Mechanisms of long-term, epigenetic stress memory in annual and perennial Brassicaceae species

Principal Investigator: Prof. Dr. Daniel Schubert

While the immediate responses of plants to stress encounter are well studied, little is known how plants obtain a long-term, mitotically stable memory of stress. There is strong evidence that epigenetic mechanisms play a major role in stress memory, but the epigenetic regulators and stress-associated chromatin modifications have largely not been identified. However, one of the major epigenetic systems, the Polycomb-group (PcG) proteins, target and regulate a large set of stress-responsive genes, while the counteracting Trithorax-group (TrxG) proteins have an important role in priming and memory responses.
In addition, it is likely that different species have evolved different mechanisms and capabilities to maintain information about a stress. Particular in perennial plants, which are repeatedly exposed to similar stressors during their lifecycle, persistence of stress memory and heritability of stress-induced chromatin modifications are likely more pronounced than in annual plants.

This project investigates the hypothesis that duration and extent of long-term, epigenetic stress memory is dependent on plant life strategy and life span. The project takes advantage of resources we have developed: first, we have identified a unique set of “perennialised”, long-lived mutants in the annual Arabidopsis thaliana. Second, we have uncovered a stress-inducible histone modification that likely counteracts Pc-G silencing. The modification might therefore be involved in resetting of epigenetic gene regulation and in priming genes for enhanced activation upon a triggering stimulus.

We will exploit these resources to investigate epigenetic gene regulation of short- and long-term memory of (i) a cold experience and (ii) exposure to β-aminobutyric acid. Specifically, we will study the mechanisms which determine for how long these stimuli prime a plant for improved frost tolerance. We will address the following questions: (1) Is cold stress memory more persistent in “perennialised” A. thaliana lines and the natural perennial Arabis alpina compared to short-lived A. thaliana lines? What are the associated transcriptomic and epigenomic changes? (2) Is the age of the plant relevant for the extent of stress memory in A. alpina? (3) How long-lasting is the stress-induced histone modification in A. thaliana and A. alpina? Is it stressor-specific, how is it molecularly controlled and what is its genome-wide occupancy? (4) Does the stress-induced modification associate and possibly prime for additional histone modifications? To elucidate these questions, we will apply a combination of (epi)genetic, biochemical and physiological approaches.

Overall, this project will strongly contribute to uncover the role of epigenetic gene regulation in long-term stress memory, its persistence in plants with different life strategies and the role of stress-inducible histone modifications in stress priming and memory. Thus, this project aims to unravel epigenetic mechanisms of priming and stress memory in dependence of the ecological context of the studied plant species.

References

• Deleris, A., Stroud, H., Bernatavichute, Y., Johnson, E., Klein, G., Schubert, D. and Jacobsen, S.E. 2012. Loss of the DNA methyltransferase MET1 induces H3K9 hypermethylation at PcG target genes, and relocation of H3K27 trimethylation to transposons in Arabidopsis. PLoS Gen. 8: e1003062.
• Kleinmanns, J.A. and Schubert, D. 2014. Polycomb and Trithorax group protein-mediated control of stress responses in plants. Biol. Chem. 395: 1291-1300.
• Lafos, M., Kroll, P., Hohenstatt, M.L., Thorpe, F.L., Clarenz, O. and Schubert, D. 2011. Dynamic regulation of H3K27 trimethylation during Arabidopsis differentiation. PLoS Gen. 7: e1002040.
• Makarevich, G., Leroy, O., Akinci, U., Schubert, D., Clarenz, O., Goodrich, J., Grossniklaus, U. and Köhler, C. 2006. Different Polycomb group complexes regulate common target genes in Arabidopsis. EMBO Rep. 7: 947-952.
• Mueller-Xing,.R., Clarenz, O., Pokorny, L., Goodrich, J. and Schubert, D. 2014. Polycomb-group proteins and FLOWERING LOCUS T maintain commitment to flowering in Arabidopsis thaliana. Plant Cell 26: 2457-2471.
• Mueller-Xing, R., Schubert, D. and Goodrich, J. 2015. Non-inductive conditions expose the cryptic bract of flower phytomeres. Plant Signal. Behav. 10: e1010868.
• Schatlowski, N., Creasey, K., Goodrich, J. and Schubert, D. 2008. Keeping plants in shape: Polycomb-group genes and histone methylation. Semin. Cell. Dev. Biol. 19: 547-553.
• Schatlowski, N., Stahl, Y., Hohenstatt, M. L., Goodrich, J. and Schubert, D. 2010. The CURLY LEAF interacting protein BLISTER controls expression of Polycomb-group target genes and cellular differentiation of Arabidopsis thaliana. Plant Cell 22: 2291-2305.
• Schubert, D., Primavesi, L., Bishopp, A., Roberts, G., Doonan, J., Jenuwein, T. and Goodrich, J. 2006. Silencing by plant Polycomb-group proteins requires dispersed trimethylation of histone H3 at lysine 27. EMBO J. 25: 4638-4649.