@article{KappelFriedrichOberkofleretal.2023,
  author    = {Kappel, Christian and Friedrich, Thomas and Oberkofler, Vicky and Jiang, Li and Crawford, Tim and Lenhard, Michael and B{\"a}urle, Isabel},
  title     = {Genomic and epigenomic determinants of heat stress-induced transcriptional memory in Arabidopsis},
  series = {Genome biology : biology for the post-genomic era},
  volume    = {24},
  journal   = {Genome biology : biology for the post-genomic era},
  number    = {1},
  publisher = {BioMed Central},
  address   = {London},
  issn      = {1474-760X},
  doi       = {10.1186/s13059-023-02970-5},
  pages     = {23},
  year      = {2023},
  abstract  = {Background Transcriptional regulation is a key aspect of environmental stress responses. Heat stress induces transcriptional memory, i.e., sustained induction or enhanced re-induction of transcription, that allows plants to respond more efficiently to a recurrent HS. In light of more frequent temperature extremes due to climate change, improving heat tolerance in crop plants is an important breeding goal. However, not all heat stress-inducible genes show transcriptional memory, and it is unclear what distinguishes memory from non-memory genes. To address this issue and understand the genome and epigenome architecture of transcriptional memory after heat stress, we identify the global target genes of two key memory heat shock transcription factors, HSFA2 and HSFA3, using time course ChIP-seq. Results HSFA2 and HSFA3 show near identical binding patterns. In vitro and in vivo binding strength is highly correlated, indicating the importance of DNA sequence elements. In particular, genes with transcriptional memory are strongly enriched for a tripartite heat shock element, and are hallmarked by several features: low expression levels in the absence of heat stress, accessible chromatin environment, and heat stress-induced enrichment of H3K4 trimethylation. These results are confirmed by an orthogonal transcriptomic data set using both de novo clustering and an established definition of memory genes. Conclusions Our findings provide an integrated view of HSF-dependent transcriptional memory and shed light on its sequence and chromatin determinants, enabling the prediction and engineering of genes with transcriptional memory behavior.},
  language  = {en}
}
@article{FriedrichOberkoflerTrindadeetal.2021,
  author    = {Friedrich, Thomas and Oberkofler, Vicky and Trindade, In{\^e}s and Altmann, Simone and Brzezinka, Krzysztof and L{\"a}mke, J{\"o}rn S. and Gorka, Michal and Kappel, Christian and Sokolowska, Ewelina and Skirycz, Aleksandra and Graf, Alexander and B{\"a}urle, Isabel},
  title     = {Heteromeric HSFA2/HSFA3 complexes drive transcriptional memory after heat stress in Arabidopsis},
  series = {Nature Communications},
  volume    = {12},
  journal   = {Nature Communications},
  number    = {1},
  publisher = {Nature Publishing Group UK},
  address   = {[London]},
  issn      = {2041-1723},
  doi       = {10.1038/s41467-021-23786-6},
  pages     = {15},
  year      = {2021},
  abstract  = {Adaptive plasticity in stress responses is a key element of plant survival strategies. For instance, moderate heat stress (HS) primes a plant to acquire thermotolerance, which allows subsequent survival of more severe HS conditions. Acquired thermotolerance is actively maintained over several days (HS memory) and involves the sustained induction of memory-related genes. Here we show that FORGETTER3/ HEAT SHOCK TRANSCRIPTION FACTOR A3 (FGT3/HSFA3) is specifically required for physiological HS memory and maintaining high memory-gene expression during the days following a HS exposure. HSFA3 mediates HS memory by direct transcriptional activation of memory-related genes after return to normal growth temperatures. HSFA3 binds HSFA2, and in vivo both proteins form heteromeric complexes with additional HSFs. Our results indicate that only complexes containing both HSFA2 and HSFA3 efficiently promote transcriptional memory by positively influencing histone H3 lysine 4 (H3K4) hyper-methylation. In summary, our work defines the major HSF complex controlling transcriptional memory and elucidates the in vivo dynamics of HSF complexes during somatic stress memory. Moderate heat stress primes plants to acquire tolerance to subsequent, more severe heat stress. Here the authors show that the HSFA3 transcription factor forms a heteromeric complex with HSFA2 to sustain activated transcription of genes required for acquired thermotolerance by promoting H3K4 hyper-methylation.},
  language  = {en}
}
@article{CastellanosFriedrichPetrovicetal.2020,
  author    = {Castellanos, Reynel Urrea and Friedrich, Thomas and Petrovic, Nevena and Altmann, Simone and Brzezinka, Krzysztof and Gorka, Michal and Graf, Alexander and B{\"a}urle, Isabel},
  title     = {FORGETTER2 protein phosphatase and phospholipase D modulate heat stress memory in Arabidopsis},
  series = {The plant journal},
  volume    = {104},
  journal   = {The plant journal},
  number    = {1},
  publisher = {Wiley},
  address   = {Hoboken},
  issn      = {0960-7412},
  doi       = {10.1111/tpj.14927},
  pages     = {7 -- 17},
  year      = {2020},
