Priming the chromatin in response to heat stress in Arabidopsis thaliana

Principal Investigator: Prof. Dr. Isabel Bäurle

Moderate heat stress (HS) primes a plant to subsequently withstand high temperatures that are lethal to a plant in the naïve state. After returning to non-stress temperatures the primed state is maintained over several days, and this memory is genetically separable from the thermopriming itself. While the molecular events that lead to thermopriming are relatively well understood, little is known about the mechanism of thermomemory, i. e. the maintenance of the primed state after HS.

This project addresses the contribution of chromatin regulation to thermomemory in Arabidopsis thaliana. In the past funding period, we have identified thermomemory-related genes based on their sustained induction after a priming HS. We have used a subset of these genes to study chromatin dynamics during the memory phase. To this end, we have compared the chromatin at several memory-related loci in the naïve, primed and triggered states by analysing histone modifications, nucleosome distribution and DNA methylation. We identified a specific histone modification on thermomemory-related genes that increases during the later stages of thermomemory (when active transcription declines). Interestingly, this modification is defective in a thermomemory-deficient mutant. Thus, this modification may act as a mark of recent transcriptional activity and mediate a modified physiological response upon recurring HS. Building on these findings, in the second funding period we aim to determine the functional relevance of this thermomemory mark, and investigate its molecular regulation. Specifically, we will address the following questions: What is the role of the candidate memory mark in the transcriptional and physiological response to a triggering stimulus? How is the candidate memory mark established and maintained at individual genomic loci? Is the acquisition of the mark associated with higher-order chromatin structures? How is this affected in accessions with varying thermomemory? Why do some heat-induced genes show sustained expression through the memory phase and others do not? We will investigate these questions using an array of molecular and genetic approaches such as chromatin immunoprecipitation, gene expression analyses, reverse genetics, mutant and promoter analyses.

In summary, this project will elucidate the role of chromatin structure during thermomemory and provide insights into its regulation.

References

• Bäurle, I. and Dean, C. 2008. Differential interactions of the autonomous pathway RRM proteins and chromatin regulators in the silencing of Arabidopsis targets. PLoS ONE 3: e2733-2741.
• Bäurle, I. and Laux, T. 2005. Regulation of WUSCHEL transcription in the stem cell niche of the Arabidopsis shoot meristem. Plant Cell 17: 2271-2280.
• Bäurle, I., Smith, L., Baulcombe, D. and Dean, C. 2007. Widespread role for the flowering time regulators FCA and FPA in RNA-mediated chromatin silencing. Science 318: 109-112.
• Hilker, M., Schwachtje, J., Baier, M., Balazadeh, S., Bäurle, I., Geiselhardt, S., Hincha, D.K., Kunze, R., Mueller-Roeber, B., Rillig, M.C., Rolff, J., Romeis, T., Schmülling, T., Steppuhn, A., van Dongen, J., Withcomb, S.J., Wurst, S., Zuther, E. and Kopka, J. 2015. Priming and memory of stress responses in organisms lacking a nervous system. Biol. Rev. doi: 10.1111/brv.12215.
• Kabelitz, T., Kappel, C., Henneberger, K., Benke, E., Nöh, C. and Bäurle, I. 2014. eQTL mapping of transposon silencing reveals a position-dependent stable escape from epigenetic silencing and transposition of AtMu1 in the Arabidopsis lineage. Plant Cell 26: 3261-3271.
• Lämke, J., Brzezinka, K., Altmann, S. and Bäurle, I. A hit-and-run HSF governs sustained histone methylation and transcriptional memory after heat stress. EMBO J., in press, accepted Nov. 2015.
• Liu, F., Quesada, V., Crevillen, P., Bäurle, I., Swiezewski, S. and Dean, C. 2007. The Arabidopsis RNA binding protein FCA requires a Lysine Specific Demethylase 1 homologue to effect FLC down-regulation. Mol. Cell 28: 398-407.
• Stief, A., Altmann, S., Hoffmann, K., Pant, B.D., Scheible, W.R. and Bäurle, I. 2014. Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant Cell 26: 1792-1807.
• Stief, A., Brzezinka, K., Lämke, J. and Bäurle, I. 2014. Epigenetic responses to heat stress at different time scales and the involvement of small RNAs. Plant Signal. Behav. 9: e970430.