TY - JOUR A1 - Shahnejat-Bushehri, Sara A1 - Allu, Annapurna Devi A1 - Mehterov, Nikolay A1 - Thirumalaikumar, Venkatesh P. A1 - Alseekh, Saleh A1 - Fernie, Alisdair A1 - Mueller-Roeber, Bernd A1 - Balazadeh, Salma T1 - Arabidopsis NAC Transcription Factor JUNGBRUNNEN1 Exerts Conserved Control Over Gibberellin and Brassinosteroid Metabolism and Signaling Genes in Tomato JF - Frontiers in plant science N2 - The Arabidopsis thaliana NAC transcription factor JUNGBRUNNEN1 (AtJUB1) regulates growth by directly repressing GA3ox1 and DWF4, two key genes involved in gibberellin (GA) and brassinosteroid (BR) biosynthesis, respectively, leading to GA and BR deficiency phenotypes. AtJUB1 also reduces the expression of PIF4, a bHLH transcription factor that positively controls cell elongation, while it stimulates the expression of DELLA genes, which are important repressors of growth. Here, we extend our previous findings by demonstrating that AtJUB1 induces similar GA and BR deficiency phenotypes and changes in gene expression when overexpressed in tomato (Solanum lycopersicum). Importantly, and in accordance with the growth phenotypes observed, AtJUB1 inhibits the expression of growth-supporting genes, namely the tomato orthologs of GA3ox1, DWF4 and PIF4, but activates the expression of DELLA orthologs, by directly binding to their promoters. Overexpression of AtJUB1 in tomato delays fruit ripening, which is accompanied by reduced expression of several ripeningrelated genes, and leads to an increase in the levels of various amino acids (mostly proline, beta-alanine, and phenylalanine), gamma-aminobutyric acid (GABA), and major organic acids including glutamic acid and aspartic acid. The fact that AtJUB1 exerts an inhibitory effect on the GA/BR biosynthesis and PIF4 genes but acts as a direct activator of DELLA genes in both, Arabidopsis and tomato, strongly supports the model that the molecular constituents of the JUNGBRUNNEN1 growth control module are considerably conserved across species. KW - Arabidopsis KW - tomato KW - fruit KW - growth KW - transcription factor KW - gibberellic acid KW - brassinosteroid KW - DELLA proteins Y1 - 2017 U6 - https://doi.org/10.3389/fpls.2017.00214 SN - 1664-462X VL - 8 PB - Frontiers Research Foundation CY - Lausanne ER - TY - JOUR A1 - Watanabe, Mutsumi A1 - Tohge, Takayuki A1 - Balazadeh, Salma A1 - Erban, Alexander A1 - Giavalisco, Patrick A1 - Kopka, Joachim A1 - Mueller-Roeber, Bernd A1 - Fernie, Alisdair A1 - Hoefgen, Rainer T1 - Comprehensive Metabolomics Studies of Plant Developmental Senescence JF - Plant Senescence: Methods and Protocols N2 - Leaf senescence is an essential developmental process that involves diverse metabolic changes associated with degradation of macromolecules allowing nutrient recycling and remobilization. In contrast to the significant progress in transcriptomic analysis of leaf senescence, metabolomics analyses have been relatively limited. A broad overview of metabolic changes during leaf senescence including the interactions between various metabolic pathways is required to gain a better understanding of the leaf senescence allowing to link transcriptomics with metabolomics and physiology. In this chapter, we describe how to obtain comprehensive metabolite profiles and how to dissect metabolic shifts during leaf senescence in the model plant Arabidopsis thaliana. Unlike nucleic acid analysis for transcriptomics, a comprehensive metabolite profile can only be achieved by combining a suite of analytic tools. Here, information is provided for measurements of the contents of chlorophyll, soluble proteins, and starch by spectrophotometric methods, ions by ion