Dr. Koen Verhoeven
Senior ResearcherTerrestrial Ecology |
Research themes
Research expertiseEcological genetics and epigenetics Ecology and genetics of biological invasions Plant evolutionary ecology
Page last updated: 20-09-2019
I am an ecological geneticist with a broad interest in plant adaptation. My research uses genetic and genomic tools and applies them in ecologically relevant contexts in order to understand how plant populations respond to changing environments.
One of my research interests is in ecological epigenetics: what role does epigenetic variation play in ecology and microevolution? This research line has been funded in part through a personal VIDI grant from the Dutch Research Council and through an EU H2020 ITN training network which I coordinate (www.epidiverse.eu). Other topics that I work on include genetic and ecological aspects of plant invasions, the evolutionary ecology of asexually reproducing plants, and intraspecific variation in plant-microbiome interactions.
- 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 with Dr Lauren McIntyre, Computational Genomics, Purdue University, Indiana USA
- 1998 - 2003: PhD project, Netherlands Institute of Ecology and Haifa University, Israel. Thesis defended at Utrecht University
- 1996 - 1998: Projects for rainforest conservation in Costa Rica, Bioproca Foundation
- 1995: MSc in Ecology, University of Nijmegen
Visit my lab page for more info on people and projects
1. Ecological epigenetics: exploring the epigenetic contribution to plasticity and adaptation
I coordinate the H2020 Marie Skłodowska-Curie Innovative Training Network EPIDIVERSE. This network includes 15 PhD student projects in 12 research groups from ecology, molecular genetics and bioinformatics in seven countries. Together, these projects address epigenetic variation in three plant species (wild strawberry, black poplar and field pennycress). The aim of EPIDIVERSE is to investigate how epigenetic mechanisms contribute to natural variation, stress responses and adaptation of plants with different life history characteristics. The network is a joint effort to apply high-resolution epigenetic analysis approaches to natural plant systems in ecological contexts. In our group, 2 EPIDIVERSE projects are carried out:
- PhD project Morgane van Antro (2018-2022): Effects of plant life histories on environmental and transgenerational dynamics of DNA methylation
- PhD project Cristian Peña (2018-2022): Epigenetic contribution to phenotypic plasticity in Black Poplar
Heritable epigenetic variation in asexual plant lineages. Asexually reproducing lineages are excellent models for studying the causes and consequences of heritable epigenetic variation, also in natural ecological contexts, that builds up within genetically uniform backgrounds. This research line was established via an NWO-funded VIDI personal research grant (2011-2016). Focus is on analysis of DNA methylation in clonal duckweed (the world’s fastest-growing angiosperm) and apomictic dandelion. Output from this research includes a reduced-representation method for highly multiplexed, reference-free screening of DNA methylation (epiGBS) and a draft dandelion reference genome (with Wageningen University collaborators).
- MSc project Stella Prelovšek (2018): Influence of temperature on epigenetic changes in common duckweed
2. Plant-soil biota interactions: intraspecific variation and role in plant adaptation
Plants engage in biotic interactions with pathogenic as well as to beneficial soil organisms. For instance, through association with beneficial soil microbes plants can express increased growth via improved nutrient uptake, disease resistance, and abiotic stress tolerance. Such microbe-mediated plant traits could be important for ecological adaptation and for crop improvement, but natural or artificial selection can only shape these traits if genetic variation exists for the ability to engage with specific beneficial microbes. In this research we explore genetic variation for, and ecological consequences of, plant interactions with specific soil biota.
