@article{HilkerSchwachtjeBaieretal.2016, author = {Hilker, Monika and Schwachtje, Jens and Baier, Margarete and Balazadeh, Salma and B{\"a}urle, Isabel and Geiselhardt, Sven and Hincha, Dirk K. and Kunze, Reinhard and Mueller-Roeber, Bernd and Rillig, Matthias G. and Rolff, Jens and Schm{\"u}lling, Thomas and Steppuhn, Anke and van Dongen, Joost and Whitcomb, Sarah J. and Wurst, Susanne and Zuther, Ellen and Kopka, Joachim}, title = {Priming and memory of stress responses in organisms lacking a nervous system}, series = {Biological reviews}, volume = {91}, journal = {Biological reviews}, publisher = {Wiley-Blackwell}, address = {Hoboken}, issn = {1464-7931}, doi = {10.1111/brv.12215}, pages = {1118 -- 1133}, year = {2016}, 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} } @article{SchneebergerEccard2021, author = {Schneeberger, Karin and Eccard, Jana}, title = {Experience of social density during early life is associated with attraction to conspecific odour in the common vole (Microtus arvalis)}, series = {Ethology : international journal of behavioural biology}, volume = {127}, journal = {Ethology : international journal of behavioural biology}, number = {10}, publisher = {Wiley-Blackwell}, address = {Berlin}, issn = {0179-1613}, doi = {10.1111/eth.13211}, pages = {908 -- 913}, year = {2021}, abstract = {Social organisation in species with fluctuating population sizes can change with density. Therefore, information on (future) density obtained during early life stages may be associated with social behaviour. Olfactory cues may carry important social information. We investigated whether early life experience of different experimental densities was subsequently associated with differences in attraction to adult conspecific odours. We used common voles (Microtus arvalis), a rodent species undergoing extreme density fluctuations. We found that individuals originating from high experimental density populations kept in large outdoor enclosures invested more time in inspecting conspecific olfactory cues than individuals from low-density populations. Generally, voles from both treatments spent more time with the olfactory cues than expected by chance and did not differ in their latency to approach the odour samples. Our findings indicate either that early experience affects odour sensitivity or that animals evaluate the social information contained in conspecific odours differently, depending on their early life experience of conspecific density.}, language = {en} } @article{LiuLaemkeLinetal.2018, author = {Liu, Hsiang-chin and L{\"a}mke, J{\"o}rn and Lin, Siou-ying and Hung, Meng-Ju and Liu, Kuan-Ming and Charng, Yee-yung and B{\"a}urle, Isabel}, title = {Distinct heat shock factors and chromatin modifications mediate the organ-autonomous transcriptional memory of heat stress}, series = {The plant journal}, volume = {95}, journal = {The plant journal}, number = {3}, publisher = {Wiley}, address = {Hoboken}, issn = {0960-7412}, doi = {10.1111/tpj.13958}, pages = {401 -- 413}, year = {2018}, abstract = {Plants can be primed by a stress cue to mount a faster or stronger activation of defense mechanisms upon subsequent stress. A crucial component of such stress priming is the modified reactivation of genes upon recurring stress; however, the underlying mechanisms of this are poorly understood. Here, we report that dozens of Arabidopsis thaliana genes display transcriptional memory, i.e. stronger upregulation after a recurring heat stress, that lasts for at least 3 days. We define a set of transcription factors involved in this memory response and show that the transcriptional memory results in enhanced transcriptional activation within minutes of the onset of a heat stress cue. Further, we show that the transcriptional memory is active in all tissues. It may last for up to a week, and is associated during this time with histone H3 lysine 4 hypermethylation. This transcriptional memory is cis-encoded, as we identify a promoter fragment that confers memory onto a heterologous gene. In summary, heat-induced transcriptional memory is a widespread and sustained response, and our study provides a framework for future mechanistic studies of somatic stress memory in higher plants.