TY  - JOUR
A1  - Köslin-Findeklee, Fabian
A1  - Rizi, Vajiheh Safavi
A1  - Becker, Martin A.
A1  - Parra-Londono, Sebastian
A1  - Arif, Muhammad
A1  - Balazadeh, Salma
A1  - Müller-Röber, Bernd
A1  - Kunze, Reinhard
A1  - Horst, Walter J.
T1  - Transcriptomic analysis of nitrogen starvation- and cultivar-specific leaf senescence in winter oilseed rape (Brassica napus L.)
JF  - Plant science : an international journal of experimental plant biology
N2  - High nitrogen (N) efficiency, characterized by high grain yield under N limitation, is an important agricultural trait in Brassica napus L. cultivars related to delayed senescence of older leaves during reproductive growth (a syndrome called stay-green). The aim of this study was thus to identify genes whose expression is specifically altered during N starvation-induced leaf senescence and that can be used as markers to distinguish cultivars at early stages of senescence prior to chlorophyll loss. To this end, the transcriptomes of leaves of two B. napus cultivars differing in stay-green characteristics and N efficiency were analyzed 4 days after the induction of senescence by either N starvation, leaf shading or detaching. In addition to N metabolism genes, N starvation mostly (and specifically) repressed genes related to photosynthesis, photorespiration and cell-wall structure, while genes related to mitochondrial electron transport and flavonoid biosynthesis were predominately up-regulated. A kinetic study over a period of 12 days with four B. napus cultivars differing in their stay-green characteristics confirmed the cultivar-specific regulation of six genes in agreement with their senescence behavior: the senescence regulator ANAC029, the anthocyanin synthesis-related genes ANS and DFR-like1, the ammonium transporter AMT1:4, the ureide transporter UPSS, and SPS1 involved in sucrose biosynthesis. The identified genes represent markers for the detection of cultivar-specific differences in N starvation-induced leaf senescence and can thus be employed as valuable tools in B. napus breeding. (C) 2015 Elsevier Ireland Ltd. All rights reserved.
KW  - Brassica napus
KW  - Genotypic differences
KW  - Leaf senescence
KW  - Molecular marker
KW  - N efficiency
KW  - Stay-green
Y1  - 2015
U6  - https://doi.org/10.1016/j.plantsci.2014.11.018
SN  - 0168-9452
VL  - 233
SP  - 174
EP  - 185
PB  - Elsevier
CY  - Clare
ER  - 
TY  - JOUR
A1  - Kamranfar, Iman
A1  - Xue, Gang-Ping
A1  - Tohge, Takayuki
A1  - Sedaghatmehr, Mastoureh
A1  - Fernie, Alisdair R.
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  - Garapati, Prashanth
A1  - Xue, Gang-Ping
A1  - Munne-Bosch, Sergi
A1  - Balazadeh, Salma
T1  - Transcription Factor ATAF1 in Arabidopsis Promotes Senescence by Direct Regulation of Key Chloroplast Maintenance and Senescence Transcriptional Cascades
JF  - Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants
N2  - Senescence represents a fundamental process of late leaf development. Transcription factors (TFs) play an important role for expression reprogramming during senescence; however, the gene regulatory networks through which they exert their functions, and their physiological integration, are still largely unknown. Here, we identify the Arabidopsis (Arabidopsis thaliana) abscisic acid (ABA)- and hydrogen peroxide-activated TF Arabidopsis thaliana ACTIVATING FACTOR1 (ATAF1) as a novel upstream regulator of senescence. ATAF1 executes its physiological role by affecting both key chloroplast maintenance and senescence-promoting TFs, namely GOLDEN2-LIKE1 (GLK1) and ORESARA1 (ARABIDOPSIS NAC092), respectively. Notably, while ATAF1 activates ORESARA1, it represses GLK1 expression by directly binding to their promoters, thereby generating a transcriptional output that shifts the physiological balance toward the progression of senescence. We furthermore demonstrate a key role of ATAF1 for ABA- and hydrogen peroxide-induced senescence, in accordance with a direct regulatory effect on ABA homeostasis genes, including NINE-CIS-EPOXYCAROTENOID DIOXYGENASE3 involved in ABA biosynthesis and ABC TRANSPORTER G FAMILY MEMBER40, encoding an ABA transport protein. Thus, ATAF1 serves as a core transcriptional activator of senescence by coupling stress-related signaling with photosynthesis- and senescence-related transcriptional cascades.
