contributes to plant responses in natural populations.

    https://doi.org/10.3389/fevo.2022.868826
  • Functional Ecology
    2022

    Experimental evidence of rapid heritable adaptation in the absence of initial standing genetic variation

    The success of genetically depauperate populations in the face of environmental change is contrary to the expectation that high genetic diversity is required for rapid adaptation. Alternative pathways such as environmentally induced genetic modifications and non-genetic heritable phenotypes have been proposed mechanisms for heritable adaptation within an ecologically relevant time frame. However, experimental evidence is currently lacking to establish if, and to what extent, these sources of phenotypic variation can produce a response.
    To test if adaptation can rapidly occur in the absence of initial standing genetic variation and recombination in small populations, we (a) exposed replicate monoclonal populations of the microzooplankton Brachionus calyciflorus to a culturing regime that selected for phenotypic variants with elevated population growth with either high or low phosphorus food for a period of 55 days and (b) examined population level response in two fully factorial common garden experiments at day 15 and 35 of the exposure experiment.
    Within six generations, we observed heritable local adaptation to nutrient limitation. More specifically, populations with a history of exposure to low P food exhibited higher population growth rates under low P food conditions than populations with a high P exposure history. However, the capacity for such a response was found to vary among clones.
    Our study finds that although standing genetic variation is considered essential for rapid heritable adaptation, the rapid emergence of de novo genetic variation or alternative sources of phenotypic variation could aid in the establishment and persistence of low-diversity populations.
    https://doi.org/10.1111/1365-2435.13943
  • mSystems
    2022

    Exploring the Interspecific Interactions and the Metabolome of the Soil Isolate Hylemonella gracilis

    Olaf Tyc, Purva Kulkarni, Adam Ossowicki, Vittorio Tracanna, Marnix H Medema, Peter van Baarlen, Wilfred F J van IJcken, Koen Verhoeven, Paolina Garbeva
    Microbial community analysis of aquatic environments showed that an important component of its microbial diversity consists of bacteria with cell sizes of ~0.1 μm. Such small bacteria can show genomic reductions and metabolic dependencies with other bacteria. However, so far, no study has investigated if such bacteria exist in terrestrial environments like soil. Here, we isolated soil bacteria that passed through a 0.1-μm filter. The complete genome of one of the isolates was sequenced and the bacterium was identified as Hylemonella gracilis. A set of coculture assays with phylogenetically distant soil bacteria with different cell and genome sizes was performed. The coculture assays revealed that H. gracilis grows better when interacting with other soil bacteria like Paenibacillus sp. AD87 and Serratia plymuthica. Transcriptomics and metabolomics showed that H. gracilis was able to change gene expression, behavior, and biochemistry of the interacting bacteria without direct cell-cell contact. Our study indicates that in soil there are bacteria that can pass through a 0.1-μm filter. These bacteria may have been overlooked in previous research on soil microbial communities. Such small bacteria, exemplified here by H. gracilis, can induce transcriptional and metabolomic changes in other bacteria upon their interactions in soil. In vitro, the studied interspecific interactions allowed utilization of growth substrates that could not be utilized by monocultures, suggesting that biochemical interactions between substantially different sized soil bacteria may contribute to the symbiosis of soil bacterial communities.
    https://doi.org/10.1128/msystems.00574-22
  • Journal of Animal Ecology
    2022

    Changes in the rearing environment cause reorganization of molecular networks associated with DNA methylation

    Bridgett vonHoldt, Rebecca Y. Kartzinel, Kees van Oers, Koen Verhoeven, Jenny Ouyang

    Disentangling the interaction between the genetic basis and environmental context underlying phenotypic variation is critical for understanding organismal evolution. Environmental change, such as increased rates of urbanization, can induce shifts in phenotypic plasticity with some individuals adapting to city life while others are displaced. A key trait that can facilitate adaptation is the degree at which animals respond to stressors. This stress response, which includes elevation of baseline circulating concentrations of glucocorticoids, has a heritable component and exhibits intra- and inter-individual variation. However, the mechanisms behind this variability and whether they might be responsible for adaptation to different environments are not known. Variation in DNA methylation can be a potential mechanism that mediates environmental effects on the stress response, as early-life stressors increase glucocorticoid concentrations and change adult phenotype. We used an inter- and intra-environmental cross-foster experiment to analyse the contribution of DNA methylation to early-life phenotypic variation. We found that at hatching, urban house wren (Troglodytes aedon) offspring had higher methylation frequencies compared with their rural counterparts. We also observed age-related patterns in offspring methylation, indicating the developmental effects of the rearing environment on methylation. At fledgling, differential methylation analyses showed that cellular respiration genes were differentially methylated in broods of different origins and behavioural and metabolism genes were differentially methylated in broods of different rearing environments. Lastly, hyper-methylation of a single gene (CNTNAP2) is associated with decreased glucocorticoid levels and the rearing environment. These differential methylation patterns linked to a specific physiological phenotype suggest that DNA methylation may be a mechanism by which individuals adjust to novel environments during their lifespan. Characterizing genetic and environmental influences on methylation is critical for understanding the role of epigenetic mechanisms in evolutionary adaptation.

    https://doi.org/10.1111/1365-2656.13878
  • Molecular Ecology Resources
    2022

    epiGBS2

    F. Gawehns, Maarten Postuma, Morgane Van Antro, Adam Nunn, Bernice Sepers, Samar Fatma, Thomas Van Gurp, Niels C. A. M. Wagemaker, A.C. Mateman, Slavica Milanovic-Ivanovic, Ivo Groβe, Kees van Oers, Philippine Vergeer, Koen Verhoeven

    Several reduced-representation bisulfite sequencing methods have been developed in recent years to determine cytosine methylation de novo in nonmodel species. Here, we present epiGBS2, a laboratory protocol based on epiGBS with a revised and user-friendly bioinformatics pipeline for a wide range of species with or without a reference genome. epiGBS2 is cost- and time-efficient and the computational workflow is designed in a user-friendly and reproducible manner. The library protocol allows a flexible choice of restriction enzymes and a double digest. The bioinformatics pipeline was integrated in the Snakemake workflow management system, which makes the pipeline easy to execute and modular, and parameter settings for important computational steps flexible. We implemented bismark for alignment and methylation analysis and we preprocessed alignment files by double masking to enable single nucleotide polymorphism calling with Freebayes (epiFreebayes). The performance of several critical steps in epiGBS2 was evaluated against baseline data sets from Arabidopsis thaliana and great tit (Parus major), which confirmed its overall good performance. We provide a detailed description of the laboratory protocol and an extensive manual of the bioinformatics pipeline, which is publicly accessible on github (https://github.com/nioo-knaw/epiGBS2) and zenodo (https://doi.org/10.5281/zenodo.4764652).

    https://doi.org/10.1111/1755-0998.13597
  • Scientific Reports
    12-2021

    Gene body DNA methylation in seagrasses

    Laura Entrambasaguas, Miriam Ruocco, Koen Verhoeven, Gabriele Procaccini, Lazaro Marín-Guirao

    The role of DNA methylation and its interaction with gene expression and transcriptome plasticity is poorly understood, and current insight comes mainly from studies in very few model plant species. Here, we study gene body DNA methylation (gbM) and gene expression patterns in ecotypes from contrasting thermal environments of two marine plants with contrasting life history strategies in order to explore the potential role epigenetic mechanisms could play in gene plasticity and responsiveness to heat stress. In silico transcriptome analysis of CpGO/E ratios suggested that the bulk of Posidonia oceanica and Cymodocea nodosa genes possess high levels of intragenic methylation. We also observed a correlation between gbM and gene expression flexibility: genes with low DNA methylation tend to show flexible gene expression and plasticity under changing conditions. Furthermore, the empirical determination of global DNA methylation (5-mC) showed patterns of intra and inter-specific divergence that suggests a link between methylation level and the plants’ latitude of origin and life history. Although we cannot discern whether gbM regulates gene expression or vice versa, or if other molecular mechanisms play a role in facilitating transcriptome responsiveness, our findings point to the existence of a relationship between gene responsiveness and gbM patterns in marine plants.

    https://doi.org/10.1038/s41598-021-93606-w
  • Epigenetics and Chromatin
    12-2021

    The methylome of Biomphalaria glabrata and other mollusks

    Nelia Luviano, Marie Lopez, F. Gawehns, Cristian Chaparro, Paola B. Arimondo, Slavica Milanovic-Ivanovic, Patrice David, Koen Verhoeven, Céline Cosseau, Christoph Grunau

    Background: 5-Methylcytosine (5mC) is an important epigenetic mark in eukaryotes. Little information about its role exists for invertebrates. To investigate the contribution of 5mC to phenotypic variation in invertebrates, alteration of methylation patterns needs to be produced. Here, we apply new non-nucleoside DNA methyltransferase inhibitors (DNMTi) to introduce aleatory changes into the methylome of mollusk species. Results: Flavanone inhibitor Flv1 was efficient in reducing 5mC in the freshwater snails Biomphalaria glabrata and Physa acuta, and to a lesser degree, probably due to lower stability in sea water, in the oyster Crassostrea gigas. Flv1 has no toxic effects and significantly decreased the 5mC level in the treated B. glabrata and in its offspring. Drug treatment triggers significant variation in the shell height in both generations. A reduced representation bisulfite-sequencing method called epiGBS corroborates hypomethylation effect of Flv1 in both B. glabrata generations and identifies seven Differential Methylated Regions (DMR) out of 32 found both in Flv1-exposed snails and its progeny, from which 5 were hypomethylated, demonstrating a multigenerational effect. By targeted bisulfite sequencing, we confirmed hypomethylation in a locus and show that it is associated with reduced gene expression. Conclusions: Flv1 is a new and efficient DNMTi that can be used to induce transient and heritable modifications of the epigenetic landscape and phenotypic traits in mollusks, a phylum of the invertebrates in which epigenetics is understudied.

