Population Epigenetics and Epigenomics

Our DNA stores heritable information in the form of a four letter code; A, C, G and T. Textbook genetics tells us that the code can be mutated (e.g. letter A turns into letter G), and that such mutations alter the functions of genes. In plants, it is becoming increasingly clear that heritable alterations in gene function can also be caused by meiotically stable epimutations, which arise independently of DNA changes. A well-known example of an epimutation is the accidental gain or loss of DNA methylation, the chemical modification of a cytosine (the letter C in the DNA code) into 5-methylcytosine.   

We have previously shown that experimentally-induced as well as spontaneously occurring epimutations can be remarkably stable across generations, and can in some cases even contribute to the heritability of important plant traits. Because of these observations, epigenetic modifications - such as DNA methylation - have emerged as potentially important factors in plant evolution, and as possible molecular targets for the improvement of commercial crops.   

The Focus Group Population epigenetics and epigenomics aims to explore the agricultural and evolutionary implications of heritable epimutations in plants. One major aspect of this work is the development of computational methods for the analysis of population-level epigenomic sequencing data. The goal is to find efficient ways to detect ‘epimutatable’ regions in plant genomes, and to characterize these regions in terms of epigenomic patterns of variation both within and across plant species. A second aspect of our work is to infer the sources, stability and phenotypic impact of heritable epimutations either by direct observation of multi-generational data, or indirectly by using inference methods from evolutionary genetics.  

The Focus Group consists of TUM-IAS Rudolf Mößbauer Tenure Track Prof. Frank Johannes (TUM School of Life Sciences Weihenstephan), TUM-IAS Hans Fischer Fellow Prof. Robert J. Schmitz (University of Georgia), postdoctoral researcher Dr. Rashmi Hazarika (TUM School of Life Sciences Weihenstephan) and TUM-IAS funded doctoral candidate Talha Mubeen (TUM School of Life Sciences Weihenstephan).

Publications by the Focus Group

2023

  • Agius, Dolores Rita; Kapazoglou, Aliki; Avramidou, Evangelia; Baranek, Miroslav; Carneros, Elena; Caro, Elena; Castiglione, Stefano; Cicatelli, Angela; Radanovic, Aleksandra; Ebejer, Jean-Paul; Gackowski, Daniel; Guarino, Francesco; Gulyás, Andrea; Hidvégi, Norbert; Hoenicka, Hans; Inácio, Vera; Johannes, Frank; Karalija, Erna; Lieberman-Lazarovich, Michal; Martinelli, Federico; Maury, Stéphane; Mladenov, Velimir; Morais-Cecílio, Leonor; Pecinka, Ales; Tani, Eleni; Testillano, Pilar S.; Todorov, Dimitar; Valledor, Luis; Vassileva, Valya: Exploring the crop epigenome: a comparison of DNA methylation profiling techniques. Frontiers in Plant Science 14, 2023 mehr…
  • Goeldel, Constantin; Johannes, Frank: Stochasticity in gene body methylation. Current Opinion in Plant Biology 75, 2023, 102436 mehr…
  • Kakoulidou, Ioanna; Johannes, Frank: <scp>DNA</scp> methylation remodeling in <scp>F1</scp> hybrids. The Plant Journal, 2023 mehr…
  • Kuhlmann, Markus; Jiang, Hua; Catoni, Marco; Johannes, Frank: Editorial: DNA methylation in plants associated with abiotic stress, volume II. Frontiers in Plant Science 14, 2023 mehr…
  • T. Sellinger, F. Johannes, A. Tellier,: Improved inference of population histories by integrating genomic and epigenomic data. bioRxiv, 2023, mehr…
  • Yao, N.; Zhang, Z.; Yu, L.; Hazarika, R.; Yu, C.; Jang, H.; Smith, L. M.; Ton, J.; Liu, L.; Stachowicz, J. J.; Reusch, T. B. H.; Schmitz, R. J.; Johannes, F.: An evolutionary epigenetic clock in plants. Science 381 (6665), 2023, 1440-1445 mehr…