Y1  - 2015
U6  - https://doi.org/10.1104/pp.15.00567
SN  - 0032-0889
SN  - 1532-2548
VL  - 168
IS  - 3
SP  - 1122
EP  - +
PB  - American Society of Plant Physiologists
CY  - Rockville
ER  - 
TY  - JOUR
A1  - Garapati, Prashanth
A1  - Feil, Regina
A1  - Lunn, John Edward
A1  - Van Dijck, Patrick
A1  - Balazadeh, Salma
A1  - Müller-Röber, Bernd
T1  - Transcription Factor Arabidopsis Activating Factor1 Integrates Carbon Starvation Responses with Trehalose Metabolism
JF  - Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants
N2  - Plants respond to low carbon supply by massive reprogramming of the transcriptome and metabolome. We show here that the carbon starvation-induced NAC (for NO APICAL MERISTEM/ARABIDOPSIS TRANSCRIPTION ACTIVATION FACTOR/CUP-SHAPED COTYLEDON) transcription factor Arabidopsis (Arabidopsis thaliana) Transcription Activation Factor1 (ATAF1) plays an important role in this physiological process. We identified TREHALASE1, the only trehalase-encoding gene in Arabidopsis, as a direct downstream target of ATAF1. Overexpression of ATAF1 activates TREHALASE1 expression and leads to reduced trehalose-6-phosphate levels and a sugar starvation metabolome. In accordance with changes in expression of starch biosynthesis-and breakdown-related genes, starch levels are generally reduced in ATAF1 overexpressors but elevated in ataf1 knockout plants. At the global transcriptome level, genes affected by ATAF1 are broadly associated with energy and carbon starvation responses. Furthermore, transcriptional responses triggered by ATAF1 largely overlap with expression patterns observed in plants starved for carbon or energy supply. Collectively, our data highlight the existence of a positively acting feedforward loop between ATAF1 expression, which is induced by carbon starvation, and the depletion of cellular carbon/energy pools that is triggered by the transcriptional regulation of downstream gene regulatory networks by ATAF1.
Y1  - 2015
U6  - https://doi.org/10.1104/pp.15.00917
SN  - 0032-0889
SN  - 1532-2548
VL  - 169
IS  - 1
SP  - 379
EP  - 390
PB  - American Society of Plant Physiologists
CY  - Rockville
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  - JOUR
A1  - Ma, Xuemin
A1  - Balazadeh, Salma
A1  - Mueller-Roeber, Bernd
T1  - Tomato fruit ripening factor NOR controls leaf senescence
JF  - Journal of experimental botany
N2  - NAC transcription factors (TFs) are important regulators of expressional reprogramming during plant development, stress responses, and leaf senescence. NAC TFs also play important roles in fruit ripening. In tomato (Solanum lycopersicum), one of the best characterized NACs involved in fruit ripening is NON-RIPENING (NOR), and the non-ripening (nor) mutation has been widely used to extend fruit shelf life in elite varieties. Here, we show that NOR additionally controls leaf senescence. Expression of NOR increases with leaf age, and developmental as well as dark-induced senescence are delayed in the nor mutant, while overexpression of NOR promotes leaf senescence. Genes associated with chlorophyll degradation as well as senescence-associated genes (SAGs) show reduced and elevated expression, respectively, in nor mutants and NOR overexpressors. Overexpression of NOR also stimulates leaf senescence in Arabidopsis thaliana. In tomato, NOR supports senescence by directly and positively regulating the expression of several senescence-associated genes including, besides others, SlSAG15 and SlSAG113, SlSGR1, and SlYLS4. Finally, we find that another senescence control NAC TF, namely SlNAP2, acts upstream of NOR to regulate its expression. Our data support a model whereby NAC TFs have often been recruited by higher plants for both the control of leaf senescence and fruit ripening.