    https://doi.org/10.1186/s13072-021-00422-7
  • Genome Biology
    06-10-2020

    AlphaBeta

    Yadollah Shahryary, Aikaterini Symeonidi, Rashmi R. Hazarika, Johanna Denkena, Talha Mubeen, Brigitte Hofmeister, Thomas Van Gurp, Maria Colomé-Tatché, Koen Verhoeven, Gerald Tuskan, Robert J. Schmitz, Frank Johannes

    Stochastic changes in DNA methylation (i.e., spontaneous epimutations) contribute to methylome diversity in plants. Here, we describe AlphaBeta, a computational method for estimating the precise rate of such stochastic events using pedigree-based DNA methylation data as input. We demonstrate how AlphaBeta can be employed to study transgenerationally heritable epimutations in clonal or sexually derived mutation accumulation lines, as well as somatic epimutations in long-lived perennials. Application of our method to published and new data reveals that spontaneous epimutations accumulate neutrally at the genome-wide scale, originate mainly during somatic development and that they can be used as a molecular clock for age-dating trees.

    https://doi.org/10.1186/s13059-020-02161-6
  • Integrative and Comparative Biology
    2020

    Epigenetics of animal personality

    Kees van Oers, Bernice Sepers, W. Sies, F. Gawehns, Koen Verhoeven, Veronika Laine
    The search for the hereditary mechanisms underlying quantitative traits traditionally focused on the identification of underlying genomic polymorphisms such as single-nucleotide polymorphisms. It has now become clear that epigenetic mechanisms, such as DNA methylation, can consistently alter gene expression over multiple generations. It is unclear, however, if and how DNA methylation can stably be transferred from one generation to the next and can thereby be a component of the heritable variation of a trait. In this study, we explore whether DNA methylation responds to phenotypic selection using whole-genome and genome-wide bisulfite approaches. We assessed differential erythrocyte DNA methylation patterns between extreme personality types in the Great Tit (Parus major). For this, we used individuals from a four-generation artificial bi-directional selection experiment and siblings from eight F2 inter-cross families. We find no differentially methylated sites when comparing the selected personality lines, providing no evidence for the so-called epialleles associated with exploratory behavior. Using a pair-wise sibling design in the F2 intercrosses, we show that the genome-wide DNA methylation profiles of individuals are mainly explained by family structure, indicating that the majority of variation in DNA methylation in CpG sites between individuals can be explained by genetic differences. Although we found some candidates explaining behavioral differences between F2 siblings, we could not confirm this with a whole-genome approach, thereby confirming the absence of epialleles in these F2 intercrosses. We conclude that while epigenetic variation may underlie phenotypic variation in behavioral traits, we were not able to find evidence that DNA methylation can explain heritable variation in personality traits in Great Tits.
    https://doi.org/10.1093/icb/icaa138
  • New Phytologist
    01-2019

    Opportunities and limitations of reduced representation bisulfite sequencing in plant ecological epigenomics

    Ovidiu Paun, Koen Verhoeven, Christina L. Richards
    Investigating the features and implications of epigenetic mechanisms across the breadth of organisms and ecosystems is important for understanding the ecological relevance of epigenetics. Several cost-effective reduced representation bisulfite sequencing approaches (RRBS) have been recently developed and applied to different organisms that lack a well annotated reference genome. These new approaches improve the assessment of epigenetic diversity in ecological settings and may provide functional insights. We assess here the opportunities and limitations of RRBS in nonmodel plant species. Well thought out experimental designs that include complementary gene expression studies, and the improvement of genomics resources for the target group, promise to maximize the effect of future RRBS studies.
    https://doi.org/10.1111/nph.15388
  • Biological Invasions
    01-09-2018

    Effects of admixture in native and invasive populations of Lythrum salicaria

    Jun Shi, Mirka Macel, Katja Tielbörger, Koen Verhoeven
    Intraspecific hybridization between diverged populations can enhance fitness via various genetic mechanisms. The benefits of such admixture have been proposed to be particularly relevant in biological invasions, when invasive populations originating from different source populations are found sympatrically. However, it remains poorly understood if admixture is an important contributor to plant invasive success and how admixture effects compare between invasive and native ranges. Here, we used experimental crosses in Lythrum salicaria, a species with well-established history of multiple introductions to Eastern North America, to quantify and compare admixture effects in native European and invasive North American populations. We observed heterosis in between-population crosses both in native and invasive ranges. However, invasive-range heterosis was restricted to crosses between two different Eastern and Western invasion fronts, whereas heterosis was absent in geographically distant crosses within a single large invasion front. Our results suggest that multiple introductions have led to already-admixed invasion fronts, such that experimental crosses do not further increase performance, but that contact between different invasion fronts further enhances fitness after admixture. Thus, intra-continental movement of invasive plants in their introduced range has the potential to boost invasiveness even in well-established and successfully spreading invasive species.
    https://doi.org/10.1007/s10530-018-1707-2
  • Ecology and Evolution
    03-2018

    Epigenetic population differentiation in field- and common garden-grown Scabiosa columbaria plants

    Maartje P. Groot, Niels C. A. M. Wagemaker, N.J. Ouborg, Koen Verhoeven, Philippine Vergeer

    Populations often differ in phenotype and these differences can be caused by adaptation by natural selection, random neutral processes, and environmental responses. The most straightforward way to divide mechanisms that influence phenotypic variation is heritable variation and environmental-induced variation (e.g., plasticity). While genetic variation is responsible for most heritable phenotypic variation, part of this is also caused by nongenetic inheritance. Epigenetic processes may be one of the underlying mechanisms of plasticity and nongenetic inheritance and can therefore possibly contribute to heritable differences through drift and selection. Epigenetic variation may be influenced directly by the environment, and part of this variation can be transmitted to next generations. Field screenings combined with common garden experiments will add valuable insights into epigenetic differentiation, epigenetic memory and can help to reveal part of the relative importance of epigenetics in explaining trait variation. We explored both genetic and epigenetic diversity, structure and differentiation in the field and a common garden for five British and five French Scabiosa columbaria populations. Genetic and epigenetic variation was subsequently correlated with trait variation. Populations showed significant epigenetic differentiation between populations and countries in the field, but also when grown in a common garden. By comparing the epigenetic variation between field and common garden-grown plants, we showed that a considerable part of the epigenetic memory differed from the field-grown plants and was presumably environmentally induced. The memory component can consist of heritable variation in methylation that is not sensitive to environments and possibly genetically based, or environmentally induced variation that is heritable, or a combination of both. Additionally, random epimutations might be responsible for some differences as well. By comparing epigenetic variation in both the field and common environment, our study provides useful insight into the environmental and genetic components of epigenetic variation.

    https://doi.org/10.1002/ece3.3931
  • Ecology and Evolution
    03-2018

    Increased transgenerational epigenetic variation, but not predictable epigenetic variants, after environmental exposure in two apomictic dandelion lineages

    Veronica Preite, Carla Oplaat, Arjen Biere, Jan Kirschner, Wim H. van der Putten, Koen Verhoeven

    DNA methylation is one of the mechanisms underlying epigenetic modifications. DNA methylations can be environmentally induced and such induced modifications can at times be transmitted to successive generations. However, it remains speculative how common such environmentally induced transgenerational DNA methylation changes are and if they persist for more than one offspring generation. We exposed multiple accessions of two different apomictic dandelion lineages of the Taraxacum officinale group (Taraxacum alatum and T. hemicyclum) to drought and salicylic acid (SA) treatment. Using methylation-sensitive amplified fragment length polymorphism markers (MS-AFLPs) we screened anonymous methylation changes at CCGG restriction sites throughout the genome after stress treatments and assessed the heritability of induced changes for two subsequent unexposed offspring generations. Irrespective of the initial stress treatment, a clear buildup of heritable DNA methylation variation was observed across three generations, indicating a considerable background rate of heritable epimutations. Less evidence was detected for environmental effects. Drought stress showed some evidence for accession-specific methylation changes, but only in the exposed generation and not in their offspring. By contrast, SA treatment caused an increased rate of methylation change in offspring of treated plants. These changes were seemingly undirected resulting in increased transgenerational epigenetic variation between offspring individuals, but not in predictable epigenetic variants. While the functional consequences of these MS-AFLP-detected DNA methylation changes remain to be demonstrated, our study shows that (1) stress-induced transgenerational DNA methylation modification in dandelions is genotype and context-specific; and (2) inherited environmental DNA methylation effects are mostly undirected and not targeted to specific loci.

    https://doi.org/10.1002/ece3.3871
  • Nature Communications
    2018

    Cross-species interference of gene expression

    Irene de Bruijn, Koen Verhoeven
    Microbes can contribute to protection of animals and plants against diseases. A recent study reveals a mechanism by which a bacterium controls fungal infection in wheat, involving secretion of a metabolite that affects histone acetyltransferase activity of a plant pathogenic fungus.
    https://doi.org/10.1038/s41467-018-07353-0
  • New Phytologist
    2018

    Intergenerational environmental effects: Functional signals in offspring transcriptomes and metabolomes after parental jasmonic acid treatment in apomictic dandelion

    Koen Verhoeven, Eline H. Verbon, Thomas Van Gurp, Carla Oplaat, Julie Ferreira de Carvalho, Alison M. Morse, Mark Stahl, Mirka Macel, L.M. McIntyre
    Parental environments can influence offspring traits. However, the magnitude of the impact of parental environments on offspring molecular phenotypes is poorly understood. Here, we test the direct effects and intergenerational effects of jasmonic acid (JA) treatment, which is involved in herbivory-induced defense signaling, on transcriptomes and metabolomes in apomictic common dandelion (Taraxacum officinale).
    In a full factorial crossed design with parental and offspring JA and control treatments, we performed leaf RNA-seq gene expression analysis, LC-MS metabolomics and total phenolics assays in offspring plants.
    Expression analysis, leveraged by a de novo assembled transcriptome, revealed an induced response to JA exposure that is consistent with known JA effects. The intergenerational effect of treatment was considerable: 307 of 858 detected JA-responsive transcripts were affected by parental JA treatment. In terms of the numbers of metabolites affected, the magnitude of the chemical response to parental JA exposure was c. 10% of the direct JA treatment response. Transcriptome and metabolome analyses both identified the phosphatidylinositol signaling pathway as a target of intergenerational JA effects.
    Our results highlight that parental environments can have substantial effects in offspring generations. Transcriptome and metabolome assays provide a basis for zooming in on the potential mechanisms of inherited JA effects.
    https://doi.org/10.1111/nph.14835
  • Frontiers in Plant Science
    2018