chromatography, thiols and amino acids by HPLC, primary metabolites by GC/TOF-MS, and secondary metabolites and lipophilic metabolites by LC/ESI-MS. These metabolite profiles provide a rich catalogue of metabolic changes during leaf senescence, which is a helpful database and blueprint to be correlated to future studies such as transcriptome and proteome analyses, forward and reverse genetic studies, or stress-induced senescence studies. KW - Senescence KW - Metabolomics KW - Arabidopsis KW - GC/MS KW - LC/MS KW - HPLC KW - IC Y1 - 2018 SN - 978-1-4939-7672-0 SN - 978-1-4939-7670-6 U6 - https://doi.org/10.1007/978-1-4939-7672-0_28 SN - 1064-3745 SN - 1940-6029 VL - 1744 SP - 339 EP - 358 PB - Humana Press CY - Totowa ER - TY - JOUR A1 - Thirumalaikumar, Venkatesh P. A1 - Devkar, Vikas A1 - Mehterov, Nikolay A1 - Ali, Shawkat A1 - Ozgur, Rengin A1 - Turkan, Ismail A1 - Müller-Röber, Bernd A1 - Balazadeh, Salma T1 - NAC transcription factor JUNGBRUNNEN1 enhances drought tolerance in tomato JF - Plant Biotechnology Journal N2 - Water deficit (drought stress) massively restricts plant growth and the yield of crops; reducing the deleterious effects of drought is therefore of high agricultural relevance. Drought triggers diverse cellular processes including the inhibition of photosynthesis, the accumulation of cell-damaging reactive oxygen species and gene expression reprogramming, besides others. Transcription factors (TF) are central regulators of transcriptional reprogramming and expression of many TF genes is affected by drought, including members of the NAC family. Here, we identify the NAC factor JUNGBRUNNEN1 (JUB1) as a regulator of drought tolerance in tomato (Solanum lycopersicum). Expression of tomato JUB1 (SlJUB1) is enhanced by various abiotic stresses, including drought. Inhibiting SlJUB1 by virus-induced gene silencing drastically lowers drought tolerance concomitant with an increase in ion leakage, an elevation of hydrogen peroxide (H2O2) levels and a decrease in the expression of various drought-responsive genes. In contrast, overexpression of AtJUB1 from Arabidopsis thaliana increases drought tolerance in tomato, alongside with a higher relative leaf water content during drought and reduced H2O2 levels. AtJUB1 was previously shown to stimulate expression of DREB2A, a TF involved in drought responses, and of the DELLA genes GAI and RGL1. We show here that SlJUB1 similarly controls the expression of the tomato orthologs SlDREB1, SlDREB2 and SlDELLA. Furthermore, AtJUB1 directly binds to the promoters of SlDREB1, SlDREB2 and SlDELLA in tomato. Our study highlights JUB1 as a transcriptional regulator of drought tolerance and suggests considerable conservation of the abiotic stress-related gene regulatory networks controlled by this NAC factor between Arabidopsis and tomato. KW - Arabidopsis KW - tomato KW - transcription factor KW - drought KW - reactive oxygen species KW - DELLA Y1 - 2017 U6 - https://doi.org/10.1111/pbi.12776 SN - 1467-7644 SN - 1467-7652 VL - 16 IS - 2 SP - 354 EP - 366 PB - Wiley CY - Hoboken ER - TY - JOUR A1 - Kamranfar, Iman A1 - Xue, Gang-Ping A1 - Tohge, Takayuki A1 - Sedaghatmehr, Mastoureh A1 - Fernie, Alisdair A1 - Balazadeh, Salma A1 - Mueller-Roeber, Bernd T1 - Transcription factor RD26 is a key regulator of metabolic reprogramming during dark-induced senescence JF - New phytologist : international journal of plant science N2 - Leaf senescence is a key process in plants that culminates in the degradation of cellular constituents and massive reprogramming of metabolism for the recovery of nutrients from aged leaves for their reuse in newly developing sinks. We used molecular-biological