KW  - Aging
KW  - leaf
KW  - NAC
KW  - non-ripening
KW  - NOR
KW  - senescence
KW  - tomato
KW  - transcription factor
Y1  - 2019
U6  - https://doi.org/10.1093/jxb/erz098
SN  - 0022-0957
SN  - 1460-2431
VL  - 70
IS  - 10
SP  - 2727
EP  - 2740
PB  - Oxford Univ. Press
CY  - Oxford
ER  - 
TY  - JOUR
A1  - Gliwicka, Marta
A1  - Balazadeh, Salma
A1  - Caldana, Camila
A1  - Müller-Röber, Bernd
A1  - Gaj, Malgorzata D.
T1  - The use of multi-qPCR platform and tan1 mutant in identification of TF genes involved in somatic embryogenesis in Arabidopsis
Y1  - 2009
UR  - http://www.ib.uj.edu.pl/abc/index.php?d=06
SN  - 0001-5296
ER  - 
TY  - JOUR
A1  - Sedaghatmehr, Mastoureh
A1  - Müller-Röber, Bernd
A1  - Balazadeh, Salma
T1  - The plastid metalloprotease FtsH6 and small heat shock protein HSP21 jointly regulate thermomemory in Arabidopsis
JF  - Nature Communications
N2  - Acquired tolerance to heat stress is an increased resistance to elevated temperature following a prior exposure to heat. The maintenance of acquired thermotolerance in the absence of intervening stress is called ‘thermomemory’ but the mechanistic basis for this memory is not well defined. Here we show that Arabidopsis HSP21, a plastidial small heat shock protein that rapidly accumulates after heat stress and remains abundant during the thermomemory phase, is a crucial component of thermomemory. Sustained memory requires that HSP21 levels remain high. Through pharmacological interrogation and transcriptome profiling, we show that the plastid-localized metalloprotease FtsH6 regulates HSP21 abundance. Lack of a functional FtsH6 protein promotes HSP21 accumulation during the later stages of thermomemory and increases thermomemory capacity. Our results thus reveal the presence of a plastidial FtsH6–HSP21 control module for thermomemory in plants.
Y1  - 2016
U6  - https://doi.org/10.1038/ncomms12439
SN  - 2041-1723
VL  - 7
PB  - Nature Publ. Group
CY  - London
ER  - 
TY  - JOUR
A1  - Ma, Xuemin
A1  - Zhang, Youjun
A1  - Tureckova, Veronika
A1  - Xue, Gang-Ping
A1  - Fernie, Alisdair R.
A1  - Mueller-Röber, Bernd
A1  - Balazadeh, Salma
T1  - The NAC Transcription Factor SlNAP2 Regulates Leaf Senescence and Fruit Yield in Tomato
JF  - Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants
N2  - Leaf senescence is an essential physiological process in plants that supports the recycling of nitrogen and other nutrients to support the growth of developing organs, including young leaves, seeds, and fruits. Thus, the regulation of senescence is crucial for evolutionary success in wild populations and for increasing yield in crops. Here, we describe the influence of a NAC transcription factor, SlNAP2 (Solanum lycopersicum NAC-like, activated by Apetala3/Pistillata), that controls both leaf senescence and fruit yield in tomato (S. lycopersicum). SlNAP2 expression increases during age-dependent and dark-induced leaf senescence. We demonstrate that SlNAP2 activates SlSAG113 (S. lycopersicum SENESCENCE-ASSOCIATED GENE113), a homolog of Arabidopsis (Arabidopsis thaliana) SAG113, chlorophyll degradation genes such as SlSGR1 (S. lycopersicum senescence-inducible chloroplast stay-green protein 1) and SlPAO (S. lycopersicum pheide a oxygenase), and other downstream targets by directly binding to their promoters, thereby promoting leaf senescence. Furthermore, SlNAP2 directly controls the expression of genes important for abscisic acid (ABA) biosynthesis, S. lycopersicum 9-cis-epoxycarotenoid dioxygenase 1 (SlNCED1); transport, S. lycopersicum ABC transporter G family member 40 (SlABCG40); and degradation, S. lycopersicum ABA 8′-hydroxylase (SlCYP707A2), indicating that SlNAP2 has a complex role in establishing ABA homeostasis during leaf senescence. Inhibiting SlNAP2 expression in transgenic tomato plants impedes leaf senescence but enhances fruit yield and sugar content likely due to prolonged leaf photosynthesis in aging tomato plants. Our data indicate that SlNAP2 has a central role in controlling leaf senescence and fruit yield in tomato.