}, language = {en} } @article{AlluSimancasBalazadehetal.2017, author = {Allu, Annapurna Devi and Simancas, Barbara and Balazadeh, Salma and Munne-Bosch, Sergi}, title = {Defense-Related Transcriptional Reprogramming in Vitamin E-Deficient Arabidopsis Mutants Exposed to Contrasting Phosphate Availability}, series = {Frontiers in plant science}, volume = {8}, journal = {Frontiers in plant science}, publisher = {Frontiers Research Foundation}, address = {Lausanne}, issn = {1664-462X}, doi = {10.3389/fpls.2017.01396}, pages = {20}, year = {2017}, abstract = {Vitamin E inhibits the propagation of lipid peroxidation and helps protecting photosystem II from photoinhibition, but little is known about its possible role in plant response to Pi availability. Here, we aimed at examining the effect of vitamin E deficiency in Arabidopsis thaliana vte mutants on phytohormone contents and the expression of transcription factors in plants exposed to contrasting Pi availability. Plants were subjected to two doses of Pi, either unprimed (controls) or previously exposed to low Pi (primed). In the wild type, alpha-tocopherol contents increased significantly in response to repeated periods of low Pi, which was paralleled by increased growth, indicative of a priming effect. This growth-stimulating effect was, however, abolished in vte mutants. Hormonal profiling revealed significant effects of Pi availability, priming and genotype on the contents of jasmonates and salicylates; remarkably, vte mutants showed enhanced accumulation of both hormones under low Pi. Furthermore, expression profiling of 1,880 transcription factors by qRT-PCR revealed a pronounced effect of priming on the transcript levels of 45 transcription factors mainly associated with growth and stress in wild-type plants in response to low Pi availability; while distinct differences in the transcriptional response were detected in vte mutants. We conclude that alpha-tocopherol plays a major role in the response of plants to Pi availability not only by protecting plants from photo-oxidative stress, but also by exerting a control over growth-and defense-related transcriptional reprogramming and hormonal modulation.}, 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{BaeurleTrindade2020, author = {B{\"a}urle, Isabel and Trindade, In{\^e}s}, title = {Chromatin regulation of somatic abiotic stress memory}, series = {Journal of experimental botany}, volume = {71}, journal = {Journal of experimental botany}, number = {17}, publisher = {Oxford Univiversity Press}, address = {Oxford}, issn = {0022-0957}, doi = {10.1093/jxb/eraa098}, pages = {5269 -- 5279}, year = {2020}, abstract = {In nature, plants are often subjected to periods of recurrent environmental stress that can strongly affect their development and productivity. To cope with these conditions, plants can remember a previous stress, which allows them to respond more efficiently to a subsequent stress, a phenomenon known as priming. This ability can be maintained at the somatic level for a few days or weeks after the stress is perceived, suggesting that plants can store information of a past stress during this recovery phase. While the immediate responses to a single stress event have been extensively studied, knowledge on priming effects and how stress memory is stored is still scarce. At the molecular level, memory of a past condition often involves changes in chromatin structure and organization, which may be maintained independently from transcription. In this review, we will summarize the most recent developments in the field and discuss how different levels of chromatin regulation contribute to priming and plant abiotic stress memory.}, language = {en} } @article{BaeurleBrzezinkaAltmann2018, author = {B{\"a}urle, Isabel and Brzezinka, Krzysztof and Altmann, Simone}, title = {BRUSHY1/TONSOKU/MGOUN3 is required for heat stress memory}, series = {Plant Cell \& Environment}, volume = {42}, journal = {Plant Cell \& Environment}, doi = {10.1111/pce.13365}, pages = {771 -- 781}, year = {2018}, abstract = {Plants encounter biotic and abiotic stresses many times during their life cycle and this limits their productivity. Moderate heat stress (HS) primes a plant to survive higher temperatures that are lethal in the na{\"i}ve state. Once temperature stress subsides, the memory of the priming event is actively retained