  abstract  = {Plants can mitigate environmental stress conditions through acclimation. In the case of fluctuating stress conditions such as high temperatures, maintaining a stress memory enables a more efficient response upon recurring stress. In a genetic screen forArabidopsis thalianamutants impaired in the memory of heat stress (HS) we have isolated theFORGETTER2(FGT2) gene, which encodes a type 2C protein phosphatase (PP2C) of the D-clade.Fgt2mutants acquire thermotolerance normally; however, they are defective in the memory of HS. FGT2 interacts with phospholipase D alpha 2 (PLD alpha 2), which is involved in the metabolism of membrane phospholipids and is also required for HS memory. In summary, we have uncovered a previously unknown component of HS memory and identified the FGT2 protein phosphatase and PLD alpha 2 as crucial players, suggesting that phosphatidic acid-dependent signaling or membrane composition dynamics underlie HS memory.},
  language  = {en}
}
@misc{FriedrichFaivreBaeurleetal.2018,
  author    = {Friedrich, Thomas and Faivre, Lea and B{\"a}urle, Isabel and Schubert, Daniel},
  title     = {Chromatin-based mechanisms of temperature memory in plants},
  series = {Plant, cell \& environment : cell physiology, whole-plant physiology, community physiology},
  volume    = {42},
  journal   = {Plant, cell \& environment : cell physiology, whole-plant physiology, community physiology},
  number    = {3},
  publisher = {Wiley},
  address   = {Hoboken},
  issn      = {0140-7791},
  doi       = {10.1111/pce.13373},
  pages     = {762 -- 770},
  year      = {2018},
  abstract  = {For successful growth and development, plants constantly have to gauge their environment. Plants are capable to monitor their current environmental conditions, and they are also able to integrate environmental conditions over time and store the information induced by the cues. In a developmental context, such an environmental memory is used to align developmental transitions with favourable environmental conditions. One temperature-related example of this is the transition to flowering after experiencing winter conditions, that is, vernalization. In the context of adaptation to stress, such an environmental memory is used to improve stress adaptation even when the stress cues are intermittent. A somatic stress memory has now been described for various stresses, including extreme temperatures, drought, and pathogen infection. At the molecular level, such a memory of the environment is often mediated by epigenetic and chromatin modifications. Histone modifications in particular play an important role. In this review, we will discuss and compare different types of temperature memory and the histone modifications, as well as the reader, writer, and eraser proteins involved.},
  language  = {en}
}
@article{KabelitzBrzezinkaFriedrichetal.2016,
  author    = {Kabelitz, Tina and Brzezinka, Krzysztof and Friedrich, Thomas and Gorka, Michal and Graf, Alexander and Kappel, Christian and B{\"a}urle, Isabel},
  title     = {A JUMONJI Protein with E3 Ligase and Histone H3 Binding Activities Affects Transposon Silencing in Arabidopsis},
  series = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants},
  volume    = {171},
  journal   = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants},
  publisher = {American Society of Plant Physiologists},
  address   = {Rockville},
  issn      = {0032-0889},
  doi       = {10.1104/pp.15.01688},
  pages     = {344 -- 358},
  year      = {2016},
  abstract  = {Transposable elements (TEs) make up a large proportion of eukaryotic genomes. As their mobilization creates genetic variation that threatens genome integrity, TEs are epigenetically silenced through several pathways, and this may spread to neighboring sequences. JUMONJI (JMJ) proteins can function as antisilencing factors and prevent silencing of genes next to TEs. Whether TE silencing is counterbalanced by the activity of antisilencing factors is still unclear. Here, we characterize JMJ24 as a regulator of TE silencing. We show that loss of JMJ24 results in increased silencing of the DNA transposon AtMu1c, while overexpression of JMJ24 reduces silencing. JMJ24 has a JumonjiC (JmjC) domain and two RING domains. JMJ24 autoubiquitinates in vitro, demonstrating E3 ligase activity of the RING domain(s). JMJ24-JmjC binds the N-terminal tail of histone H3, and full-length JMJ24 binds histone H3 in vivo. JMJ24 activity is anticorrelated with histone H3 Lys 9 dimethylation (H3K9me2) levels at AtMu1c. Double mutant analyses with epigenetic silencing mutants suggest that JMJ24 antagonizes histone H3K9me2 and requires H3K9 methyltransferases for its activity on AtMu1c. Genome-wide transcriptome analysis indicates that JMJ24 affects silencing at additional TEs. Our results suggest that the JmjC domain of JMJ24 has lost demethylase activity but has been retained as a binding domain for histone H3. This is in line with phylogenetic analyses indicating that JMJ24 (with the mutated JmjC domain) is widely conserved in angiosperms. Taken together, this study assigns a role in TE silencing to a conserved JmjC-domain protein with E3 ligase activity, but no demethylase activity.},
  language  = {en}
}