Y1  - 2018
U6  - https://doi.org/10.1104/pp.18.00292
SN  - 0032-0889
SN  - 1532-2548
VL  - 177
IS  - 3
SP  - 1286
EP  - 1302
PB  - American Society of Plant Physiologists
CY  - Rockville
ER  - 
TY  - JOUR
A1  - Brotman, Yariv
A1  - Landau, Udi
A1  - Pnini, Smadar
A1  - Lisec, Jan
A1  - Balazadeh, Salma
A1  - Müller-Röber, Bernd
A1  - Zilberstein, Aviah
A1  - Willmitzer, Lothar
A1  - Chet, Ilan
A1  - Viterbo, Ada
T1  - The LysM Receptor-Like Kinase LysM RLK1 is required to activate defense and abiotic-stress responses induced by overexpression of fungal chitinases in arabidopsis plants
JF  - Molecular plant
N2  - Application of crab shell chitin or pentamer chitin oligosaccharide to Arabidopsis seedlings increased tolerance to salinity in wild-type but not in knockout mutants of the LysM Receptor-Like Kinase1 (CERK1/LysM RLK1) gene, known to play a critical role in signaling defense responses induced by exogenous chitin. Arabidopsis plants overexpressing the endochitinase chit36 and hexoaminidase excy1 genes from the fungus Trichoderma asperelleoides T203 showed increased tolerance to salinity, heavy-metal stresses, and Botrytis cinerea infection. Resistant lines, overexpressing fungal chitinases at different levels, were outcrossed to lysm rlk1 mutants. Independent homozygous hybrids lost resistance to biotic and abiotic stresses, despite enhanced chitinase activity. Expression analysis of 270 stress-related genes, including those induced by reactive oxygen species (ROS) and chitin, revealed constant up-regulation (at least twofold) of 10 genes in the chitinase-overexpressing line and an additional 76 salt-induced genes whose expression was not elevated in the lysm rlk1 knockout mutant or the hybrids harboring the mutation. These findings elucidate that chitin-induced signaling mediated by LysM RLK1 receptor is not limited to biotic stress response but also encompasses abiotic-stress signaling and can be conveyed by ectopic expression of chitinases in plants.
KW  - abiotic stress
KW  - chitin-induced signaling
KW  - chitinases
KW  - LysM receptor kinase
KW  - Trichoderma
Y1  - 2012
U6  - https://doi.org/10.1093/mp/sss021
SN  - 1674-2052
VL  - 5
IS  - 5
SP  - 1113
EP  - 1124
PB  - Oxford Univ. Press
CY  - Oxford
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  - Tabatabaei, Iman
A1  - Alseekh, Saleh
A1  - Shahid, Mohammad
A1  - Leniak, Ewa
A1  - Wagner, Mateusz
A1  - Mahmoudi, Henda
A1  - Thushar, Sumitha
A1  - Fernie, Alisdair R.
A1  - Murphy, Kevin M.
A1  - Schmöckel, Sandra M.
A1  - Tester, Mark
A1  - Müller-Röber, Bernd
A1  - Skirycz, Aleksandra
A1  - Balazadeh, Salma
T1  - The diversity of quinoa morphological traits and seed metabolic composition
JF  - Scientific data
N2  - Quinoa (Chenopodium quinoa Willd.) is an herbaceous annual crop of the amaranth family (Amaranthaceae). It is increasingly cultivated for its nutritious grains, which are rich in protein and essential amino acids, lipids, and minerals. Quinoa exhibits a high tolerance towards various abiotic stresses including drought and salinity, which supports its agricultural cultivation under climate change conditions. The use of quinoa grains is compromised by anti-nutritional saponins, a terpenoid class of secondary metabolites deposited in the seed coat; their removal before consumption requires extensive washing, an economically and environmentally unfavorable process; or their accumulation can be reduced through breeding. In this study, we analyzed the seed metabolomes, including amino acids, fatty acids, and saponins, from 471 quinoa cultivars, including two related species, by liquid chromatography - mass spectrometry. Additionally, we determined a large number of agronomic traits including biomass, flowering time, and seed yield. The results revealed considerable diversity between genotypes and provide a knowledge base for future breeding or genome editing of quinoa.