    Transgenerational Effects and Epigenetic Memory in the Clonal Plant Trifolium repens

    Alejandra Pilar Rendina González, Veronica Preite, Koen Verhoeven, Vít Latzel
    Transgenerational effects can modify phenotypes of offspring generations playing thus a potentially important role in ecology and evolution of many plant species. These effects have been studied mostly across generations of sexually reproducing species. A substantial proportion of plant species are however reproducing asexually, for instance via clonal growth. Transgenerational effects are thought to be enabled by heritable epigenetic modification of DNA, although unambiguous evidence is still scarce. On the clonal herb white clover (Trifolium repens), we tested the generality of clonal transgenerational effects across five genotypes and five parental environments including soil contamination and above-ground competition. Moreover, by genome wide-methylation variation analysis we explored the role of drought, one of the parental environments that triggered the strongest transgenerational effects. We tested the induction of epigenetic changes in offspring generations using several intensities and durations of drought stress. We found that transgenerational effects of different environments were highly genotype specific and all tested environments triggered transgenerational effects at least in some genotypes. In addition, parental drought stresses triggered epigenetic change in T. repens and most of the induced epigenetic change was maintained across several clonal offspring generations. We conclude that transgenerational effects are common and genotype specific in clonal plant T. repens and potentially under epigenetic control.
    https://doi.org/10.3389/fpls.2018.01677
  • Planta
    2018

    LAESI mass spectrometry imaging as a tool to differentiate the root metabolome of native and range-expanding plant species

    Purva Kulkarni, Rutger Wilschut, Koen Verhoeven, Wim H. van der Putten, Paolina Garbeva
    Our understanding of chemical diversity in biological samples has greatly improved through recent advances in mass spectrometry (MS). MS-based-imaging (MSI) techniques have further enhanced this by providing spatial information on the distribution of metabolites and their relative abundance. This study aims to employ laser-assisted electrospray ionization (LAESI) MSI as a tool to profile and compare the root metabolome of two pairs of native and range expanding plant species. It has been proposed that successful range-expanding plant species, like introduced exotic invaders, have a novel, or a more diverse secondary chemistry. Although some tests have been made using aboveground plant materials, tests using root materials are rare. We tested the hypothesis that range-expanding plants possess more diverse root chemistries than native plant species. To examine the root chemistry of the selected plant species, LAESI-MSI was performed in positive ion mode and data was acquired in a mass range of m/z 50-1200 with a spatial resolution of 100 μm. The acquired data was analyzed using in-house scripts, and differences in the spatial profiles were studied for discriminatory mass features. The results revealed clear differences in the metabolite profiles amongst and within both pairs of congeneric plant species, in the form of distinct metabolic fingerprints. The use of ambient conditions and the fact that no sample preparation was required, established LAESI-MSI as an ideal technique for untargeted metabolomics and for direct correlation of the acquired data to the underlying metabolomic complexity present in intact plant samples.
    https://doi.org/10.1101/322867
  • Genome Biology and Evolution
    01-11-2017

    Determinants of the Efficacy of Natural Selection on Coding and Noncoding Variability in Two Passerine Species

    Pádraic Corcoran, Toni I. Gossmann, Henry J Barton, Jon Slate, Kai Zeng, Veronika Laine, Kees van Oers, Koen Verhoeven, Marcel E. Visser
    Population genetic theory predicts that selection should be more effective when the effective population size (Ne) is larger, and that the efficacy of selection should correlate positively with recombination rate. Here, we analyzed the genomes of ten great tits and ten zebra finches. Nucleotide diversity at 4-fold degenerate sites indicates that zebra finches have a 2.83-fold larger Ne. We obtained clear evidence that purifying selection is more effective in zebra finches. The proportion of substitutions at 0-fold degenerate sites fixed by positive selection (α) is high in both species (great tit 48%; zebra finch 64%) and is significantly higher in zebra finches. When α was estimated on GC-conservative changes (i.e., between A and T and between G and C), the estimates reduced in both species (great tit 22%; zebra finch 53%). A theoretical model presented herein suggests that failing to control for the effects of GC-biased gene conversion (gBGC) is potentially a contributor to the overestimation of α, and that this effect cannot be alleviated by first fitting a demographic model to neutral variants. We present the first estimates in birds for α in the untranslated regions, and found evidence for substantial adaptive changes. Finally, although purifying selection is stronger in high-recombination regions, we obtained mixed evidence for α increasing with recombination rate, especially after accounting for gBGC. These results highlight that it is important to consider the potential confounding effects of gBGC when quantifying selection and that our understanding of what determines the efficacy of selection is incomplete.
    https://doi.org/10.1093/gbe/evx213
  • Oecologia
    01-06-2017

    Evolutionary responses to climate change in a range expanding plant

    Mirka Macel, Tomás Dostálek, Sonja Esch, Anna Bucharová, Nicole M. van Dam, Katja Tielbörger, Koen Verhoeven, Zuzana Münzbergová
    To understand the biological effects of climate change, it is essential to take into account species' evolutionary responses to their changing environments. Ongoing climate change is resulting in species shifting their geographical distribution ranges poleward. We tested whether a successful range expanding plant has rapidly adapted to the regional conditions in its novel range, and whether adaptation could be driven by herbivores. Furthermore, we investigated if enemy release occurred in the newly colonized areas and whether plant origins differed in herbivore resistance. Plants were cloned and reciprocally transplanted between three experimental sites across the range. Effects of herbivores on plant performance were tested by individually caging plants with either open or closed cages. There was no indication of (regional) adaptation to abiotic conditions. Plants originating from the novel range were always larger than plants from the core distribution at all experimental sites, with or without herbivory. Herbivore damage was highest and not lowest at the experimental sites in the novel range, suggesting no release from enemy impact. Genotypes from the core were more damaged compared to genotypes from newly colonized areas at the most northern site in the novel range, which was dominated by generalist slug herbivory. We also detected subtle shifts in chemical defenses between the plant origins. Genotypes from the novel range had more inducible defenses. Our results suggest that plants that are expanding their range with climate change may evolve increased vigor and altered herbivore resistance in their new range, analogous to invasive plants.
    https://doi.org/10.1007/s00442-017-3864-x
  • Ecology Letters
    2017

    Ecological plant epigenetics: Evidence from model and non-model species, and the way forward

    Christina L. Richards, Conchita Alonso, Claude Becker, Oliver Bossdorf, Etienne Bucher, Maria Colomé-Tatché, Walter Durka, Jan Engelhardt, Bence Gaspar, Andreas Gogol-Döring, Ivo Grosse, Thomas Van Gurp, Katrin Heer, Ilkka Kronholm, Christian Lampei, Vít Latzel, Marie Mirouze, Lars Opgenoorth, Ovidiu Paun, Sonja J. Prohaska, Stefan A. Rensing, Peter F. Stadler, Emiliano Trucchi, Kristian Ullrich, Koen Verhoeven
    https://doi.org/10.1111/ele.12858
  • Molecular Biology and Evolution
    2017

    Small RNAs reflect grandparental environments in apomictic dandelion

    L. Morgado, Veronica Preite, Carla Oplaat, S. Anava, Julie Ferreira de Carvalho, O. Rechavi, F. Johannes, Koen Verhoeven
    Plants can show long-term effects of environmental stresses and in some cases a stress “memory” has been reported to persist across generations, potentially mediated by epigenetic mechanisms. However, few documented cases exist of transgenerational effects that persist for multiple generations and it remains unclear if or how epigenetic mechanisms are involved. Here, we show that the composition of small regulatory RNAs in apomictic dandelion lineages reveals a footprint of drought stress and salicylic acid treatment experienced two generations ago. Overall proportions of 21 and 24 nt RNA pools were shifted due to grandparental treatments. While individual genes did not show strong up- or downregulation of associated sRNAs, the subset of genes that showed the strongest shifts in sRNA abundance was significantly enriched for several GO terms including stress-specific functions. This suggests that a stress-induced signal was transmitted across multiple unexposed generations leading to persistent changes in epigenetic gene regulation.
    https://doi.org/10.1093/molbev/msx150
  • PLoS Biology
    05-01-2016

    A Latex Metabolite Benefits Plant Fitness under Root Herbivore Attack

    Meret Huber, Janina Epping, Christian Schulze Gronover, Julia Fricke, Zohra Aziz, Théo Brillatz, Michael Swyers, Tobias G. Köllner, Heiko Vogel, Almuth Hammerbacher, Daniella Triebwasser-Freese, Christelle A. M. Robert, Koen Verhoeven, Veronica Preite, Jonathan Gershenzon, Matthias Erb

    Dandelion plants protect their roots from the larva of the common cockchafer beetle by accumulating and releasing a sesquiterpene lactone deterrent in their exuded latex.

    https://doi.org/10.1371/journal.pbio.1002332
  • BMC Genomics
    2016

    Gene and transposable element methylation in great tit (Parus major) brain and blood

    Martijn Derks, K.M. Schachtschneider, Ole Madsen, Elio G.W.M. Schijlen, Koen Verhoeven, Kees van Oers

    Background

    Studies on vertebrate DNA methylomes have revealed a regulatory role of tissue specific DNA methylation in relation to gene expression. However, it is not well known how tissue-specific methylation varies between different functional and structural components of genes and genomes. Using whole-genome bisulfite sequencing data we here describe both CpG and non-CpG methylation profiles of whole blood and brain tissue in relation to gene features, CpG-islands (CGIs), transposable elements (TE), and their functional roles in an ecological model species, the great tit (Parus major).