- PhD project Paola Rallo (co-PIs Koen Verhoeven and Jan Kammenga, WUR; 2019-2023): Intraspecific variation in grass-microbiome interactions: genetic determinants and ecological relevance of variation in microbiome composition
Prof. Dr. Lauren McIntyre (Department of Molecular Genetics & Microbiology, University of Florida, Gainesville): design and analysis of -omics experiments
Prof. Dr. Nele Horemans (Biosphere Impact Studies, CSK-CEN, Mol, Belgium): epigenetic inheritance in duckweed and epigenetic effects of radiation in dandelion
Prof. Dr. Frank Johannes (Technical University Munich): quantitative epigenetics in Arabidopsis
Prof. Dr. Eric Schranz (Biosystematics, Wageningen University): Dandelion reference genome
Prof. Dr. Kees van Oers (NIOO-KNAW, Animal Ecology): Epigenetic variation in Great Tit
Prof. Dr. Christina Richards (University of South Florida, Tampa): epiGBS and DNA methylation in natural populations
- Paun, O., Verhoeven, K. J. F., & Richards, C. L. (2019). Opportunities and limitations of reduced representation bisulfite sequencing in plant ecological epigenomics. New Phytologist, 221(2), 738-742. https://doi.org/10.1111/nph.15388
- Shi, J., Joshi, J., Tielbörger, K., Verhoeven, K. J. F., & Macel, M. (2018). Costs and benefits of admixture between foreign genotypes and local populations in the field. Ecology and Evolution, 8(7). https://doi.org/10.1002/ece3.3946
- De Bruijn, I., & Verhoeven, K. J. F. (2018). Cross-species interference of gene expression: Comment. Nature Communications, 9, [5019]. https://doi.org/10.1038/s41467-018-07353-0
- Shi, J., Macel, M., Tielbörger, K., & Verhoeven, K. J. F. (2018). Effects of admixture in native and invasive populations of Lythrum salicaria. Biological Invasions, 20(9), 2381-2393. https://doi.org/10.1007/s10530-018-1707-2
- Groot, M. P., Wagemaker, N. CAM., Ouborg, N. J., Verhoeven, K. J. F., & Vergeer, P. (2018). Epigenetic population differentiation in field- and common garden-grown Scabiosa columbaria plants. Ecology and Evolution, 8(6), 3505-3517. https://doi.org/10.1002/ece3.3931
- Preite, V., Oplaat, C., Biere, A., Kirschner, J., van der Putten, W. H., & Verhoeven, K. J. F. (2018). Increased transgenerational epigenetic variation, but not predictable epigenetic variants, after environmental exposure in two apomictic dandelion lineages. Ecology and Evolution, 8(5), 3047-3059. https://doi.org/10.1002/ece3.3871
- Verhoeven, K. J. F., Verbon, E. H., Van Gurp, T. P., Oplaat, C., Ferreira de Carvalho, J. L., Morse, A. M.,... McIntyre, L. M. (2018). Intergenerational environmental effects: Functional signals in offspring transcriptomes and metabolomes after parental jasmonic acid treatment in apomictic dandelion. New Phytologist, 217(2), 871-882. https://doi.org/10.1111/nph.14835
- Kulkarni, P., A. Wilschut, R., J.F. Verhoeven, K., H. van der Putten, W., & Garbeva, P. (2018). LAESI mass spectrometry imaging as a tool to differentiate the root metabolome of native and range-expanding plant species. Planta, 248(December), 1515-1523. https://doi.org/10.1101/322867, https://doi.org/10.1007/s00425-018-2989-4
- Rendina González, A. P., Preite, V., Verhoeven, K. J. F., & Latzel, V. (2018). Transgenerational Effects and Epigenetic Memory in the Clonal Plant Trifolium repens. Frontiers in Plant Science, 9, 1677. https://doi.org/10.3389/fpls.2018.01677
- Corcoran, P., Gossmann, T. I., Barton, H. J., The Great Tit HapMap Consortium, Slate, J., & Zeng, K. (2017). Determinants of the Efficacy of Natural Selection on Coding and Noncoding Variability in Two Passerine Species. Genome Biology and Evolution, 9(11), 2987-3007. https://doi.org/10.1093/gbe/evx213