Y1  - 2022
U6  - https://doi.org/10.1038/s41597-022-01399-y
SN  - 2052-4463
VL  - 9
IS  - 1
PB  - Nature Research
CY  - Berlin
ER  - 
TY  - JOUR
A1  - Lotkowska, Magda E.
A1  - Tohge, Takayuki
A1  - Fernie, Alisdair R.
A1  - Xue, Gang-Ping
A1  - Balazadeh, Salma
A1  - Müller-Röber, Bernd
T1  - The Arabidopsis Transcription Factor MYB112 Promotes Anthocyanin Formation during Salinity and under High Light Stress
JF  - Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants
N2  - MYB transcription factors (TFs) are important regulators of flavonoid biosynthesis in plants. Here, we report MYB112 as a formerly unknown regulator of anthocyanin accumulation in Arabidopsis (Arabidopsis thaliana). Expression profiling after chemically induced overexpression of MYB112 identified 28 up-and 28 down-regulated genes 5 h after inducer treatment, including MYB7 and MYB32, which are both induced. In addition, upon extended induction, MYB112 also positively affects the expression of PRODUCTION OF ANTHOCYANIN PIGMENT1, a key TF of anthocyanin biosynthesis, but acts negatively toward MYB12 and MYB111, which both control flavonol biosynthesis. MYB112 binds to an 8-bp DNA fragment containing the core sequence (A/T/G)(A/C) CC(A/T)(A/G/T)(A/C)(T/C). By electrophoretic mobility shift assay and chromatin immunoprecipitation coupled to quantitative polymerase chain reaction, we show that MYB112 binds in vitro and in vivo to MYB7 and MYB32 promoters, revealing them as direct downstream target genes. We further show that MYB112 expression is up-regulated by salinity and high light stress, environmental parameters that both require the MYB112 TF for anthocyanin accumulation under these stresses. In contrast to several other MYB TFs affecting anthocyanin biosynthesis, MYB112 expression is not controlled by nitrogen limitation or an excess of carbon. Thus, MYB112 constitutes a regulator that promotes anthocyanin accumulation under abiotic stress conditions.
Y1  - 2015
U6  - https://doi.org/10.1104/pp.15.00605
SN  - 0032-0889
SN  - 1532-2548
VL  - 169
IS  - 3
SP  - 1862
EP  - 1880
PB  - American Society of Plant Physiologists
CY  - Rockville
ER  - 
TY  - JOUR
A1  - Machens, Fabian
A1  - Balazadeh, Salma
A1  - Müller-Röber, Bernd
A1  - Messerschmidt, Katrin
T1  - Synthetic Promoters and Transcription Factors for Heterologous Protein Expression in Saccharomyces cerevisiae
JF  - Frontiers in Bioengineering and Biotechnology
N2  - Orthogonal systems for heterologous protein expression as well as for the engineering of synthetic gene regulatory circuits in hosts like Saccharomyces cerevisiae depend on synthetic transcription factors (synTFs) and corresponding cis-regulatory binding sites. We have constructed and characterized a set of synTFs based on either transcription activator-like effectors or CRISPR/Cas9, and corresponding small synthetic promoters (synPs) with minimal sequence identity to the host’s endogenous promoters. The resulting collection of functional synTF/synP pairs confers very low background expression under uninduced conditions, while expression output upon induction of the various synTFs covers a wide range and reaches induction factors of up to 400. The broad spectrum of expression strengths that is achieved will be useful for various experimental setups, e.g., the transcriptional balancing of expression levels within heterologous pathways or the construction of artificial regulatory networks. Furthermore, our analyses reveal simple rules that enable the tuning of synTF expression output, thereby allowing easy modification of a given synTF/synP pair. This will make it easier for researchers to construct tailored transcriptional control systems.