    Results

    We show that hypomethylation at the transcription start site (TSS) is enriched in genes with functional classes that relate directly to processes specific to each tissue type. We find that 6877 (~21 %) of the CGIs are differentially methylated between blood and brain, of which 1186 and 2055 are annotated to promoter and intragenic regions, respectively. We observe that CGI methylation in promoter regions is more conserved between tissues compared to CGI methylation in intra and inter-genic regions. Differentially methylated CGIs in promoter and intragenic regions are overrepresented in genomic loci linked to development, suggesting a distinct role for CGI methylation in regulating expression during development. Additionally, we find significant non-CpG methylation in brain but not in blood with a strong preference for methylation at CpA dinucleotide sites. Finally, CpG hypermethylation of TEs is significantly stronger in brain compared to blood, but does not correlate with TE activity. Surprisingly, TEs showed significant hypomethylation in non-CpG contexts which was negatively correlated with TE expression.


    Conclusion

    The discovery that TSS methylation levels are directly linked to functional classes related to each tissue provides new insights in the regulatory role of DNA-methylation patterns. The dominant sequence motifs for brain non-CpG methylation, similar to those found in mammals, suggests that a conserved non-CpG regulatory mechanism was already present in the amniote ancestor. The negative correlation between brain non-CpG methylation and TE activity (not found for CpG methylation) suggests that non-CpG is the dominant regulatory form of methylation in TE silencing.
    https://doi.org/10.1186/s12864-016-2653-y
  • Molecular Ecology
    2016

    Genetic and epigenetic differences associated with environmental gradients in replicate populations of two salt marsh perennials

    C.M. Foust, Veronica Preite, Aaron W. Schrey, M. Alvarez, Marta H. Robertson, Koen Verhoeven, C.L. Richards
    While traits and trait plasticity are partly genetically based, investigating epigenetic mechanisms may provide more nuanced understanding of the mechanisms underlying response to environment. Using AFLP and methylation-sensitive AFLP, we tested the hypothesis that differentiation to habitats along natural salt marsh environmental gradients occurs at epigenetic, but not genetic loci in two salt marsh perennials. We detected significant genetic and epigenetic structure among populations and among subpopulations, but we found multilocus patterns of differentiation to habitat type only in epigenetic variation for both species. In addition, more epigenetic than genetic loci were correlated with habitat in both species. When we analysed genetic and epigenetic variation simultaneously with partial Mantel, we found no correlation between genetic variation and habitat and a significant correlation between epigenetic variation and habitat in Spartina alterniflora. In Borrichia frutescens, we found significant correlations between epigenetic and/or genetic variation and habitat in four of five populations when populations were analysed individually, but there was no significant correlation between genetic or epigenetic variation and habitat when analysed jointly across the five populations. These analyses suggest that epigenetic mechanisms are involved in the response to salt marsh habitats, but also that the relationships among genetic and epigenetic variation and habitat vary by species. Site-specific conditions may also cloud our ability to detect response in replicate populations with similar environmental gradients. Future studies analysing sequence data and the correlation between genetic variation and DNA methylation will be powerful to identify the contributions of genetic and epigenetic response to environmental gradients.
    https://doi.org/10.1111/mec.13522
  • Preslia
    2016

    Identification of oligoclonal agamospermous microspecies: taxonomic specialists versus microsatellites.

    Jan Kirschner, Carla Oplaat, Koen Verhoeven, V. Zeisek, I. Uhlemann, B. Trávnícek, J. Räsänen, Rutger Wilschut, J. Štěpánek
  • Nature Communications
    2016

    Evolutionary signals of selection on cognition from the great tit genome and methylome

    Veronika Laine, Toni I. Gossmann, K.M. Schachtschneider, Colin J. Garroway, Ole Madsen, Koen Verhoeven, Victor de Jager, H-J. Megens, W.C. Warren, P. Minx, R.P.M.A. Crooijmans, Pádraic Corcoran, Ben C. Sheldon, J. Slate, Kai Zeng, Kees van Oers, Marcel E. Visser, M.A.M. Groenen
    For over 50 years, the great tit (Parus major) has been a model species for research in evolutionary, ecological and behavioural research; in particular, learning and cognition have been intensively studied. Here, to provide further insight into the molecular mechanisms behind these important traits, we de novo assemble a great tit reference genome and whole-genome re-sequence another 29 individuals from across Europe. We show an overrepresentation of genes related to neuronal functions, learning and cognition in regions under positive selection, as well as increased CpG methylation in these regions. In addition, great tit neuronal non-CpG methylation patterns are very similar to those observed in mammals, suggesting a universal role in neuronal epigenetic regulation which can affect learning-, memory- and experience-induced plasticity. The high-quality great tit genome assembly will play an instrumental role in furthering the integration of ecological, evolutionary, behavioural and genomic approaches in this model species.
    https://doi.org/10.1038/ncomms10474
  • Molecular Ecology
    2016

    Natural epigenetic variation contributes to heritable flowering divergence in a widespread asexual dandelion lineage

    Rutger Wilschut, Carla Oplaat, Basten Snoek, Jan Kirschner, Koen Verhoeven
    Epigenetic variation has been proposed to contribute to the success of asexual plants, either as a contributor to phenotypic plasticity or by enabling transient adaptation via selection on transgenerationally stable, but reversible, epialleles. While recent studies in experimental plant populations have shown the potential for epigenetic mechanisms to contribute to adaptive phenotypes, it remains unknown whether heritable variation in ecologically relevant traits is at least partially epigenetically determined in natural populations. Here, we tested the hypothesis that DNA methylation variation contributes to heritable differences in flowering time within a single widespread apomictic clonal lineage of the common dandelion (Taraxacum officinale s. lat.). Apomictic clone members of the same apomictic lineage collected from different field sites showed heritable differences in flowering time, which was correlated with inherited differences in methylation-sensitive AFLP marker profiles. Differences in flowering between apomictic clone members were significantly reduced after in vivo demethylation using the DNA methyltransferase inhibitor zebularine. This synchronization of flowering times suggests that flowering time divergence within an apomictic lineage was mediated by differences in DNA methylation. While the underlying basis of the methylation polymorphism at functional flowering time-affecting loci remains to be demonstrated, our study shows that epigenetic variation contributes to heritable phenotypic divergence in ecologically relevant traits in natural plant populations. This result also suggests that epigenetic mechanisms can facilitate adaptive divergence within genetically uniform asexual lineages.
    https://doi.org/10.1111/mec.13502
  • BMC Genomics
    2016

    Recent and dynamic transposable elements contribute to genomic divergence under asexuality

    Julie Ferreira de Carvalho, Victor de Jager, Thomas Van Gurp, N. Wagenmaker, Koen Verhoeven
    Background:Transposable elements (TEs) are mobile pieces of genetic information with high mutagenic potentialfor the host genome. Transposition is often neutral or deleterious but may also generate potentially adaptivegenetic variation. This additional source of variation could be especially relevant in non-recombining speciesreproducing asexually. However, evidence is lacking to determine the relevance of TEs in plant asexual genomeevolution and their associated effects. Here, we characterize the repetitive fraction of the genome of the commondandelion,Taraxacum officinaleand compare it between five accessions from the same apomictic lineage. The mainobjective of this study is to evaluate the extent of within-lineage divergence attributed to TE content and activity.We examined the repetitive genomic contribution, diversity, transcription and methylation changes to characterizeaccession-specific TEs.Results:Using low-coverage genomic sequencing, we report a highly heterogeneous TE compartment in the triploidapomictT. officinalerepresenting up to 38.6 % of the homoploid genome. The repetitive compartment is dominated byLTR retrotransposon families accompanied by few non-LTR retrotransposons and DNA transposons. Up to half of therepeat clusters are biased towards very high read identity, indicating recent and potentially ongoing activity of these TEfamilies. Interestingly, the five accessions are divided into two main clades based on their TE composition. Clade 2 is moredynamic than clade 1 with higher abundance ofGypsy Chromovirussequences and transposons. Furthermore, a few low-abundant genomic TE clusters exhibit high level of transcription in two of the accessions analysed. Using reducedrepresentation bisulfite sequencing, we detected 18.9 % of loci differentially methylated, of which 25.4 and 40.7 % areannotated as TEs or functional genes, respectively. Additionally, we show clear evidence for accession-specific TE familiesthat are differentially transcribed and differentially methylated within the apomictic lineage, including oneCopia Ale IILTRelement and aPIF-HarbingerDNA transposon.Conclusion:We report here a very young and dynamic repetitivecompartment that enhances divergence within oneasexual lineage ofT. officinale. We speculate that accession-specific TE families that are both transcriptionally andepigenetically variable are more prone to trigger changes inexpression on nearby coding sequences. These findingsemphasize the potential of TE-induced mutations on functional genes during asexual genome evolution.
    https://doi.org/10.1186/s12864-016-3234-9
  • Molecular Ecology
    2016

    Evidence from Pyrosequencing Indicates that Natural Variation in Animal Personality is Associated with DRD4 DNA Methylation

    Eveline Verhulst, A.C. Mateman, M.V. Zwier, Samuel P. Caro, Koen Verhoeven, Kees van Oers
    Personality traits are heritable and respond to natural selection, but are at the same time influenced by the ontogenetic environment. Epigenetic effects, such as DNA methylation, have been proposed as a key mechanism to control personality variation. However, to date little is known about the contribution of epigenetic effects to natural variation in behaviour. Here, we show that great tit (Parus major) lines artificially selected for divergent exploratory behaviour for four generations differ in their DNA methylation levels at the dopamine receptor D4 (DRD4) gene. This D4 receptor is statistically associated with personality traits in both humans and nonhuman animals, including the great tit. Previous work in this songbird failed to detect functional genetic polymorphisms within DRD4 that could account for the gene–trait association. However, our observation supports the idea that DRD4 is functionally involved in exploratory behaviour but that its effects are mediated by DNA methylation. While the exact mechanism underlying the transgenerational consistency of DRD4 methylation remains to be elucidated, this study shows that epigenetic mechanisms are involved in shaping natural variation in personality traits. We outline how this first finding provides a basis for investigating the epigenetic contribution to personality traits in natural systems and its subsequent role for understanding the ecology and evolution of behavioural consistency.
    https://doi.org/10.1111/mec.13519
  • Nature Methods
    2016

    epiGBS: reference-free reduced representation bisulfite sequencing

    Thomas Van Gurp, Niels C. A. M. Wagemaker, Björn Wouters, Philippine Vergeer, Joop N. J. Ouborg, Koen Verhoeven
    We describe epiGBS, a reduced representation bisulfite sequencing method for cost-effective exploration and comparative analysis of DNA methylation and genetic variation in hundreds of samples de novo. This method uses genotyping by sequencing of bisulfite-converted DNA followed by reliable de novo reference construction, mapping, variant calling, and distinction of single-nucleotide polymorphisms (SNPs) versus methylation variation (software is available at https://github.com/thomasvangurp/epiGBS). The output can be loaded directly into a genome browser for visualization and into RnBeads for analysis of differential methylation.