2022

  • Giansanti, Piero; Samaras, Patroklos; Bian, Yangyang; Meng, Chen; Coluccio, Andrea; Frejno, Martin; Jakubowsky, Hannah; Dobiasch, Sophie; Hazarika, Rashmi R.; Rechenberger, Julia; Calzada-Wack, Julia; Krumm, Johannes; Mueller, Sebastian; Lee, Chien-Yun; Wimberger, Nicole; Lautenbacher, Ludwig; Hassan, Zonera; Chang, Yun-Chien; Falcomatà, Chiara; Bayer, Florian P.; Bärthel, Stefanie; Schmidt, Tobias; Rad, Roland; Combs, Stephanie E.; The, Matthew; Johannes, Frank; Saur, Dieter; de Angelis, Martin Hrabe; Wilhelm, Mathias; Schneider, Günter; Kuster, Bernhard: Mass spectrometry-based draft of the mouse proteome. Nature Methods 19 (7), 2022, 803-811 mehr…
  • Hazarika, Rashmi R.; Serra, Michele; Zhang, Zhilin; Zhang, Yinwen; Schmitz, Robert J.; Johannes, Frank: Molecular properties of epimutation hotspots. Nature Plants 8 (2), 2022, 146-156 mehr…
  • Hüther, Patrick; Hagmann, Jörg; Nunn, Adam; Kakoulidou, Ioanna; Pisupati, Rahul; Langenberger, David; Weigel, Detlef; Johannes, Frank; Schultheiss, Sebastian J.; Becker, Claude: MethylScore, a pipeline for accurate and context-aware identification of differentially methylated regions from population-scale plant whole-genome bisulfite sequencing data. Quantitative Plant Biology 3, 2022 mehr…
  • I. Kakoulidou, R. S. Piecyk, R. C. Meyer, M. Kuhlmann, C. Gutjahr, T. Altmann, F. Johannes: Parental pericentromeric methylation status drives methylome remodelling and heterosis in epigenetic hybrids. bioRxiv, 2022, mehr…
  • Piecyk, Robert S.; Schlegel, Luca; Johannes, Frank: Predicting 3D chromatin interactions from DNA sequence using Deep Learning. Computational and Structural Biotechnology Journal 20, 2022, 3439-3448 mehr…

2021

  • Denkena, Johanna; Johannes, Frank; Colomé-Tatché, Maria: Region-level epimutation rates in Arabidopsis thaliana. Heredity 127 (2), 2021, 190-202 mehr…
  • Johannes, Frank: Epigenomics in trees: decoding the plastic lives of mangroves. New Phytologist 233 (5), 2021, 1971-1973 mehr…
  • Kakoulidou, Ioanna; Avramidou, Evangelia V.; Baránek, Miroslav; Brunel-Muguet, Sophie; Farrona, Sara; Johannes, Frank; Kaiserli, Eirini; Lieberman-Lazarovich, Michal; Martinelli, Federico; Mladenov, Velimir; Testillano, Pilar S.; Vassileva, Valya; Maury, Stéphane: Epigenetics for Crop Improvement in Times of Global Change. Biology 10 (8), 2021, 766 mehr…
  • Symeonidi, Aikaterini; Nicolaou, Anguelos; Johannes, Frank; Christlein, Vincent: Recursive Convolutional Neural Networks for Epigenomics. 2020 25th International Conference on Pattern Recognition (ICPR), IEEE, 2021 mehr…
  • Yao, Nan; Schmitz, Robert J.; Johannes, Frank: Epimutations Define a Fast-Ticking Molecular Clock in Plants. Trends in Genetics 37 (8), 2021, 699-710 mehr…
  • Zhang, Yinwen; Jang, Hosung; Xiao, Rui; Kakoulidou, Ioanna; Piecyk, Robert S.; Johannes, Frank; Schmitz, Robert J.: Heterochromatin is a quantitative trait associated with spontaneous epiallele formation. Nature Communications 12 (1), 2021 mehr…