KW  - JUB1
KW  - synthetic biology
KW  - transcriptional regulation
KW  - gene expression
KW  - synthetic circuits
KW  - dead Cas9
KW  - chimeric transcription factors
Y1  - 2017
U6  - https://doi.org/10.3389/fbioe.2017.00063
SN  - 2296-4185
VL  - 5
SP  - 1
EP  - 11
PB  - Frontiers
CY  - Lausanne
ER  - 
TY  - JOUR
A1  - Thirumalaikumar, Venkatesh P.
A1  - Gorka, Michal
A1  - Schulz, Karina
A1  - Masclaux-Daubresse, Celine
A1  - Sampathkumar, Arun
A1  - Skirycz, Aleksandra
A1  - Vierstra, Richard D.
A1  - Balazadeh, Salma
T1  - Selective autophagy regulates heat stress memory in Arabidopsis by NBR1-mediated targeting of HSP90.1 and ROF1
JF  - Autophagy
N2  - In nature, plants are constantly exposed to many transient, but recurring, stresses. Thus, to complete their life cycles, plants require a dynamic balance between capacities to recover following cessation of stress and maintenance of stress memory. Recently, we uncovered a new functional role for macroautophagy/autophagy in regulating recovery from heat stress (HS) and resetting cellular memory of HS inArabidopsis thaliana. Here, we demonstrated that NBR1 (next to BRCA1 gene 1) plays a crucial role as a receptor for selective autophagy during recovery from HS. Immunoblot analysis and confocal microscopy revealed that levels of the NBR1 protein, NBR1-labeled puncta, and NBR1 activity are all higher during the HS recovery phase than before. Co-immunoprecipitation analysis of proteins interacting with NBR1 and comparative proteomic analysis of annbr1-null mutant and wild-type plants identified 58 proteins as potential novel targets of NBR1. Cellular, biochemical and functional genetic studies confirmed that NBR1 interacts with HSP90.1 (heat shock protein 90.1) and ROF1 (rotamase FKBP 1), a member of the FKBP family, and mediates their degradation by autophagy, which represses the response to HS by attenuating the expression ofHSPgenes regulated by the HSFA2 transcription factor. Accordingly, loss-of-function mutation ofNBR1resulted in a stronger HS memory phenotype. Together, our results provide new insights into the mechanistic principles by which autophagy regulates plant response to recurrent HS.
KW  - Arabidopsis thaliana
KW  - heat stress
KW  - HSFA2
KW  - HSP90.1
KW  - NBR1
KW  - ROF1
KW  - selective autophagy
KW  - stress memory
KW  - stress recovery
Y1  - 2020
U6  - https://doi.org/10.1080/15548627.2020.1820778
SN  - 1554-8635
VL  - 17
IS  - 9
SP  - 2184
EP  - 2199
PB  - Taylor & Francis
CY  - Abingdon
ER  - 
TY  - JOUR
A1  - Allu, Annapurna Devi
A1  - Soja, Aleksandra Maria
A1  - Wu, Anhui
A1  - Szymanski, Jedrzej
A1  - Balazadeh, Salma
T1  - Salt stress and senescence: identification of cross-talk regulatory components
JF  - Journal of experimental botany
N2  - Leaf senescence is an active process with a pivotal impact on plant productivity. It results from extensive signalling cross-talk coordinating environmental factors with intrinsic age-related mechanisms. Although many studies have shown that leaf senescence is affected by a range of external parameters, knowledge about the regulatory systems that govern the interplay between developmental programmes and environmental stress is still vague. Salinity is one of the most important environmental stresses that promote leaf senescence and thus affect crop yield. Improving salt tolerance by avoiding or delaying senescence under stress will therefore play an important role in maintaining high agricultural productivity. Experimental evidence suggests that hydrogen peroxide (H2O2) functions as a common signalling molecule in both developmental and salt-induced leaf senescence. In this study, microarray-based gene expression profiling on Arabidopsis thaliana plants subjected to long-term salinity stress to induce leaf senescence was performed, together with co-expression network analysis for H2O2-responsive genes that are mutually up-regulated by salt induced-and developmental leaf senescence. Promoter analysis of tightly co-expressed genes led to the identification of seven cis-regulatory motifs, three of which were known previously, namely CACGTGT and AAGTCAA, which are associated with reactive oxygen species (ROS)-responsive genes, and CCGCGT, described as a stress-responsive regulatory motif, while the others, namely ACGCGGT, AGCMGNC, GMCACGT, and TCSTYGACG were not characterized previously. These motifs are proposed to be novel elements involved in the H2O2-mediated control of gene expression during salinity stress-triggered and developmental senescence, acting through upstream transcription factors that bind to these sites.