and metabolomics approaches to identify NAC transcription factor (TF) RD26 as an important regulator of metabolic reprogramming in Arabidopsis thaliana. RD26 directly activates CHLOROPLAST VESICULATION (CV), encoding a protein crucial for chloroplast protein degradation, concomitant with an enhanced protein loss in RD26 over-expressors during senescence, but a reduced decline of protein in rd26 knockout mutants. RD26 also directly activates LKR/SDH involved in lysine catabolism, and PES1 important for phytol degradation. Metabolic profiling revealed reduced c-aminobutyric acid (GABA) in RD26 overexpressors, accompanied by the induction of respective catabolic genes. Degradation of lysine, phytol and GABA is instrumental for maintaining mitochondrial respiration in carbon-limiting conditions during senescence. RD26 also supports the degradation of starch and the accumulation of mono-and disaccharides during senescence by directly enhancing the expression of AMY1, SFP1 and SWEET15 involved in carbohydrate metabolism and transport. Collectively, during senescence RD26 acts by controlling the expression of genes across the entire spectrum of the cellular degradation hierarchy. KW - Arabidopsis KW - fatty acid KW - primary metabolism KW - protein and amino acid degradation KW - respiration KW - senescence Y1 - 2018 U6 - https://doi.org/10.1111/nph.15127 SN - 0028-646X SN - 1469-8137 VL - 218 IS - 4 SP - 1543 EP - 1557 PB - Wiley CY - Hoboken ER - TY - JOUR A1 - Sedaghatmehr, Mastoureh A1 - Thirumalaikumar, Venkatesh P. A1 - Kamranfar, Iman A1 - Marmagne, Anne A1 - Masclaux-Daubresse, Celine A1 - Balazadeh, Salma T1 - A regulatory role of autophagy for resetting the memory of heat stress in plants JF - Plant, cell & environment : cell physiology, whole-plant physiology, community physiology N2 - 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. KW - Arabidopsis KW - heat shock proteins KW - priming KW - resetting Y1 - 2019 U6 - https://doi.org/10.1111/pce.13426 SN - 0140-7791 SN - 1365-3040 VL - 42 IS - 3 SP - 1054 EP - 1064 PB - Wiley CY - Hoboken ER - TY - JOUR A1 - Czarnocka, Weronika A1 - Van Der Kelen, Katrien A1 - Willems, Patrick A1 - Szechynska-Hebda, Magdalena A1 - Shahnejat-Bushehri, Sara A1 - Balazadeh, Salma A1 - Rusaczonek, Anna A1 - Müller-Röber, Bernd A1 - Van Breusegem, Frank A1 - Karpinski, Stanislaw T1 - The dual role of LESION SIMULATING DISEASE 1 as a condition-dependent scaffold protein and transcription regulator JF - Plant, cell & environment : cell physiology, whole-plant physiology, community physiology N2 - Since its discovery over two decades ago as an important cell death regulator in Arabidopsis thaliana, the role of LESION SIMULATING DISEASE 1 (LSD1) has been studied intensively within both biotic and abiotic stress responses as well as with respect to plant fitness regulation. However, its molecular mode of action remains enigmatic. Here, we demonstrate that nucleo-cytoplasmic LSD1 interacts with a broad range of other proteins that are engaged in various molecular pathways such as ubiquitination, methylation, cell cycle control, gametogenesis, embryo development and cell wall formation. The interaction of LSD1 with these partners is dependent on redox status, as oxidative stress significantly changes the quantity and types of LSD1-formed complexes. Furthermore, we show that LSD1 regulates the number and size of leaf mesophyll cells and affects plant vegetative growth. Importantly, we also reveal that in addition to its function as a scaffold protein, LSD1 acts as a transcriptional regulator. Taken together, our results demonstrate that LSD1 plays a dual role within the cell by acting as a