    https://doi.org/10.1038/nmeth.3763
  • Ecology and Evolution
    2015

    Adaptive plasticity and epigenetic variation in response to warming in an Alpine plant

    Adrienne B. Nicotra, Deborah L. Segal, Gemma L. Hoyle, Aaron W. Schrey, Koen Verhoeven, Christina L. Richards
    https://doi.org/10.1002/ece3.1329
  • Molecular Ecology
    2015

    The epigenetic footprint of poleward range-expanding plants in apomictic dandelions

    Veronica Preite, Basten Snoek, Carla Oplaat, Arjen Biere, Wim H. van der Putten, Koen Verhoeven
    Epigenetic modifications, such as DNA methylation variation, can generate heritable phenotypic variation independent of the underlying genetic code. However, epigenetic variation in natural plant populations is poorly documented and little understood. Here, we test if northward range expansion of obligate apomicts of the common dandelion (Taraxacum officinale) is associated with DNA methylation variation. We characterized and compared patterns of genetic and DNA-methylation variation in greenhouse-reared offspring of T. officinale that were collected along a latitudinal transect of northward range expansion in Europe. Genetic AFLP and epigenetic MS-AFLP markers revealed high levels of local diversity and modest but significant heritable differentiation between sampling locations and between the Southern, Central and Northern regions of the transect. Patterns of genetic and epigenetic variation were significantly correlated, reflecting the genetic control over epigenetic variation and/or the accumulation of lineage-specific spontaneous epimutations, which may be selectively neutral. In addition, we identified a small component of DNA methylation differentiation along the transect that is independent of genetic variation. This epigenetic differentiation might reflect environment-specific induction or, in case the DNA methylation variation affects relevant traits and fitness, selection of heritable DNA methylation variants. Such generated epigenetic variants might contribute to the adaptive capacity of individual asexual lineages under changing environments. Our results highlight the potential of heritable DNA methylation variation to contribute to population differentiation along ecological gradients. Further studies are needed using higher-resolution methods to understand the functional significance of such natural occurring epigenetic differentiation.
    https://doi.org/10.1111/mec.13329
  • Journal of Ecology
    2015

    Range expansion in asexual dandelions: selection for general-purpose genotypes?

    Carla Oplaat, Koen Verhoeven

    [KEYWORDS: Apomixis geographic parthenogenesis jack-of-all-trades strategy master-of-some strategy phenotypic plasticity Taraxacum officinale (common dandelion)] Phenotypic plasticity and broad ecological tolerance are hypothesized as important traits in the range expansion of asexual species, because individual asexual lineages have to face spatial and temporal environmental variation with limited opportunity for genetic adaptation. The hypothesis that asexual lineages are general-purpose genotypes (GPG) has been previously tested, with mixed results, in species that have both sexual and asexual variants. Such comparisons can be confounded with intra-specific ploidy level differences that are often observed between the two reproductive types. Avoiding the confounding effects of ploidy differences, we test whether northward range expansion selects for a GPG strategy in asexual lineages of the common dandelion (Taraxacum officinale), a species that shows geographic parthenogenesis. We compared the biomass of asexual lineages that were collected along a geographic transect from close to the asexuals’ area of origin (central Europe, where asexuals descend from sexual ancestors in mixed populations) towards their northern distribution edge (Northern Europe, where only asexual lineages occur) in three different experimental environments: optimal, drought and shaded conditions. The geometric mean performance across test environments did not differ significantly between plants from different regions along the transect. However, southern lineages typically showed larger differences in biomass between different test environments, mainly caused by a relatively high performance in the optimal environment. Northern and mid-latitude lineages showed more even performance across the different environments. Synthesis. Our results suggest that phenotypic plasticity is important in the asexual range expansion of Taraxacum officinale and that range shifting in this species is accompanied by a change in phenotypic plasticity strategy from lineages with high ability to increase biomass in optimal growing conditions (master-of-some strategy) to lineages that maintain more constant performance in different environments (GPG or jack-of-all-trades strategy) from core to range edge. This article is protected by copyright. All rights reserved.




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    https://doi.org/10.1111/1365-2745.12347
  • Evolution
    2014

    Epigenetic variation in asexually reproducing organisms

    Koen Verhoeven, Veronica Preite
    The role that epigenetic inheritance can play in adaptation may differ between sexuals and asexuals because (1) the dynamics of adaptation differ under sexual and asexual reproduction and the opportunities offered by epigenetic inheritance may affect these dynamics differently; and (2) in asexual reproduction epigenetic reprogramming mechanisms that are associated with meiosis can be bypassed, which could promote the buildup of epigenetic variation in asexuals. Here, we evaluate current evidence for an epigenetic contribution to adaptation in asexuals. We argue that two aspects of epigenetic variation should have particular relevance for asexuals, namely epigenetics-mediated phenotypic plasticity within and between generations, and heritable variation via stochastic epimutations. An evaluation of epigenetic reprogramming mechanisms suggests that some, but not all, forms of asexual reproduction enhance the likelihood of stable transmission of epigenetic marks across generations compared to sexual reproduction. However, direct tests of these predicted sexual–asexual differences are virtually lacking. Stable transmission of DNA methylation, transcriptomes, and phenotypes from parent to clonal offspring are demonstrated in various asexual species, and clonal genotypes from natural populations show habitat-specific DNA methylation. We discuss how these initial observations can be extended to demonstrate an epigenetic contribution to adaptation.
    https://doi.org/10.1111/evo.12320
  • BMC Evolutionary Biology
    2013

    Geographic parthenogenesis and plant-enemy interactions in the common dandelion

    Background: Many species with sexual and asexual variants show a pattern of geographic parthenogenesis where asexuals have broader and higher-latitude distribution than sexuals. Because sexual reproduction is often considered a costly evolutionary strategy that is advantageous in the face of selection by coevolving pests and pathogens, one possible explanation for geographic parthenogenesis is that populations at higher latitudes are exposed to fewer pests and pathogens. We tested this hypothesis in the common dandelion (Taraxacum officinale), a species with well-established geographic parthenogenesis, by screening prevalence and effects of several specialized pests and pathogens in natural dandelion populations. Results: We did a population survey of 18 dandelion populations along a geographic transect that ranged from the area where sexual and asexual dandelions co-occur northward into the area where only asexuals occur. In addition we used four southern and four northern populations in a 8x8 cross-inoculation greenhouse experiment in which plants were exposed experimentally to each other's natural field soil microbial communities. The cross-inoculation experiment indicated a higher pathogenicity of soil microbial communities from the southern, mostly sexual, populations compared to soil microbial communities from the northern asexual populations. Northern dandelion populations also showed reduced infestation by a specialized seed-eating weevil. A similar trend of reduced rust fungus infection in northern populations was observed but this trend was not statistically significant. Conclusions: The prevalence of pests and pathogens decreased along the south-to-north axis of geographic parthenogenesis. This highlights the potential of biotic interactions in shaping patterns of geographic parthenogenesis.
    https://doi.org/10.1186/1471-2148-13-23
  • PLoS One
    2013

    Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea

    T. Tytgat, Koen Verhoeven, Jeroen Jansen, Ciska Raaijmakers, Tanja Bakx-Schotman, L.M. McIntyre, Wim H. van der Putten, Arjen Biere, Nicole M. van Dam
    Plants respond to herbivore attack by rapidly inducing defenses that are mainly regulated by jasmonic acid (JA). Due to the systemic nature of induced defenses, attack by root herbivores can also result in a shoot response and vice versa, causing interactions between above- and belowground herbivores. However, little is known about the molecular mechanisms underlying these interactions. We investigated whether plants respond differently when roots or shoots are induced. We mimicked herbivore attack by applying JA to the roots or shoots of Brassica oleracea and analyzed molecular and chemical responses in both organs. In shoots, an immediate and massive change in primary and secondary metabolism was observed. In roots, the JA-induced response was less extensive and qualitatively different from that in the shoots. Strikingly, in both roots and shoots we also observed differential responses in primary metabolism, development as well as defense specific traits depending on whether the JA induction had been below- or aboveground. We conclude that the JA response is not only tissue-specific but also dependent on the organ that was induced. Already very early in the JA signaling pathway the differential response was observed. This indicates that both organs have a different JA signaling cascade, and that the signal eliciting systemic responses contains information about the site of induction, thus providing plants with a mechanism to tailor their responses specifically to the organ that is damaged.
    https://doi.org/10.1371/journal.pone.0065502
  • PLoS One
    2013

    Consistent errors in first strand cDNA due to random hexamer mispriming

    Thomas Van Gurp, L.M. McIntyre, Koen Verhoeven
    Priming of random hexamers in cDNA synthesis is known to show sequence bias, but in addition it has been suggested recently that mismatches in random hexamer priming could be a cause of mismatches between the original RNA fragment and observed sequence reads. To explore random hexamer mispriming as a potential source of these errors, we analyzed two independently generated RNA-seq datasets of synthetic ERCC spikes for which the reference is known. First strand cDNA synthesized by random hexamer priming on RNA showed consistent position and nucleotide-specific mismatch errors in the first seven nucleotides. The mismatch errors found in both datasets are consistent in distribution and thermodynamically stable mismatches are more common. This strongly indicates that RNA-DNA mispriming of specific random hexamers causes these errors. Due to their consistency and specificity, mispriming errors can have profound implications for downstream applications if not dealt with properly.
    https://doi.org/10.1371/journal.pone.0085583
  • PLoS One
    2012