2020

  • Costa, Maria-Cecilia D.; Johannes, Frank: Epigenetics: Switching Genes On and Off. Frontiers for Young Minds 8, 2020 mehr…
  • Hofmeister, Brigitte T.; Denkena, Johanna; Colomé-Tatché, Maria; Shahryary, Yadollah; Hazarika, Rashmi; Grimwood, Jane; Mamidi, Sujan; Jenkins, Jerry; Grabowski, Paul P.; Sreedasyam, Avinash; Shu, Shengqiang; Barry, Kerrie; Lail, Kathleen; Adam, Catherine; Lipzen, Anna; Sorek, Rotem; Kudrna, Dave; Talag, Jayson; Wing, Rod; Hall, David W.; Jacobsen, Daniel; Tuskan, Gerald A.; Schmutz, Jeremy; Johannes, Frank; Schmitz, Robert J.: A genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa. Genome Biology 21 (1), 2020 mehr…
  • Mergner, Julia; Frejno, Martin; List, Markus; Papacek, Michael; Chen, Xia; Chaudhary, Ajeet; Samaras, Patroklos; Richter, Sandra; Shikata, Hiromasa; Messerer, Maxim; Lang, Daniel; Altmann, Stefan; Cyprys, Philipp; Zolg, Daniel P.; Mathieson, Toby; Bantscheff, Marcus; Hazarika, Rashmi R.; Schmidt, Tobias; Dawid, Corinna; Dunkel, Andreas; Hofmann, Thomas; Sprunck, Stefanie; Falter-Braun, Pascal; Johannes, Frank; Mayer, Klaus F. X.; Jürgens, Gerd; Wilhelm, Mathias; Baumbach, Jan; Grill, Erwin; Schneitz, Kay; Schwechheimer, Claus; Kuster, Bernhard: Mass-spectrometry-based draft of the Arabidopsis proteome. Nature 579 (7799), 2020, 409-414 mehr…
  • Shahryary, Yadollah; Hazarika, Rashmi R.; Johannes, Frank: MethylStar: A fast and robust pre-processing pipeline for bulk or single-cell whole-genome bisulfite sequencing data. BMC Genomics 21 (1), 2020 mehr…
  • Shahryary, Yadollah; Symeonidi, Aikaterini; Hazarika, Rashmi R.; Denkena, Johanna; Mubeen, Talha; Hofmeister, Brigitte; van Gurp, Thomas; Colomé-Tatché, Maria; Verhoeven, Koen; Tuskan, Gerald; Schmitz, Robert J; Johannes, Frank: AlphaBeta: Computational inference of epimutation rates and spectra from high-throughput DNA methylation data in plants. bioRxiv, 2020 mehr…

2019

  • Furci, Leonardo; Jain, Ritushree; Stassen, Joost; Berkowitz, Oliver; Whelan, James; Roquis, David; Baillet, Victoire; Colot, Vincent; Johannes, Frank; Ton, Jurriaan: Identification and characterisation of hypomethylated DNA loci controlling quantitative resistance in Arabidopsis. eLife 8, 2019 mehr…
  • Hofmeister, Brigitte T.; Denkena, Johanna; Colomé-Tatché, Maria; Shahryary, Yadollah; Hazarika, Rashmi; Grimwood, Jane; Mamidi, Sujan; Jenkins, Jerry; Grabowski, Paul P.; Sreedasyam, Avinash; Shu, Shengqiang; Barry, Kerrie; Lail, Kathleen; Adam, Catherine; Lipzen, Anna; Sorek, Rotem; Kudrna, Dave; Talag, Jayson; Wing, Rod; Hall, David W.; Tuskan, Gerald A.; Schmutz, Jeremy; Johannes, Frank; Schmitz, Robert J.: The somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa. bioRxiv, 2019 mehr…
  • Johannes, Frank: DNA methylation makes mutational history. Nature Plants 5 (8), 2019, 772-773 mehr…
  • Lu, Zefu; Marand, Alexandre P.; Ricci, William A.; Ethridge, Christina L.; Zhang, Xiaoyu; Schmitz, Robert J.: The prevalence, evolution and chromatin signatures of plant regulatory elements. Nature Plants 5 (12), 2019, 1250-1259 mehr…
  • Ricci, William A.; Lu, Zefu; Ji, Lexiang; Marand, Alexandre P.; Ethridge, Christina L.; Murphy, Nathalie G.; Noshay, Jaclyn M.; Galli, Mary; Mejía-Guerra, María Katherine; Colomé-Tatché, Maria; Johannes, Frank; Rowley, M. Jordan; Corces, Victor G.; Zhai, Jixian; Scanlon, Michael J.; Buckler, Edward S.; Gallavotti, Andrea; Springer, Nathan M.; Schmitz, Robert J.; Zhang, Xiaoyu: Widespread long-range cis-regulatory elements in the maize genome. Nature Plants 5 (12), 2019, 1237-1249 mehr…
  • Wendte, Jered M; Zhang, Yinwen; Ji, Lexiang; Shi, Xiuling; Hazarika, Rashmi R; Shahryary, Yadollah; Johannes, Frank; Schmitz, Robert J: Epimutations are associated with CHROMOMETHYLASE 3-induced de novo DNA methylation. eLife 8, 2019 mehr…

