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Project A6

The role of heat shock proteins and autophagy for thermomemory

Principal Investigators: Dr. Salma Balazadeh

Acquired thermotolerance (thermopriming) is an increased resistance of cells, tissues and organisms to elevated temperature following a prior exposure to heat. Maintenance of acquired thermotolerance (thermomemory) is associated with the synthesis of specialised stress proteins including heat shock proteins (HSPs) involved in cellular protection and accelerated tissue repair.

During phase I, we showed that the small chloroplast localised heat shock protein HSP21 plays a crucial role for long-term thermomemory in Arabidopsis thaliana. Furthermore, we provided evidence that differences in the accumulation of HSP21 protein in Col-0 (an accession with a weak thermomemory) and N13 (a strong thermomemory accession) strongly contributes to their differential thermomemory performance. We identified FtsH6, a plastid localised metalloprotease, as a protease involved in the initial degradation of HSP21 during the memory phase in Col-0. In N13, FtsH6 harbours a polymorphism within its coding sequence, resulting in a truncated and non-functional protein allowing accumulation of high levels of HSP21 during the memory phase leading to improved thermomemory maintenance. Furthermore, we showed that in addition to FtsH6, autophagy contributes to the degradation of HSP21 at later stages of the thermomemory phase. Transcript levels of several autophagy (ATG) genes are induced upon thermopriming and remain high during the memory phase. We found that autophagy mutants (atg5 and atg18a) have a better thermomemory than wild-type controls.
Based on our findings in phase I, we hypothesise that I) compartment localised sHSPs and II) the autophagy pathway play a role in thermopriming and thermomemory.

The objective of our project in phase II of the CRC 973 is to study the role of the mitochondrial heat shock proteins HSP23.5 and HSP23.6, whose expression at the transcript level during the thermomemory phase parallels that of HSP21, for their role in thermomemory. To this end, we will generate transgenic lines with enhanced or suppressed expression of these genes and characterise their thermomemory behaviour. Additionally, we aim to assess their chaperone activity and identify their target proteins upon a priming treatment. We also aim to identify their upstream transcriptional regulators, assuming those to be early regulators of priming and memory.

With respect to the control of thermomemory by autophagy we propose to further study the involvement of ATG genes in the process and monitor autophagosome formation during the memory phase in wild-type plants and atg mutants. Additionally, we will analyse the role of autophagy for the protection against the accumulation of aggregated proteins. To this respect we will identify the targets of ATG proteins during thermomemory. To unravel the transcriptional control of thermomemory-relevant ATG genes we will identify upstream transcriptional factors controlling their expression after thermopriming. Additionally, we propose to study the role of autophagy for the degradation of HSP21.

To summarise, this research provides new insight into the role of heat shock proteins and autophagy for thermomemory.


  • Allu, A.D., Soja, A.M., Wu, A., Szymanski, J. and Balazadeh, S. 2014. Salt stress and senescence: Identification of crosstalk regulatory components. J. Exp. Bot. 65: 3993-4008.
  • Balazadeh, S., Jaspert, N., Arif, M., Mueller-Roeber, B. and Maurino, VG. 2012. Expression of ROS-responsive genes and transcription factors after metabolic formation of H2O2 in chloroplasts. Front. Plant Sci. 3: 234.
  • Balazadeh, S., Kwasniewski, M., Caldana, C., Merhnia, M., Zanor, M.-I., Xue, G.-P. and Mueller-Roeber, B. 2011. ORS1, a H2O2-responsive NAC transcription factor, controls senescence in Arabidopsis thaliana. Mol. Plant. 8: 1-15.
  • Balazadeh, S., Schildhauer, J., Wagner L.A., Munné-Bosch, S., Fernie, A.R., Proost, S., Humbeck, K. and Mueller-Roeber, B. 2014. Reversion of senescence by N resupply to N-starved Arabidopsis thaliana: transcriptomic and metabolomic consequences. J. Exp. Bot. 65: 3975-3992.
  • 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 andmemory of stress responses in organisms lacking a nervous system. Biol. Rev. doi: 10.1111/brv.12215.
  • Matallana-Ramirez, L-P., Rauf, M., Farage-Barhom, S., Dortay, H., Xue, G-P., Dröge-Laser, W., Lers, A., Balazadeh, S. and Mueller-Roeber, B. 2013. NAC transcription factor ORE1 and BIFUNCTIONAL NUCLEASE1 (BFN1) constitute a regulatory cascade during senescence in Arabidopsis. Mol. Plant. 6: 1432-1452.
  • Shahnejat-Bushehri, S., Mueller-Roeber, B. and Balazadeh, S. 2012. Arabidopsis NAC transcription factor JUNGBRUNNEN1 affects thermomemory-associated genes and enhances heat stress tolerance in primed and unprimed conditions. Plant Signal Behav. 7: 1518-1521.
  • Wu, A., Allu, AD., Garapati, P., Siddiqui, H., Dortay, H., Zanor, M-I., Asensi-Fabado, MA., Munné-Bosch, S., Antonio, C., Tohge, T., Fernie, A., Kaufmann, K., Xue, G-P., Mueller-Roeber, B. and Balazadeh, S. 2012. JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell 24: 482-506.