    Transgenerational effects of stress exposure on offspring phenotypes in apomictic dandelion

    Koen Verhoeven, Thomas Van Gurp
    Heritable epigenetic modulation of gene expression is a candidate mechanism to explain parental environmental effects on offspring phenotypes, but current evidence for environment-induced epigenetic changes that persist in offspring generations is scarce. In apomictic dandelions, exposure to various stresses was previously shown to heritably alter DNA methylation patterns. In this study we explore whether these induced changes are accompanied by heritable effects on offspring phenotypes. We observed effects of parental jasmonic acid treatment on offspring specific leaf area and on offspring interaction with a generalist herbivore; and of parental nutrient stress on offspring root-shoot biomass ratio, tissue P-content and leaf morphology. Some of the effects appeared to enhance offspring ability to cope with the same stresses that their parents experienced. Effects differed between apomictic genotypes and were not always consistently observed between different experiments, especially in the case of parental nutrient stress. While this context-dependency of the effects remains to be further clarified, the total set of results provides evidence for the existence of transgenerational effects in apomictic dandelions. Zebularine treatment affected the within-generation response to nutrient stress, pointing at a role of DNA methylation in phenotypic plasticity to nutrient environments. This study shows that stress exposure in apomictic dandelions can cause transgenerational phenotypic effects, in addition to previously demonstrated transgenerational DNA methylation effects.
    https://doi.org/10.1371/journal.pone.0038605
  • 2012

    Evolutionary significance of epigenetic variation

    C.L. Richards, Koen Verhoeven, O. Bossdorf
    Several chapters in this volume demonstrate how epigenetic work at the molecular level over the last few decades has revolutionized our understanding of genome function and developmental biology. However, epigenetic processes not only further our understanding of variation and regulation at the genomic and cellular levels, they also challenge our understanding of heritable phenotypic variation at the level of whole organisms and even the process of evolution by natural selection (Jablonka and Lamb 1989, 1995; Danchin et al. 2011). Although many of the epigenetic mechanisms involved in differential gene expression are reset each generation, some epigenetic marks are faithfully transmitted across generations (Jablonka and Raz 2009; Verhoeven et al. 2010a). In addition, we now know that natural variation exists not only at the DNA sequence level but also the epigenetic level (e.g., Vaughn et al. 2007; Herrera and Bazaga 2010). This may be particularly common in plants, and several studies suggest that epigenetic variation alone can cause significant heritable variation in phenotypic traits (e.g., Cubas et al. 1999; Johannes et al. 2009; Scoville et al. 2011). Because of these observations, there is currently increasing interest in understanding the role of epigenetic processes in ecology and evolution (e.g., Richards 2006, 2011; Bossdorf et al. 2008; Johannes et al. 2008; Richards et al. 2010a).
    https://doi.org/10.1007/978-3-7091-1130-7_16
  • Journal of Ecology
    2011

    Comparison of nutrient acquisition in exotic plant species and congeneric natives

    Annelein Meisner, Wietse de Boer, Koen Verhoeven, H.T.S. Boschker, Wim H. van der Putten
    1.The ability of exotic plant species to establish and expand in new areas may be enhanced by a relatively high ability to acquire soil nutrients. To test this hypothesis, we predicted that the capacity for nutrient acquisition would be higher in seedlings of exotic species than in seedlings of native congeners. 2.We selected the five exotic species that had recently increased in abundance in a riverine habitat in the Netherlands and that had a native congener that was common in the same habitat. We grew seedlings of each of these ten species singly in pots of soil from this habitat in a glasshouse. After two months, we measured the final dry mass and N and P content of each plant and components of microbial biomass and nutrient mineralization in the soil. We also measured these soil characteristics in pots that had been left unplanted. 3.Exotic and native congeners did not differ consistently in the uptake of N or P or in effects on components of soil mineralization. Within a genus, values of these measurements were sometimes higher, sometimes lower and sometimes similar to the exotic when compared with the native species. 4.Depending upon the statistical analysis used, biomarker-based biomass of arbuscular mycorrhizal fungi was generally higher in soil planted with exotic than with native species. Most measures of microbial biomass and soil mineralization were higher in pots that had been planted with plants than in pots with no plant. 5.Synthesis. Our results do not suggest that invasive, exotic plant species generally possess greater capacity for nutrient acquisition during the early establishment than native species do.
    https://doi.org/10.1111/j.1365-2745.2011.01858.x
  • Molecular Ecology
    2010

    Changes in genomic methylation patterns during the formation of triploid asexual dandelion lineages

    Koen Verhoeven, P.J. Van Dijk, Arjen Biere
    DNA methylation is an epigenetic mechanism that has the potential to affect plant phenotypes and that is responsive to environmental and genomic stresses such as hybridization and polyploidization. We explored de novo methylation variation that arises during the formation of triploid asexual dandelions from diploid sexual mother plants using methylation-sensitive amplified fragment length polymorphism (MS-AFLP) analysis. In dandelions, triploid apomictic asexuals are produced from diploid sexual mothers that are fertilized by polyploid pollen donors. We asked whether the ploidy level change that accompanies the formation of new asexual lineages triggers methylation changes that contribute to heritable epigenetic variation within novel asexual lineages. Comparison of MS-AFLP and AFLP fragment inheritance in a diploid × triploid cross revealed de novo methylation variation between triploid F1 individuals. Genetically identical offspring of asexual F1 plants showed modest levels of methylation variation, comparable to background levels as observed among sibs in a long-established asexual lineage. Thus, the cross between ploidy levels triggered de novo methylation variation between asexual lineages, whereas it did not seem to contribute directly to variation within new asexual lineages. The observed background level of methylation variation suggests that considerable autonomous methylation variation could build up within asexual lineages under natural conditions.
    https://doi.org/10.1111/j.1365-294X.2009.04460.x
  • New Phytologist
    2010

    Stress-induced DNA methylation changes and their heritability in asexual dandelions

    Koen Verhoeven, Jeroen Jansen, P.J. Van Dijk, Arjen Biere
    • DNA methylation can cause heritable phenotypic modifications in the absence of changes in DNA sequence. Environmental stresses can trigger methylation changes and this may have evolutionary consequences, even in the absence of sequence variation. However, it remains largely unknown to what extent environmentally induced methylation changes are transmitted to offspring, and whether observed methylation variation is truly independent or a downstream consequence of genetic variation between individ • Genetically identical apomictic dandelion (Taraxacum officinale) plants were exposed to different ecological stresses, and apomictic offspring were raised in a common unstressed environment. We used methylation-sensitive amplified fragment length polymorphism markers to screen genome-wide methylation alterations triggered by stress treatments and to assess the heritability of induced changes. • Various stresses, most notably chemical induction of herbivore and pathogen defenses, triggered considerable methylation variation throughout the genome. Many modifications were faithfully transmitted to offspring. Stresses caused some epigenetic divergence between treatment and controls, but also increased epigenetic variation among plants within treatments. • These results show the following. First, stress-induced methylation changes are common and are mostly heritable. Second, sequence-independent, autonomous methylation variation is readily generated. This highlights the potential of epigenetic inheritance to play an independent role in evolutionary processes, which is superimposed on the system of genetic inheritance.
    https://doi.org/10.1111/j.1469-8137.2009.03121.x
  • Biological Invasions
    2010

    Ecological fits, mis-fits and lotteries involving insect herbivores on the invasive plant, Bunias orientalis

    Jeff A. Harvey, Arjen Biere, Taiadjana Fortuna, Louise E.M. Vet, T. Engelkes, Elly Morrien, R. Gols, Koen Verhoeven, H. Vogel, Mirka Macel, H. Heidel-Fischer, K. Schramm, Wim H. van der Putten
    Exotic plants bring with them traits that evolved elsewhere into their new ranges. These traits may make them unattractive or even toxic to native herbivores, or vice versa. Here, interactions between two species of specialist (Pieris rapae and P. brassicae) and two species of generalist (Spodoptera exigua and Mamestra brassicae) insect herbivores were examined on two native crucifer species in the Netherlands, Brassica nigra and Sinapis arvensis, and an exotic, Bunias orientalis. Bu. orientalis originates in eastern Europe and western Asia but is now an invasive pest in many countries in central Europe. P. rapae, P. brassicae and S. exigua performed very poorly on Bu. orientalis, with close to 100% of larvae failing to pupate, whereas survival was much higher on the native plants. In choice experiments, the pierid butterflies preferred to oviposit on the native plants. Alternatively, M. brassicae developed very poorly on the native plants but thrived on Bu. orientalis. Further assays with a German Bu. orientalis population also showed that several specialist and generalist herbivores performed very poorly on this plant, with the exception of Spodoptera littoralis and M. brassicae. Bu. orientalis produced higher levels of secondary plant compounds (glucosinolates) than B. nigra but not S. arvensis but these do not appear to be important factors for herbivore development. Our results suggest that Bu. orientalis is a potential demographic ‘trap’ for some herbivores, such as pierid butterflies. However, through the effects of an evolutionary ‘lottery’, M. brassicae has found its way through the plant’s chemical ‘minefield’.
    https://doi.org/10.1007/s10530-010-9696-9
  • PLoS One
    2010

    Epistasis: obstacle or advantage for mapping complex traits?