- Richards, C. L., Alonso, C., Becker, C., Bossdorf, O., Bucher, E., Colomé-Tatché, M.,... Verhoeven, K. J. F. (2017). Ecological plant epigenetics: Evidence from model and non-model species, and the way forward. Ecology Letters, 20(12), 1576-1590. https://doi.org/10.1111/ele.12858
- Macel, M., Dostálek, T., Esch, S., Bucharová, A., van Dam, N. M., Tielbörger, K.,... Münzbergová, Z. (2017). Evolutionary responses to climate change in a range expanding plant. Oecologia, 184(2), 543-554. https://doi.org/10.1007/s00442-017-3864-x
- Morgado, L., Preite, V., Oplaat, C., Anava, S., Ferreira de Carvalho, J. L., Rechavi, O.,... Verhoeven, K. J. F. (2017). Small RNAs reflect grandparental environments in apomictic dandelion: Letter. Molecular Biology and Evolution, [msx150]. https://doi.org/10.1093/molbev/msx150
- Huber, M., Epping, J., Schulze Gronover, C., Fricke, J., Aziz, Z., Brillatz, T.,... Erb, M. (2016). A Latex Metabolite Benefits Plant Fitness under Root Herbivore Attack. PLoS Biology, 14(1), e1002332 EP -. https://doi.org/10.1371/journal.pbio.1002332
- Groot, M., Kooke, R., Knoben, N., Vergeer, P., Keurentjes, J., Ouborg, J., & Verhoeven, K. J. F. (2016). Effects of multi-generational stress exposure and offspring environment on the expression and persistence of transgenerational effects in Arabidopsis thaliana. PLoS One, 11(3), [ e0151566]. https://doi.org/10.1371/journal.pone.0151566
- van Gurp, T. P., Wagemaker, N. CAM., Wouters, B., Vergeer, P., Ouborg, J. NJ., & Verhoeven, K. JF. (2016). epiGBS: reference-free reduced representation bisulfite sequencing: brief communication. Nature Methods, 13(4), 322-324. https://doi.org/10.1038/nmeth.3763
- Verhoeven, K. J. F., vonHoldt, B., & Sork, V. (2016). Epigenetics in ecology and evolution: what we know and what we need to know. Molecular Ecology, 25(8), 1631-1638. https://doi.org/10.1111/mec.13617
- Verhulst, E., Mateman, A. C., Zwier, M. V., Caro, S. P., Verhoeven, K. J. F., & van Oers, K. (2016). Evidence from Pyrosequencing Indicates that Natural Variation in Animal Personality is Associated with DRD4 DNA Methylation. Molecular Ecology, 25(8), 1801-1811. https://doi.org/10.1111/mec.13519
- Laine, V., Gossmann, T. I., Schachtschneider, K. M., Garroway, C. J., Madsen, O., Verhoeven, K. J. F.,... Groenen, M. A. M. (2016). Evolutionary signals of selection on cognition from the great tit genome and methylome. Nature Communications, 7, [10474]. https://doi.org/10.1038/ncomms10474
- Derks, M., Schachtschneider, K. M., Madsen, O., Schijlen, E. GWM., Verhoeven, K. J. F., & van Oers, K. (2016). Gene and transposable element methylation in great tit (Parus major) brain and blood. BMC Genomics, 17, [332]. https://doi.org/10.1186/s12864-016-2653-y
- Foust, C. M., Preite, V., Schrey, A. W., Alvarez, M., Robertson, M. H., Verhoeven, K. J. F., & Richards, C. L. (2016). Genetic and epigenetic differences associated with environmental gradients in replicate populations of two salt marsh perennials. Molecular Ecology, 25(8), 1639-1652. https://doi.org/10.1111/mec.13522
- Ferreira de Carvalho, J. L., Oplaat, C., Pappas, N., Derks, M., de Ridder, D., & Verhoeven, K. J. F. (2016). Heritable gene expression differences between apomictic clone members in Taraxacum officinale: : Insights into early stages of evolutionary divergence in asexual plants. BMC Genomics, 17(1), 1-13. https://doi.org/10.1186/s12864-016-2524-6
- Kirschner, J., Oplaat, C., Verhoeven, K. J. F., Zeisek, V., Uhlemann, I., Trávnícek, B.,... Štěpánek, J. (2016). Identification of oligoclonal agamospermous microspecies: taxonomic specialists versus microsatellites. Preslia, 88, 1-17.
