AUgmented REsilience After Transmission of Epimutations

Sessile organisms like plants must be prepared to deal with the full range of fluctuations in their environment. We only start to understand how plants regulate gene activities to help them cope with environmental stresses. This involves epigenetic regulation, which serves as a cellular memory. One prominent example of a developmental decision under epigenetic control is the fact that plants can remember for how long they have been exposed to cold in winter to coordinate flowering with spring. Similarly, plants that encountered environmental stress early during development will be more resilient to the same stress later, an adaptation called acclimation or priming. Many aspects of this epigenetic memory are not understood, and we will use the model plant Arabidopsis to study this phenomenon. We will apply heat and salt stress early during development and investigate gene activities and epigenetic changes at subsequent timepoints in leaves, stem cells, gametes and in the offspring. Investigating the very limited number of stem cells, eggs and sperm cells is possible with innovative techniques developed by partners at the Gregor Mendel Institute in Vienna and at the University of Zurich. This will be combined with analysis of genetic and epigenetic responses to heat and salt stress in Arabidopsis plants originating from different locations and adapted to different environments. This is done in collaboration with the partners at the Max Planck Institute of Developmental Biology in Tübingen, providing high quality full genome information of selected Arabidopsis strains from diverse and well-characterized geographic origins. This collaborative experimental set up allows to find out how environmental signals are converted into epigenetic memory and whether and how plant stem cells are processing and passing this information on to floral organs, gametes and eventually the next generation. We will use the results to test the hypothesis whether we can create more stress-resilient plants by directly targeting and modifying the plants epigenome. This will be done in collaboration with partners from the University of Warwick who use novel techniques to modulate the epigenetic memory of plants. In summary, with a series of novel techniques and the complementary expertise of the AUREATE consortium we will gain a deeper understanding of memory effects and their role during stress adaptation in plants. If modulating the epigenetic stress memory can produce more stress-resistance, without the need for genetic engineering, the results will also be informative and relevant for potential applications in crop species.

Epigenetics is the science that describes heritable phenotypic changes independent of alterations of the DNA sequence. Popular science frequently suggests that we should include epigenetics in our way of thinking about evolution, reconsider Lamarckian inheritance, and accept the notion that we -as organisms- are masters of our genes by controlling nutrition and lifestyle. Among biologists, the term is rather used to describe how cells of an organism can acquire very different shapes and functions during development, despite having the same genetic information. Mechanistically, epigenetics studies the organization of the genome within the nucleus because this determines the accessibility and activity of the underlying sequence information. DNA methylation, a chemical modification of one of the DNA bases, is a well-studied epigenetic mark that can be copied during replication and interact with a range of proteins. Interestingly, epigenetic mechanisms play a role in defense against invaders: they can control virus amplification and selfish genetic elements called transposons. Transposon sequences represent large parts of most genomes, and their activity can have detrimental effects on the organism by inserting into host genes or altering their regulation. If this happens in cells that produce egg and sperm cells, such mutations are mostly deleterious for the next generation and beneficial in only very few cases. Therefore, epigenetic control over transposon activity is critical along the germline, the cells that connect one generation with the next. Many aspects and the degree of epigenetic inheritance are still unknown. For example, one crucial element often not understood is how epigenetic changes can enter the germline. In AUREATE, we used an elegant model system to study the epigenetic inheritance of DNA methylation and its possible mechanisms in cells contributing to the germline. In the small annual plant Arabidopsis, it is well established that DNA methylation can or cannot be heritable. Therefore, we designed an experiment to perturb DNA methylation by applying heat stress and using mutant plants defective in the enzymes necessary for catalyzing methylation of DNA. An additional novelty of our approach is that we established the isolation of stem cells from the shoot tip that later form flowers, therefore later egg and sperm cells. We found exciting differences between the stem cells and the surrounding somatic cells and discovered that there are even different types of stem cells - those which are part of the germline and those which are not. Furthermore, we found that transposons try to proliferate in particular stem cells and identified proteins that act in defense in this parasite-host tug-of-war. Current and future findings will increase our understanding of plant development and evolution and the role of genetic and environmental conditions.