    Koen Verhoeven, G. Casella, L.M. McIntyre
    Identification of genetic loci in complex traits has focused largely on one-dimensional genome scans to search for associations between single markers and the phenotype. There is mounting evidence that locus interactions, or epistasis, are a crucial component of the genetic architecture of biologically relevant traits. However, epistasis is often viewed as a nuisance factor that reduces power for locus detection. Counter to expectations, recent work shows that fitting full models, instead of testing marker main effect and interaction components separately, in exhaustive multi-locus genome scans can have higher power to detect loci when epistasis is present than single-locus scans, and improvement that comes despite a much larger multiple testing alpha-adjustment in such searches. We demonstrate, both theoretically and via simulation, that the expected power to detect loci when fitting full models is often larger when these loci act epistatically than when they act additively. Additionally, we show that the power for single locus detection may be improved in cases of epistasis compared to the additive model. Our exploration of a two step model selection procedure shows that identifying the true model is difficult. However, this difficulty is certainly not exacerbated by the presence of epistasis, on the contrary, in some cases the presence of epistasis can aid in model selection. The impact of allele frequencies on both power and model selection is dramatic.
    https://doi.org/10.1371/journal.pone.0012264
  • Journal of Ecology
    2010

    Plant-soil feedback: Experimental approaches, statistical analyses and biological interpretations

    Pella Brinkman, Wim H. van der Putten, E.J. Bakker, Koen Verhoeven
    1. Feedback between plants and soil organisms has become widely recognized as a driving force of community composition and ecosystem functioning. However, there is little uniformity in quantification and analysis of plant soil feedback effects. Meta-analysis suggested that the various experimental methods tend to result in different feedback values. Yet, a direct comparison of the different experimental approaches and their statistical analyses is lacking. 2. We used currently applied methods to calculate plant soil feedback value ranges and compared their statistical analyses to those based on actual biomass data. Then, we re-analysed a case study to compare plant soil feedback values obtained under the same environmental conditions, but using different experimental approaches: soil sterilization, addition of soil inoculum, and soil conditioning by own vs. foreign plant species. 3. Different measures to calculate plant soil feedback values were more variable in positive than in negative feedback values. Analysis of calculated feedback values that are based on treatment averages can lead to a serious inflation of type I errors. 4. In our case study, both the strength and the direction of the feedback effects depended on the experimental approach that was chosen, leading to diverging conclusions on whether feedback to a certain soil was positive or negative. Soil sterilization and addition of soil organisms yielded larger feedback than comparison of own and foreign soil. 5. Synthesis. The ecological interpretation of plant soil feedback effects strongly depends on the experimental procedure. When the research question focuses on the strength and the sign of plant soil feedback, soil sterilization (presumed that the side effect of increased nutrient availability can be controlled) or addition of soil inoculum is to be preferred. When the research question concerns the specificity of soil feedback effects, plant performance can be better compared between own and foreign soil. We recommend that when using calculated feedback values, the original data need to be presented as well in order to trace the cause of the effect.
    https://doi.org/10.1111/j.1365-2745.2010.01695.x
  • Ecology Letters
    2009

    Plant invaders and their novel natural enemies: who is naive?

    Introduced exotic species encounter a wide range of non-coevolved enemies and competitors in their new range. Evolutionary novelty is a key aspect of these interactions, but who benefits from novelty: the exotic species or their new antagonists? Paradoxically, the novelty argument has been used to explain both the release from and the suppression by natural enemies. We argue that this paradox can be solved by considering underlying interaction mechanisms. Using plant defenses as a model, we argue that mismatches between plant and enemy interaction traits can enhance plant invasiveness in the case of toxin-based defenses, whereas invasiveness is counteracted by mismatches in recognition-based defenses and selective foraging of generalist herbivores on plants with rare toxins. We propose that a mechanistic understanding of ecological mismatches can help to explain and predict when evolutionary novelty will enhance or suppress exotic plant invasiveness. This knowledge may also enhance our understanding of plant abundance following range expansion, or during species replacements along successional stages.
    https://doi.org/10.1111/j.1461-0248.2008.01248.x
  • Nature
    2008

    Successful range-expanding plants experience less above-ground and below-ground enemy impact

    Many species are currently moving to higher latitudes and altitudes1, 2, 3. However, little is known about the factors that influence the future performance of range-expanding species in their new habitats. Here we show that range-expanding plant species from a riverine area were better defended against shoot and root enemies than were related native plant species growing in the same area. We grew fifteen plant species with and without non-coevolved polyphagous locusts and cosmopolitan, polyphagous aphids. Contrary to our expectations, the locusts performed more poorly on the range-expanding plant species than on the congeneric native plant species, whereas the aphids showed no difference. The shoot herbivores reduced the biomass of the native plants more than they did that of the congeneric range expanders. Also, the range-expanding plants developed fewer pathogenic effects4, 5 in their root-zone soil than did the related native species. Current predictions forecast biodiversity loss due to limitations in the ability of species to adjust to climate warming conditions in their range6, 7, 8. Our results strongly suggest that the plants that shift ranges towards higher latitudes and altitudes may include potential invaders, as the successful range expanders may experience less control by above-ground or below-ground enemies than the natives.
    https://doi.org/10.1038/nature07474
  • Molecular Ecology
    2008

    Habitat-specific natural selection at a flowering time QTL is a main driver of local adaptation in two wild barley populations

    Koen Verhoeven, H. Poorter, E. Nevo, Arjen Biere
    Understanding the genetic basis of local adaptation requires insight in the fitness effects of individual loci under natural field conditions. While rapid progress is made in the search for genes that control differences between plant populations, it is typically unknown whether the genes under study are in fact key targets of habitat-specific natural selection. Using a quantitative trait loci (QTL) approach, we show that a QTL associated with flowering-time variation between two locally adapted wild barley populations is an important determinant of fitness in one, but not in the other population's native habitat. The QTL mapped to the same position as a habitat-specific QTL for field fitness that affected plant reproductive output in only one of the parental habitats, indicating that the genomic region is under differential selection between the native habitats. Consistent with the QTL results, phenotypic selection of flowering time differed between the two environments, whereas other traits (growth rate and seed weight) were under selection but experienced no habitat-specific differential selection. This implies the flowering-time QTL as a driver of adaptive population divergence. Our results from phenotypic selection and QTL analysis are consistent with local adaptation without genetic trade-offs in performance across environments, i.e. without alleles or traits having opposing fitness effects in contrasting environments.
    https://doi.org/10.1111/j.1365-294X.2008.03847.x
  • Molecular Biology and Evolution
    03-2005

    Genomic haplotype blocks may not accurately reflect spatial variation in historic recombination intensity

    Koen Verhoeven, Katy L Simonsen

    Recently, genomic data have revealed a "block-like" structure of haplotype diversity on human chromosomes. This structure is anticipated to facilitate gene mapping studies, because strong associations among loci within a block may allow haplotype variation to be tagged with a limited number of markers. But its usefulness to mapping efforts depends on the consistency of the block structure within and among populations, which in turn depends on how the block structure arises. Recombination hot spots are generally thought to underlie the block structure, but haplotype blocks can also develop stochastically under random recombination, in which case the block structure will show limited consistency among populations. Using coalescent models, which we upscaled to simulate the evolution of haplotypes with many markers at fixed distances, we show that the relationship between block boundaries and historic recombination intensity may be surprisingly weak. The majority of historic recombinations do not leave a footprint in present-day linkage disequilibrium patterns, and the block structure is sensitive to factors that affect the timing of recombination relative to marker mutation events in the genealogy, such as marker frequency bias and historic population size changes. Our results give insight into the potential of stochastic events to affect haplotype block structure, which can limit the usefulness of the block structure to mapping studies.

    https://doi.org/10.1093/molbev/msi058
  • Oecologia
    2005

    A genetic analysis of relative growth rate and underlying components in Hordeum spontaneum

    H. Poorter, C.P.E. Van Rijn, T.K. Vanhala, Koen Verhoeven, Y.E.M. de Jong, A.J.M. Stams, H. Lambers
    Species from productive and unproductive habitats differ inherently in their relative growth rate (RGR) and a wide range of correlated quantitative traits. We investigated the genetic basis of this trait complex, and specifically assessed whether it is under the control of just one or a few genes that can act as master switches by simultaneously affecting a range of traits in the complex. To address this problem, we crossed two Hordeum spontaneum lines originating from two habitats that differ in productivity. The F3 offspring, in which parental alleles are present in different combinations due to recombination and segregation, was analysed for RGR and its underlying components (leaf area ratio, unit leaf rate, photosynthesis, respiration), as well as a number of other physiological and morphological parameters. For this intra-specific comparison, we found a complex of positively and negatively correlated traits, which was quite similar to what is generally observed across species. A quantitative trait loci (QTL) analysis showed three major and one minor QTL for RGR. Most other variables of the growth-trait complex showed fewer QTLs that were typically scattered over various locations on the genome. Thus, at least in H. spontaneum, we found no evidence for regulation of the trait complex by one or two master switches. [KEYWORDS: Specific leaf area; Unit leaf rate; Quantitative trait loci; Trait complex; Photosynthesis]
    https://doi.org/10.1007/s00442-004-1705-1
  • Oikos
    2005

    Implementing false discovery rate control: increasing your power

    Koen Verhoeven, Katy L Simonsen, L.M. McIntyre
    Popular procedures to control the chance of making type I errors when multiple statistical tests are performed come at a high cost: a reduction in power. As the number of tests increases, power for an individual test may become unacceptably low. This is a consequence of minimizing the chance of making even a single type I error, which is the aim of, for instance, the Bonferroni and sequential Bonferroni procedures. An alternative approach, control of the false discovery rate (FDR), has recently been advocated for ecological studies. This approach aims at controlling the proportion of significant results that are in fact type I errors. Keeping the proportion of type I errors low among all significant results is a sensible, powerful, and easy-to-interpret way of addressing the multiple testing issue. To encourage practical use of the approach, in this note we illustrate how the proposed procedure works, we compare it to more traditional methods that control the familywise error rate, and we discuss some recent useful developments in FDR control.
    https://doi.org/10.1111/j.0030-1299.2005.13727.x
  • Journal of Evolutionary Biology
    2004

    Differential selection of growth rate-related traits in wild barley, Hordeum spontaneum, in contrasting greenhouse nutrient environments