KW  - Arabidopsis
KW  - hydrogen peroxide
KW  - longevity
KW  - reactive oxygen species
KW  - salt stress
KW  - senescence
KW  - signal cross-talk
KW  - transcription factor
Y1  - 2014
U6  - https://doi.org/10.1093/jxb/eru173
SN  - 0022-0957
SN  - 1460-2431
VL  - 65
IS  - 14
SP  - 3993
EP  - 4008
PB  - Oxford Univ. Press
CY  - Oxford
ER  - 
TY  - JOUR
A1  - Balazadeh, Salma
A1  - Schildhauer, Joerg
A1  - Araujo, Wagner L.
A1  - Munne-Bosch, Sergi
A1  - Fernie, Alisdair R.
A1  - Proost, Sebastian
A1  - Humbeck, Klaus
A1  - Müller-Röber, Bernd
T1  - Reversal of senescence by N resupply to N-starved Arabidopsis thaliana: transcriptomic and metabolomic consequences
JF  - Journal of experimental botany
N2  - Leaf senescence is a developmentally controlled process, which is additionally modulated by a number of adverse environmental conditions. Nitrogen shortage is a well-known trigger of precocious senescence in many plant species including crops, generally limiting biomass and seed yield. However, leaf senescence induced by nitrogen starvation may be reversed when nitrogen is resupplied at the onset of senescence. Here, the transcriptomic, hormonal, and global metabolic rearrangements occurring during nitrogen resupply-induced reversal of senescence in Arabidopsis thaliana were analysed. The changes induced by senescence were essentially in keeping with those previously described; however, these could, by and large, be reversed. The data thus indicate that plants undergoing senescence retain the capacity to sense and respond to the availability of nitrogen nutrition. The combined data are discussed in the context of the reversibility of the senescence programme and the evolutionary benefit afforded thereby. Future prospects for understanding and manipulating this process in both Arabidopsis and crop plants are postulated.
KW  - Arabidopsis
KW  - gene expression
KW  - metabolomics
KW  - nitrogen limitation
KW  - senescence
KW  - transcriptome
Y1  - 2014
U6  - https://doi.org/10.1093/jxb/eru119
SN  - 0022-0957
SN  - 1460-2431
VL  - 65
IS  - 14
SP  - 3975
EP  - 3992
PB  - Oxford Univ. Press
CY  - Oxford
ER  - 
TY  - JOUR
A1  - Parlitz, Steffi
A1  - Kunze, Reinhard
A1  - Müller-Röber, Bernd
A1  - Balazadeh, Salma
T1  - Regulation of photosynthesis and transcription factor expression by leaf shading and re-illumination in Arabidopsis thaliana leaves
JF  - Journal of plant physiology : biochemistry, physiology, molecular biology and biotechnology of plants
N2  - Leaf senescence of annual plants is a genetically programmed developmental phase. The onset of leaf senescence is however not exclusively determined by tissue age but is modulated by various environmental factors. Shading of individual attached leaves evokes dark-induced senescence. The initiation and progression of dark-induced senescence depend on the plant and the age of the affected leaf, however. In several plant species dark-induced senescence is fully reversible upon re-illumination and the leaves can regreen, but the regreening ability depends on the duration of dark incubation. We studied the ability of Arabidopsis thaliana leaves to regreen after dark-incubation with the aim to identify transcription factors (TFs) that are involved in the regulation of early dark-induced senescence and regreening. Two days shading of individual attached leaves triggers the transition into a pre-senescence state from which the leaves can largely recover. Longer periods of darkness result in irreversible senescence. Large scale qRT-PCR analysis of 1872 TF genes revealed that 649 of them are regulated in leaves during normal development, upon shading or re-illumination. Leaf shading triggered upregulation of 150 TF genes, some of which are involved in controlling senescence. Of those, 39 TF genes were upregulated after two days in the dark and regained pre-shading expression level after two days of re-illumination. Furthermore, a larger number of 422 TF genes were down regulated upon shading. In TF gene clusters with different expression patterns certain TF families are over-represented.