- Wilschut, R. A., Oplaat, C., Snoek, B., Kirschner, J., & Verhoeven, K. J. F. (2016). Natural epigenetic variation contributes to heritable flowering divergence in a widespread asexual dandelion lineage. Molecular Ecology, 25(8), 1759-1768. https://doi.org/10.1111/mec.13502
- Ferreira de Carvalho, J. L., de Jager, V. C. L., Van Gurp, T. P., Wagenmaker, N., & Verhoeven, K. J. F. (2016). Recent and dynamic transposable elements contribute to genomic divergence under asexuality. BMC Genomics, 17, [884]. https://doi.org/10.1186/s12864-016-3234-9
- Nicotra, A. B., Segal, D. L., Hoyle, G. L., Schrey, A. W., Verhoeven, K. J. F., & Richards, C. L. (2015). Adaptive plasticity and epigenetic variation in response to warming in an Alpine plant. Ecology and Evolution, 5(3), 634-647. https://doi.org/10.1002/ece3.1329
- Oplaat, C., & Verhoeven, K. (2015). Range expansion in asexual dandelions: selection for general-purpose genotypes? Journal of Ecology, 103(1), 261-268. https://doi.org/10.1111/1365-2745.12347
- Preite, V., Snoek, L. B., Oplaat, C., Biere, A., Van der Putten, W. H., & Verhoeven, K. J. F. (2015). The epigenetic footprint of poleward range-expanding plants in apomictic dandelions. Molecular Ecology, 24(17), 4406-4418. https://doi.org/10.1111/mec.13329
- Verhoeven, K. J. F., & Preite, V. (2014). Epigenetic variation in asexually reproducing organisms. Evolution, 68(3), 644-655. https://doi.org/10.1111/evo.12320
- Gsell, A. S., De Senerpont Domis, L. N., Verhoeven, K. J. F., Van Donk, E., & Ibelings, B. W. (2013). Chytrid epidemics may increase genetic diversity of a diatom spring-bloom. ISME Journal, 7(10), 2057-2059. https://doi.org/10.1038/ismej.2013.73
- Van Gurp, T. P., McIntyre, L. M., & Verhoeven, K. J. F. (2013). Consistent errors in first strand cDNA due to random hexamer mispriming. PLoS One, 8(12), [e85583]. https://doi.org/10.1371/journal.pone.0085583
- Verhoeven, K. J. F., & Biere, A. (2013). Geographic parthenogenesis and plant-enemy interactions in the common dandelion. BMC Evolutionary Biology, 13, 23. https://doi.org/10.1186/1471-2148-13-23
- Tytgat, T., Verhoeven, K. J. F., Jansen, J. J., Raaijmakers, C. E., Bakx-Schotman, J. M. T., McIntyre, L. M.,... Van Dam, N. M. (2013). Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea. PLoS One, 8(6), [e65502]. https://doi.org/10.1371/journal.pone.0065502
- Richards, C. L., Verhoeven, K. J. F., & Bossdorf, O. (2012). Evolutionary significance of epigenetic variation. In J. F. Wendel, J. Greilhuber, J. Dolezel, & I. J. Leitch [Eds.], Plant Genome Diversity Vol.1: Plant Genomes, their Residents, and their Evolutionary Dynamics (pp. 257-274). Springer. https://doi.org/10.1007/978-3-7091-1130-7_16
- Verhoeven, K. J. F., & Van Gurp, T. P. (2012). Transgenerational effects of stress exposure on offspring phenotypes in apomictic dandelion. PLoS One, 7(6), [e38605]. https://doi.org/10.1371/journal.pone.0038605
- Meisner, A., De Boer, W., Verhoeven, K. J. F., Boschker, H. T. S., & Van der Putten, W. H. (2011). Comparison of nutrient acquisition in exotic plant species and congeneric natives. Journal of Ecology, 99(6), 1308-1315. https://doi.org/10.1111/j.1365-2745.2011.01858.x
- Verhoeven, K. J. F., Macel, M., Wolfe, L. M., & Biere, A. (2011). Population admixture, biological invasions and the balance between local adaptation and inbreeding depression. Proceedings of the Royal Society B-Biological Sciences, 278(1702), 2-8. https://doi.org/10.1098/rspb.2010.1272
- Verhoeven, K. J. F., Van Dijk, P. J., & Biere, A. (2010). Changes in genomic methylation patterns during the formation of triploid asexual dandelion lineages. Molecular Ecology, 19(2), 315-324. https://doi.org/10.1111/j.1365-294X.2009.04460.x
- Harvey, J. A., Biere, A., Fortuna, T., Vet, L. E. M., Engelkes, T., Morriën, W. E.,... Van der Putten, W. H. (2010). Ecological fits, mis-fits and lotteries involving insect herbivores on the invasive plant, Bunias orientalis. Biological Invasions, 12(9), 3045-3059. https://doi.org/10.1007/s10530-010-9696-9
- Verhoeven, K. J. F., Casella, G., & McIntyre, L. M. (2010). Epistasis: obstacle or advantage for mapping complex traits? PLoS One, 5(8), [e12264]. https://doi.org/10.1371/journal.pone.0012264