    Koen Verhoeven, Arjen Biere, E. Nevo, J.M.M. Van Damme
    Across-species comparisons show that inherent variation in relative growth rate (RGR) and its underlying traits are correlated with habitat productivity. In this study, we test the hypothesis that growth rate-related traits confer differential selective effects in contrasting nutrient environments. We specifically test whether high RGR is targeted by selection in nutrient-rich environments whereas low values of traits that underlie RGR [specific leaf area (SLA), leaf mass fraction and leaf area ratio (LAR)] confer a direct fitness advantage in nutrient-poor environments, resulting in selection of low RGR as a correlated response. We measured RGR, its underlying component traits, and estimated fitness in a range of wild barley (Hordeum spontaneum) accessions grown under high and low nutrient conditions. Selection on component traits differed between the two environments, while total selection of RGR was not significant. Using multiple regression and path analysis to estimate direct fitness effects, a selective advantage of high LAR and SLA was demonstrated only under nutrient-rich conditions. While supporting the view that observed associations between habitat richness and some RGR-component traits reflect adaptation to differing nutrient regimes, our data suggest that direct selection targets component traits rather than RGR itself. [KEYWORDS: fitness Hordeum indirect selection leaf area ratio leaf mass fraction path analysis phenotypic selection relative growth rate specific leaf area unit leaf rate]
    https://doi.org/10.1046/j.1420-9101.2003.00636.x
  • Evolution
    2004

    The genetic basis of adaptive population differentiation: a quantitative trait locus analysis of fitness traits in two wild barley populations from contrasting habitats

    Koen Verhoeven, T.K. Vanhala, Arjen Biere, E. Nevo, J.M.M. Van Damme
    We used a quantitative trait locus (QTL) approach to study the genetic basis of population differentiation in wild barley, Hordeum spontaneum. Several ecotypes are recognized in this model species, and population genetic studies and reciprocal transplant experiments have indicated the role of local adaptation in shaping population differences. We derived a mapping population from a cross between a coastal Mediterranean population and a steppe inland population from Israel and assessed F3 progeny fitness in the natural growing environments of the two parental populations. Dilution of the local gene pool, estimated as the proportion of native alleles at 96 marker loci in the recombinant lines, negatively affected fitness traits at both sites. QTLs for fitness traits tended to differ in the magnitude but not in the direction of their effects across sites, with beneficial alleles generally conferring a greater fitness advantage at their native site. Several QTLs showed fitness effects at one site only, but no opposite selection on individual QTLs was observed across the sites. In a common-garden experiment, we explored the hypothesis that the two populations have adapted to divergent nutrient availabilities. In the different nutrient environments of this experiment, but not under field conditions, fitness of the F3 progeny lines increased with the number of heterozygous marker loci. Comparison of QTL-effects that underlie genotype × nutrient interaction in the common-garden experiment and genotype × site interaction in the field suggested that population differentiation at the field sites may have been driven by divergent nutrient availabilities to a limited extent. Also in this experiment no QTLs were observed with opposite fitness effects in contrasting environments. Our data are consistent with the view that adaptive differentiation can be based on selection on multiple traits changing gradually along ecological gradients. This can occur without QTLs showing opposite fitness effects in the different environments, that is, in the absence of genetic trade-offs in performance between environments. [KEYWORDS: Antagonistic pleiotropy; fitness quantitative trait loci; genetic trade-off; heterosis; Hordeum spontaneum; local adaptation]
    https://doi.org/10.1554/03-033
  • Journal of Evolutionary Biology
    2004

    Phenotypic selection and regulation of reproduction in different environments in wild barley

    S. Volis, Koen Verhoeven, S. Mendlinger, D. Ward
    Plasticity of the phenotypic architecture of wild barley, Hordeum spontaneum, was studied in response to water and nutrient stress. Direct and indirect selection on several vegetative and reproductive traits was estimated and path analysis used to reveal how regulating pathways via maternal investment differed between environments. Vegetative traits displayed differential regulating effect on fitness across experimental environments: (1) increase in size was selected for under optimal conditions and under water stress, but not under nutrient stress; (2) allocation to root biomass was selected for under optimal conditions, but it had no effect under nutrient stress and was strongly selected against when water was limiting; (3) delayed onset of reproduction was selected under nutrient limitation whereas earlier onset was selected under water stress. The regulating effect of reproductive traits on final reproductive output also differed across treatments, operating either at the 'early' stage of plant development through varying the number of initiated spikelets per spike (no stress and water stress treatment) or at the 'late' developmental stage adjusting the fertile spikelet weight (no stress and nutrient stress treatment). Reproductive output was regulated via seed abortion under no stress and water stress treatments. Although the underlying mechanism of the regulation through abortion has yet to be discovered, the specific mechanism of abortion under water stress appears to be different from that under optimal conditions. Our results demonstrate that not only is the character architecture in wild barley plastic and sensitive to changing availability of water and nutrients, but the regulating mechanism of maternal investment is also environmentally sensitive [KEYWORDS: natural selection; path analysis; phenotypic; integration; seed; abortion; seed; size-number; trade-off trait; correlations]
    https://doi.org/10.1111/j.1420-9101.2004.00738.x
  • International Journal of Plant Sciences
    2004

    Can a genetic correlation with seed mass constrain adaptive evolution of seedling desiccation tolerance in wild barley?

    Koen Verhoeven, Arjen Biere, E. Nevo, J.M.M. Van Damme
    Very young seedlings of wild barley Hordeum spontaneum have the ability to survive extended periods of severe drought. This desiccation tolerance is considered an adaptation to the rain-limited and unpredictable habitats that the species occupies. Genetic variation has been observed for this trait, but the limited evidence to date does not consistently show that genotypes from more xeric populations have better desiccation tolerance. As large seed endosperm volume may buffer the desiccating seedling from drought stress, we explored the hypothesis that tolerance to temporary but severe drought is affected by seed mass. We crossed a big-seeded with a small-seeded H. spontaneum genotype and measured seed mass and seedling survival rates after 6-ddesiccation in 140 F4 progeny families. A positive correlation was observed between family mean scores of the two traits. At the genetic level, this indicated that at least some genes underlying variation in the two traits overlapped (or show close chromosomal linkage), which is inevitable if seed mass causally affects desiccation tolerance. Quantitative Trait Loci (QTL) analysis, which can identify chromosome regions responsible for trait variation by exploring associations between trait expression and genetic markers dispersed over the genome, did not confirm this hypothesis of shared genetic control. Despite the lack of QTL evidence, the observed genetic association between seed mass and desiccation tolerance indicates that the two traits are not fully independent, implying that selection targeting one trait will cause a correlated response in the other. We discuss this finding in the context of adaptive differentiation of H. spontaneum populations, which is thought to involve selection of increasingly smaller seeds along a gradient of decreasing predictability and amount of annual precipitation. [KEYWORDS: Hordeum spontaneum; adaptation; drought; QTL analysis; correlated selection]
    https://doi.org/10.1086/382800

Projects & collaborations

Projects

  • ECORAMA – Ecology and evolution of species range margins

    Project Present
    This is a collaborative project that is led by John Pannell and Shengman Lyu at the University of Lausanne. The project investigates the genetic, demographic and evolutionary processes that determine species range margins, using Mercurialis annua as a model species. Our contribution to this project is to set up and maintain a field experiment in which experimental plant populations of different admixture histories are monitored for performance at Wageningen, which is at the current distributional range margin of the species.
    ecorama project
  • Botanical records through a social lens

    Project 2023–Present
    This collaborative project is led by Folgert Karsdorp of the KNAW Meertens Institute, and investigates the social biases and cultural aspects of historical botanical records (that is, citizen science avant la lettre). In collaboration with FLORON, our contribution to this project is to implement a case study that explores historical botanical records from the Netherlands to characterize patterns of distribution and abundance of Asteraceae species in cities through time. We aim to let these historical records inform us about which species are winners and which are losers of the urbanization process. This can provide unique information on the plant traits that mediate successful adaptation to urbanization.
    Botanical records through a social lens
  • Plant gene expression plasticity and adaptation to climate change

    Project 2023–2026
    One effect of climate change is that plants are exposed to increasing local variation in weather conditions, including more episodes of heat stress. Should plants evolve to perform better at high temperatures, or should they become more plastic and cope with a broader range of temperatures? This project compares a large panel of duckweed genotypes for genetic differences in thermal plasticity in gene expression. Because duckweeds are the fastest growing plants in the world, we can use experimental evolution approaches to test if more plastic genotypes have a selective advantage when temperature environments become more variable.
    duckweed
  • Linking space to time in ecology: Urban Evolution in Dandelions

    Project 2021–2023
    Urban environments are ever expanding and differ markedly from natural and rural ecosystems. Cities are good test cases for the adaptive capacity of plants and animals in a rapidly changing world.
    dandelion city
  • Intraspecific variation in grass microbiome interaction

    Project 2019–2023
    Through association with beneficial bacteria and fungi, plants can express increased growth via improved nutrient uptake, disease resistance, and abiotic stress tolerance.
    Lolium GWAS
  • Environmental and transgenerational dynamics of DNA methylation in plants with different life histories

    Project 2018–2022
    This project is a component of the EpiDiverse MSCA-ITN European training network. DNA methylation variants can arise spontaneously, they can be under genetic control or they can be induced by environments. In plants, some DNA methylation variants are stable across many generations whereas other variants are very transient. A good understanding of the transgenerational dynamics of DNA methylation variants is essential to understand their impact on heritable traits and their effect on adaptation.
    Kassen
  • Epigenetic contribution to phenotypic plasticity in Populus nigra

    Project 2018–2022
    This project is a component of the EpiDiverse MSCA-ITN European training network. In long-lived sessile organisms such as trees, phenotypic plasticity is an important requirement for successful persistence in changing or variable environments. Epigenetic mechanisms have the potential to mediate long-term plastic responses to environmental change. However, the importance of epigenetic mechanisms such as DNA methylation as regulators of adaptive plasticity is not well known.
    poplar experiment
  • Epigenetics of animal personality: DNA methylation and its influence on exploratory behaviour in great tits

    Project 2018–2022
    Recent studies have shown that early developmental effects and environmental conditions experienced by parents also affect personality traits, even over multiple generations. Yet, the mechanisms underlying such transgenerational regulation remain unknown, while determining them is crucial to understand how development affects heritable traits in evolutionary processes.
    Koolmees_snow_
  • Linking Ecology, Molecular Biology and Bioinformatics in plant epigenetic research

    Project 2017–2022
    Linking Ecology, Molecular Biology and Bioinformatics in plant epigenetic research
    epidiverse logo
  • Developing bioinformatics tools for future metabolomics data analysis

    Project 2017–2018
    Developing bioinformatics tools for future metabolomics data analysis.
    schimmel

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