for several days preparing the plant to better cope with recurring HS. Recently, chromatin regulation at different levels has been implicated in HS memory. Here, we report that the chromatin protein BRUSHY1 (BRU1)/TONSOKU/MGOUN3 plays a role in the HS memory in Arabidopsis thaliana. BRU1 is also involved in transcriptional gene silencing and DNA damage repair. This corresponds with the functions of its mammalian orthologue TONSOKU-LIKE/NFΚBIL2. During HS memory, BRU1 is required to maintain sustained induction of HS memory-associated genes, whereas it is dispensable for the acquisition of thermotolerance. In summary, we report that BRU1 is required for HS memory in A. thaliana, and propose a model where BRU1 mediates the epigenetic inheritance of chromatin states across DNA replication and cell division.}, language = {en} } @article{SedaghatmehrThirumalaikumarKamranfaretal.2019, author = {Sedaghatmehr, Mastoureh and Thirumalaikumar, Venkatesh P. and Kamranfar, Iman and Marmagne, Anne and Masclaux-Daubresse, Celine and Balazadeh, Salma}, title = {A regulatory role of autophagy for resetting the memory of heat stress 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.13426}, pages = {1054 -- 1064}, year = {2019}, abstract = {As sessile life forms, plants are repeatedly confronted with adverse environmental conditions, which can impair development, growth, and reproduction. During evolution, plants have established mechanisms to orchestrate the delicate balance between growth and stress tolerance, to reset cellular biochemistry once stress vanishes, or to keep a molecular memory, which enables survival of a harsher stress that may arise later. Although there are several examples of memory in diverse plants species, the molecular machinery underlying the formation, duration, and resetting of stress memories is largely unknown so far. We report here that autophagy, a central self-degradative process, assists in resetting cellular memory of heat stress (HS) in Arabidopsis thaliana. Autophagy is induced by thermopriming (moderate HS) and, intriguingly, remains high long after stress termination. We demonstrate that autophagy mediates the specific degradation of heat shock proteins at later stages of the thermorecovery phase leading to the accumulation of protein aggregates after the second HS and a compromised heat tolerance. Autophagy mutants retain heat shock proteins longer than wild type and concomitantly display improved thermomemory. Our findings reveal a novel regulatory mechanism for HS memory in plants.}, language = {en} } @article{LaemkeBrzezinkaAltmannetal.2016, author = {L{\"a}mke, J{\"o}rn and Brzezinka, Krzysztof and Altmann, Simone and B{\"a}urle, Isabel}, title = {A hit-and-run heat shock factor governs sustained histone methylation and transcriptional stress memory}, series = {The EMBO journal}, volume = {35}, journal = {The EMBO journal}, publisher = {Wiley-Blackwell}, address = {Hoboken}, issn = {0261-4189}, doi = {10.15252/embj.201592593}, pages = {162 -- 175}, year = {2016}, abstract = {In nature, plants often encounter chronic or recurring stressful conditions. Recent results indicate that plants can remember a past exposure to stress to be better prepared for a future stress incident. However, the molecular basis of this is poorly understood. Here, we report the involvement of chromatin modifications in the maintenance of acquired thermotolerance (heat stress [HS] memory). HS memory is associated with the accumulation of histone H3 lysine 4 di- and trimethylation at memory-related loci. This accumulation outlasts their transcriptional activity and marks them as recently transcriptionally active. High accumulation of H3K4 methylation is associated with hyper-induction of gene expression upon a recurring HS. This transcriptional memory and the sustained accumulation of H3K4 methylation depend on HSFA2, a transcription factor that is required for HS memory, but not initial heat responses. Interestingly, HSFA2 associates with memory-related loci transiently during the early stages following HS. In summary, we show that transcriptional memory after HS is associated with sustained H3K4 hyper-methylation and depends on a hit-and-run transcription factor, thus providing a molecular framework for HS memory.}, language = {en} }