- Brinkman, E. P., Van der Putten, W. H., Bakker, E. J., & Verhoeven, K. J. F. (2010). Plant-soil feedback: Experimental approaches, statistical analyses and biological interpretations. Journal of Ecology, 98(5), 1063-1073. https://doi.org/10.1111/j.1365-2745.2010.01695.x
- Verhoeven, K. J. F., Jansen, J. J., Van Dijk, P. J., & Biere, A. (2010). Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytologist, 185(4), 1108-1118. https://doi.org/10.1111/j.1469-8137.2009.03121.x
- Richards, C. L., Bossdorf, O., & Verhoeven, K. J. F. (2010). Understanding natural epigenetic variation. New Phytologist, 187(3), 562-564. https://doi.org/10.1111/j.1469-8137.2010.03369.x
- Verhoeven, K. J. F., Biere, A., Harvey, J. A., & Van der Putten, W. H. (2009). Plant invaders and their novel natural enemies: who is naive? Ecology Letters, 12(2), 107-117. https://doi.org/10.1111/j.1461-0248.2008.01248.x
- Verhoeven, K. J. F., Poorter, H., Nevo, E., & Biere, A. (2008). Habitat-specific natural selection at a flowering time QTL is a main driver of local adaptation in two wild barley populations. Molecular Ecology, 17(14), 3416-3424. https://doi.org/10.1111/j.1365-294X.2008.03847.x
- Biere, A., & Verhoeven, K. J. F. (2008). Local adaptation and the consequences of being dislocated from coevolved enemies. New Phytologist, 180(2), 265-268. https://doi.org/10.1111/j.1469-8137.2008.02632.x
- Engelkes, T., Morriën, W. E., Verhoeven, K. J. F., Bezemer, T. M., Biere, A., Harvey, J. A.,... Van der Putten, W. H. (2008). Successful range-expanding plants experience less above-ground and below-ground enemy impact. Nature, 456(7224), 946-948. https://doi.org/10.1038/nature07474
- Verhoeven, K. J. F., Jannink, J-L., & McIntyre, L. M. (2006). Using mating designs to uncover QTL and the genetic architecture of complex traits. Heredity, 96(2), 139-149. https://doi.org/10.1038/sj.hdy.6800763
- Poorter, H., Van Rijn, C. P. E., Vanhala, T. K., Verhoeven, K. J. F., de Jong, Y. E. M., Stams, A. J. M., & Lambers, H. (2005). A genetic analysis of relative growth rate and underlying components in Hordeum spontaneum. Oecologia, 142(3), 360-377. https://doi.org/10.1007/s00442-004-1705-1
- Verhoeven, K. J. F., & Simonsen, K. L. (2005). Genomic haplotype blocks may not accurately reflect spatial variation in historic recombination intensity. Molecular Biology and Evolution, 22(3), 735-40. https://doi.org/10.1093/molbev/msi058
- Verhoeven, K. J. F., Simonsen, K. L., & McIntyre, L. M. (2005). Implementing false discovery rate control: increasing your power. Oikos, 108(3), 643-647. https://doi.org/10.1111/j.0030-1299.2005.13727.x
- Verhoeven, K. J. F., Biere, A., Nevo, E., & Van Damme, J. M. M. (2004). Can a genetic correlation with seed mass constrain adaptive evolution of seedling desiccation tolerance in wild barley? International Journal of Plant Sciences, 165(2), 281-288. https://doi.org/10.1086/382800
- Verhoeven, K. J. F., Biere, A., Nevo, E., & Van Damme, J. M. M. (2004). Differential selection of growth rate-related traits in wild barley, Hordeum spontaneum, in contrasting greenhouse nutrient environments. Journal of Evolutionary Biology, 17(1), 184-196. https://doi.org/10.1046/j.1420-9101.2003.00636.x
- Volis, S., Verhoeven, K. J. F., Mendlinger, S., & Ward, D. (2004). Phenotypic selection and regulation of reproduction in different environments in wild barley. Journal of Evolutionary Biology, 17(5), 1121-1131. https://doi.org/10.1111/j.1420-9101.2004.00738.x
- Verhoeven, K. J. F., Vanhala, T. K., Biere, A., Nevo, E., & Van Damme, J. M. M. (2004). The genetic basis of adaptive population differentiation: a quantitative trait locus analysis of fitness traits in two wild barley populations from contrasting habitats. Evolution, 58(2), 270-283. https://doi.org/10.1554/03-033
- Verhoeven, K. J. F. (2003). A genetic analysis of selectionand adaptation in wild barley = een genetische analyse van selectie en adaptatie in wilde gerst (PhD Thesis). Wageningen: Ponsen & Looyen.
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- Verhoeven, K. J. F. (2012). nieuwe erfelijkheid: niet in je genen maar op je genen. In wetenschappelijke scheurkalender 2012