condition-dependent scaffold protein and as a transcription regulator. KW - Arabidopsis KW - thaliana KW - dry weight KW - LSD1 KW - oxidative stress KW - protein interaction KW - transcription regulation Y1 - 2017 U6 - https://doi.org/10.1111/pce.12994 SN - 0140-7791 SN - 1365-3040 VL - 40 SP - 2644 EP - 2662 PB - Wiley CY - Hoboken ER - TY - JOUR A1 - Ebrahimian-Motlagh, Saghar A1 - Ribone, Pamela A. A1 - Thirumalaikumar, Venkatesh P. A1 - Allu, Annapurna Devi A1 - Chan, Raquel L. A1 - Mueller-Roeber, Bernd A1 - Balazadeh, Salma T1 - JUNGBRUNNEN1 Confers Drought Tolerance Downstream of the HD-Zip I Transcription Factor AtHB13 JF - Frontiers in plant science N2 - Low water availability is the major environmental factor limiting growth and productivity of plants and crops and is therefore considered of high importance for agriculture affected by climate change. Identifying regulatory components controlling the response and tolerance to drought stress is thus of major importance. The NAC transcription factor (TF) JUNGBRUNNEN1 (JUB1) from Arabidopsis thaliana extends leaf longevity under non-stress growth conditions, lowers cellular hydrogen peroxide (H2O2) level, and enhances tolerance against heat stress and salinity. Here, we additionally find that JUB1 strongly increases tolerance to drought stress in Arabidopsis when expressed from both, a constitutive (CaMV 35S) and an abiotic stress-induced (RD29A) promoter. Employing a yeast one-hybrid screen we identified HD-Zip class I TF AtHB13 as an upstream regulator of JUB1. AtHB13 has previously been reported to act as a positive regulator of drought tolerance. AtHB13 and JUB1 thereby establish a joint drought stress control module. KW - Arabidopsis KW - transcription factor KW - drought KW - JUB1 KW - HB13 Y1 - 2017 U6 - https://doi.org/10.3389/fpls.2017.02118 SN - 1664-462X VL - 8 PB - Frontiers Research Foundation CY - Lausanne ER - TY - JOUR A1 - Shahnejat-Bushehri, Sara A1 - Nobmann, Barbara A1 - Allu, Annapurna Devi A1 - Balazadeh, Salma T1 - JUB1 suppresses Pseudomonas syringae-induced defense responses through accumulation of DELLA proteins JF - Journal of trace elements in medicine and biology N2 - Phytohormones act in concert to coordinate plant growth and the response to environmental cues. Gibberellins (GAs) are growth-promoting hormones that recently emerged as modulators of plant immune signaling. By regulating the stability of DELLA proteins, GAs intersect with the signaling pathways of the classical primary defense hormones, salicylic acid (SA) and jasmonic acid (JA), thereby altering the final outcome of the immune response. DELLA proteins confer resistance to necrotrophic pathogens by potentiating JA signaling and raise the susceptibility to biotrophic pathogens by attenuating the SA pathway. Here, we show that JUB1, a core element of the GA - brassinosteroid (BR) - DELLA regulatory module, functions as a negative regulator of defense responses against Pseudomonas syringae pv. tomato DC3000 (Pst DC3000) and mediates the crosstalk between growth and immunity. KW - Arabidopsis KW - defense KW - DELLA proteins KW - gibberellin KW - jasmonic acid KW - pathogens KW - salicylic acid KW - transcription factor Y1 - 2016 U6 - https://doi.org/10.1080/15592324.2016.1181245 SN - 1559-2316 SN - 1559-2324 VL - 11 PB - Elsevier CY - Philadelphia ER - TY - JOUR A1 - Allu, Annapurna Devi A1 - Brotman, Yariv A1 - Xue, Gang-Ping A1 - Balazadeh, Salma T1 - Transcription factor ANAC032 modulates JA/SA signalling in response to Pseudomonas syringae infection JF - EMBO reports N2 - Responses to pathogens, including host transcriptional reprogramming, require partially antagonistic