2018

  • Johannes, Frank; Schmitz, Robert J.: Spontaneous epimutations in plants. New Phytologist 221 (3), 2018, 1253-1259 mehr…
  • Kooke, Rik; Morgado, Lionel; Becker, Frank; van Eekelen, Henriëtte; Hazarika, Rashmi; Zheng, Qunfeng; de Vos, Ric C.H.; Johannes, Frank; Keurentjes, Joost J.B.: Epigenetic mapping of the <i>Arabidopsis</i> metabolome reveals mediators of the epigenotype-phenotype map. Genome Research 29 (1), 2018, 96-106 mehr…
  • Taudt, Aaron; Roquis, David; Vidalis, Amaryllis; Wardenaar, René; Johannes, Frank; Colomé-Tatché, Maria: METHimpute: imputation-guided construction of complete methylomes from WGBS data. BMC Genomics 19 (1), 2018 mehr…

2017

  • L. Morgado, R. C. Jansen, F. Johannes: Learning sequence patterns of AGO-sRNA affinity from high-throughput sequencing libraries to improve in silico functional small RNA detection and classification in plants. bioRxiv, 2017, mehr…
  • Lauss, Kathrin; Wardenaar, René; Oka, Rurika; van Hulten, Marieke H. A.; Guryev, Victor; Keurentjes, Joost J. B.; Stam, Maike; Johannes, Frank: Parental DNA Methylation States Are Associated with Heterosis in Epigenetic Hybrids. Plant Physiology 176 (2), 2017, 1627-1645 mehr…
  • Morgado, Lionel; Johannes, Frank: Computational tools for plant small RNA detection and categorization. Briefings in Bioinformatics, 2017 mehr…
  • Morgado, Lionel; Preite, Veronica; Oplaat, Carla; Anava, Sarit; Ferreira de Carvalho, Julie; Rechavi, Oded; Johannes, Frank; Verhoeven, Koen J.F.: Small RNAs Reflect Grandparental Environments in Apomictic Dandelion. Molecular Biology and Evolution 34 (8), 2017, 2035-2040 mehr…

2016

  • A. Taudt, M. A. Nguyen, M. Heinig, F. Johannes, M. Colomé-Tatché: chromstaR: Tracking combinatorial chromatin state dynamics in space and time. bioRxiv, 2016, mehr…
  • Diao, Wenwen; Mousset, Mathilde; Horsburgh, Gavin J.; Vermeulen, Cornelis J.; Johannes, Frank; van de Zande, Louis; Ritchie, Michael G.; Schmitt, Thomas; Beukeboom, Leo W.: Quantitative Trait Locus Analysis of Mating Behavior and Male Sex Pheromones in Nasonia Wasps. G3&amp;#58; Genes|Genomes|Genetics 6 (6), 2016, 1549-1562 mehr…
  • Taudt, Aaron; Colomé-Tatché, Maria; Johannes, Frank: Genetic sources of population epigenomic variation. Nature Reviews Genetics 17 (6), 2016, 319-332 mehr…
  • Vidalis, Amaryllis; Živković, Daniel; Wardenaar, René; Roquis, David; Tellier, Aurélien; Johannes, Frank: Methylome evolution in plants. Genome Biology 17 (1), 2016 mehr…

2015

  • Colomé-Tatché, Maria; Johannes, Frank: Signatures of Dobzhansky–Muller Incompatibilities in the Genomes of Recombinant Inbred Lines. Genetics 202 (2), 2015, 825-841 mehr…