KW  - Arabidopsis thaliana
KW  - Dark-induced senescence
KW  - Expression profiling
KW  - Regreening
KW  - Transcription factor
Y1  - 2011
U6  - https://doi.org/10.1016/j.jplph.2011.02.001
SN  - 0176-1617
VL  - 168
IS  - 12
SP  - 1311
EP  - 1319
PB  - Elsevier
CY  - Jena
ER  - 
TY  - JOUR
A1  - Shubchynskyy, Volodymyr
A1  - Boniecka, Justyna
A1  - Schweighofer, Alois
A1  - Simulis, Justinas
A1  - Kvederaviciute, Kotryna
A1  - Stumpe, Michael
A1  - Mauch, Felix
A1  - Balazadeh, Salma
A1  - Müller-Röber, Bernd
A1  - Boutrot, Freddy
A1  - Zipfel, Cyril
A1  - Meskiene, Irute
T1  - Protein phosphatase AP2C1 negatively regulates basal resistance and defense responses to Pseudomonas syringae
JF  - Journal of experimental botany
N2  - Mitogen-activated protein kinases (MAPKs) mediate plant immune responses to pathogenic bacteria. However, less is known about the cell autonomous negative regulatory mechanism controlling basal plant immunity. We report the biological role of Arabidopsis thaliana MAPK phosphatase AP2C1 as a negative regulator of plant basal resistance and defense responses to Pseudomonas syringae. AP2C2, a closely related MAPK phosphatase, also negatively controls plant resistance. Loss of AP2C1 leads to enhanced pathogen-induced MAPK activities, increased callose deposition in response to pathogen-associated molecular patterns or to P. syringae pv. tomato (Pto) DC3000, and enhanced resistance to bacterial infection with Pto. We also reveal the impact of AP2C1 on the global transcriptional reprogramming of transcription factors during Pto infection. Importantly, ap2c1 plants show salicylic acid-independent transcriptional reprogramming of several defense genes and enhanced ethylene production in response to Pto. This study pinpoints the specificity of MAPK regulation by the different MAPK phosphatases AP2C1 and MKP1, which control the same MAPK substrates, nevertheless leading to different downstream events. We suggest that precise and specific control of defined MAPKs by MAPK phosphatases during plant challenge with pathogenic bacteria can strongly influence plant resistance.
KW  - Callose
KW  - defense genes
KW  - MAPK
KW  - MAPK phosphatase
KW  - PAMP
KW  - PP2C phosphatase
KW  - Pseudomonas syringae
KW  - salicylic acid
KW  - transcription factors
Y1  - 2017
U6  - https://doi.org/10.1093/jxb/erw485
SN  - 0022-0957
SN  - 1460-2431
VL  - 68
IS  - 5
SP  - 1169
EP  - 1183
PB  - Oxford Univ. Press
CY  - Oxford
ER  - 
TY  - JOUR
A1  - Hilker, Monika
A1  - Schwachtje, Jens
A1  - Baier, Margarete
A1  - Balazadeh, Salma
A1  - Bäurle, Isabel
A1  - Geiselhardt, Sven
A1  - Hincha, Dirk K.
A1  - Kunze, Reinhard
A1  - Mueller-Roeber, Bernd
A1  - Rillig, Matthias G.
A1  - Rolff, Jens
A1  - Schmülling, Thomas
A1  - Steppuhn, Anke
A1  - van Dongen, Joost
A1  - Whitcomb, Sarah J.
A1  - Wurst, Susanne
A1  - Zuther, Ellen
A1  - Kopka, Joachim
T1  - Priming and memory of stress responses in organisms lacking a nervous system
JF  - Biological reviews
KW  - priming
KW  - stress signalling
KW  - epigenetics
KW  - memory
KW  - fitness
KW  - stress tolerance
KW  - defence
KW  - bet hedging
Y1  - 2016
U6  - https://doi.org/10.1111/brv.12215
SN  - 1464-7931
SN  - 1469-185X
VL  - 91
SP  - 1118
EP  - 1133
PB  - Wiley-Blackwell
CY  - Hoboken
ER  -