signalling pathways dependent on the phytohormones salicylic (SA) and jasmonic (JA) acids. However, upstream factors modulating the interplay of these pathways are not well characterized. Here, we identify the transcription factor ANAC032 from Arabidopsis thaliana as one such regulator in response to the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 (Pst). ANAC032 directly represses MYC2 activation upon Pst attack, resulting in blockage of coronatine-mediated stomatal reopening which restricts entry of bacteria into plant tissue. Furthermore, ANAC032 activates SA signalling by repressing NIMIN1, a key negative regulator of SA-dependent defence. Finally, ANAC032 reduces expression of JA-responsive genes, including PDF1.2A. Thus, ANAC032 enhances resistance to Pst by generating an orchestrated transcriptional output towards key SA- and JA-signalling genes coordinated through direct binding of ANAC032 to the MYC2, NIMIN1 and PDF1.2A promoters. KW - Arabidopsis KW - jasmonic acid KW - pathogens KW - salicylic acid KW - transcription factor Y1 - 2016 U6 - https://doi.org/10.15252/embr.201642197 SN - 1469-221X SN - 1469-3178 VL - 17 SP - 1578 EP - 1589 PB - Wiley-Blackwell CY - Hoboken ER - TY - GEN A1 - Thirumalaikumar, Venkatesh P. A1 - Devkar, Vikas A1 - Mehterov, Nikolay A1 - Ali, Shawkat A1 - Ozgur, Rengin A1 - Turkan, Ismail A1 - Müller-Röber, Bernd A1 - Balazadeh, Salma T1 - NAC transcription factor JUNGBRUNNEN1 enhances drought tolerance in tomato T2 - Postprints der Universität Potsdam Mathematisch-Naturwissenschaftliche Reihe N2 - Water deficit (drought stress) massively restricts plant growth and the yield of crops; reducing the deleterious effects of drought is therefore of high agricultural relevance. Drought triggers diverse cellular processes including the inhibition of photosynthesis, the accumulation of cell‐damaging reactive oxygen species and gene expression reprogramming, besides others. Transcription factors (TF) are central regulators of transcriptional reprogramming and expression of many TF genes is affected by drought, including members of the NAC family. Here, we identify the NAC factor JUNGBRUNNEN1 (JUB1) as a regulator of drought tolerance in tomato (Solanum lycopersicum). Expression of tomato JUB1 (SlJUB1) is enhanced by various abiotic stresses, including drought. Inhibiting SlJUB1 by virus‐induced gene silencing drastically lowers drought tolerance concomitant with an increase in ion leakage, an elevation of hydrogen peroxide (H2O2) levels and a decrease in the expression of various drought‐responsive genes. In contrast, overexpression of AtJUB1 from Arabidopsis thaliana increases drought tolerance in tomato, alongside with a higher relative leaf water content during drought and reduced H2O2 levels. AtJUB1 was previously shown to stimulate expression of DREB2A, a TF involved in drought responses, and of the DELLA genes GAI and RGL1. We show here that SlJUB1 similarly controls the expression of the tomato orthologs SlDREB1, SlDREB2 and SlDELLA. Furthermore, AtJUB1 directly binds to the promoters of SlDREB1, SlDREB2 and SlDELLA in tomato. Our study highlights JUB1 as a transcriptional regulator of drought tolerance and suggests considerable conservation of the abiotic stress‐related gene regulatory networks controlled by this NAC factor between Arabidopsis and tomato. T3 - Zweitveröffentlichungen der Universität Potsdam : Mathematisch-Naturwissenschaftliche Reihe - 568 KW - Arabidopsis KW - tomato KW - transcription factor KW - drought KW - reactive oxygen species KW - DELLA Y1 - 2019 U6 - http://nbn-resolving.de/urn/resolver.pl?urn:nbn:de:kobv:517-opus4-423908 SN - 1866-8372 IS - 568 ER -