TY  - JOUR
A1  - Devkar, Vikas
A1  - Thirumalaikumar, Venkatesh P.
A1  - Xue, Gang-Ping
A1  - Vallarino, Jose G.
A1  - Tureckova, Veronika
A1  - Strnad, Miroslav
A1  - Fernie, Alisdair R.
A1  - Hoefgen, Rainer
A1  - Mueller-Roeber, Bernd
A1  - Balazadeh, Salma
T1  - Multifaceted regulatory function of tomato SlTAF1 in the response to salinity stress
JF  - New phytologist : international journal of plant science
N2  - Salinity stress limits plant growth and has a major impact on agricultural productivity. Here, we identify NAC transcription factor SlTAF1 as a regulator of salt tolerance in cultivated tomato (Solanum lycopersicum).
While overexpression of SlTAF1 improves salinity tolerance compared with wild-type, lowering SlTAF1 expression causes stronger salinity-induced damage. Under salt stress, shoots of SlTAF1 knockdown plants accumulate more toxic Na+ ions, while SlTAF1 overexpressors accumulate less ions, in accordance with an altered expression of the Na+ transporter genes SlHKT1;1 and SlHKT1;2. Furthermore, stomatal conductance and pore area are increased in SlTAF1 knockdown plants during salinity stress, but decreased in SlTAF1 overexpressors.
We identified stress-related transcription factor, abscisic acid metabolism and defence-related genes as potential direct targets of SlTAF1, correlating it with reactive oxygen species scavenging capacity and changes in hormonal response. Salinity-induced changes in tricarboxylic acid cycle intermediates and amino acids are more pronounced in SlTAF1 knockdown than wild-type plants, but less so in SlTAF1 overexpressors. The osmoprotectant proline accumulates more in SlTAF1 overexpressors than knockdown plants.
In summary, SlTAF1 controls the tomato’s response to salinity stress by combating both osmotic stress and ion toxicity, highlighting this gene as a promising candidate for the future breeding of stress-tolerant crops.
KW  - abscisic acid (ABA)
KW  - ion homeostasis
KW  - NAC
KW  - proline
KW  - salt stress
KW  - SlTAF1
KW  - transcription factors
Y1  - 2019
U6  - https://doi.org/10.1111/nph.16247
SN  - 0028-646X
SN  - 1469-8137
VL  - 225
IS  - 4
SP  - 1681
EP  - 1698
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  - 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  - Allu, Annapurna Devi
A1  - Simancas, Barbara
A1  - Balazadeh, Salma
A1  - Munne-Bosch, Sergi
T1  - Defense-Related Transcriptional Reprogramming in Vitamin E-Deficient Arabidopsis Mutants Exposed to Contrasting Phosphate Availability
JF  - Frontiers in plant science
N2  - 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.
KW  - antioxidants
KW  - photosystem II
KW  - plastochromanol-8
KW  - priming
KW  - retrograde signaling
KW  - tocochromanols
KW  - vitamin E
Y1  - 2017
U6  - https://doi.org/10.3389/fpls.2017.01396
SN  - 1664-462X
VL  - 8
PB  - Frontiers Research Foundation
CY  - Lausanne
ER  - 
TY  - JOUR
A1  - Naseri, Gita
A1  - Balazadeh, Salma
A1  - Machens, Fabian
A1  - Kamranfar, Iman
A1  - Messerschmidt, Katrin
A1  - Müller-Röber, Bernd
T1  - Plant-Derived Transcription Factors for Orthologous Regulation of Gene Expression in the Yeast Saccharomyces cerevisiae
JF  - ACS synthetic biology
N2  - Control of gene expression by transcription factors (TFs) is central in many synthetic biology projects for which a tailored expression of one or multiple genes is often needed. As TFs from evolutionary distant organisms are unlikely to affect gene expression in a host of choice, they represent excellent candidates for establishing orthogonal control systems. To establish orthogonal regulators for use in yeast (Saccharomyces cerevisiae), we chose TFs from the plant Arabidopsis thaliana. We established a library of 106 different combinations of chromosomally integrated TFs, activation domains (yeast GAL4 AD, herpes simplex virus VP64, and plant EDLL) and synthetic promoters harboring cognate cis regulatory motifs driving a yEGFP reporter. Transcriptional output of the different driver/reporter combinations varied over a wide spectrum, with EDLL being a considerably stronger transcription activation domain in yeast than the GAL4 activation domain, in particular when fused to Arabidopsis NAC TFs. Notably, the strength of several NAC-EDLL fusions exceeded that of the strong yeast TDH3 promoter by 6- to 10-fold. We furthermore show that plant TFs can be used to build regulatory systems encoded by centromeric or episomal plasmids. Our library of TF-DNA binding site combinations offers an excellent tool for diverse synthetic biology applications in yeast.
KW  - Arabidopsis thaliana
KW  - artificial transcription factor
KW  - NAC transcription factor
KW  - synthetic biology
KW  - plant
Y1  - 2017
U6  - https://doi.org/10.1021/acssynbio.7b00094
SN  - 2161-5063
VL  - 6
SP  - 1742
EP  - 1756
PB  - American Chemical Society
CY  - Washington
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  - 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  - 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  - 
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  - 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  - 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  - 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  - Engqvist, Martin K. M.
A1  - Schmitz, Jessica
A1  - Gertzmann, Anke
A1  - Florian, Alexandra
A1  - Jaspert, Nils
A1  - Arif, Muhammad
A1  - Balazadeh, Salma
A1  - Müller-Röber, Bernd
A1  - Fernie, Alisdair R.
A1  - Maurino, Veronica G.
T1  - GLYCOLATE OXIDASE3, a Glycolate Oxidase Homolog of Yeast L-Lactate Cytochrome c Oxidoreductase, Supports L-Lactate Oxidation in Roots of Arabidopsis
JF  - Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants
N2  - In roots of Arabidopsis (Arabidopsis thaliana), L-lactate is generated by the reduction of pyruvate via L-lactate dehydrogenase, but this enzyme does not efficiently catalyze the reverse reaction. Here, we identify the Arabidopsis glycolate oxidase (GOX) paralogs GOX1, GOX2, and GOX3 as putative L-lactate-metabolizing enzymes based on their homology to CYB2, the L-lactate cytochrome c oxidoreductase from the yeast Saccharomyces cerevisiae. We found that GOX3 uses L-lactate with a similar efficiency to glycolate; in contrast, the photorespiratory isoforms GOX1 and GOX2, which share similar enzymatic properties, use glycolate with much higher efficiencies than L-lactate. The key factor making GOX3 more efficient with L-lactate than GOX1 and GOX2 is a 5- to 10-fold lower Km for the substrate. Consequently, only GOX3 can efficiently metabolize L-lactate at low intracellular concentrations. Isotope tracer experiments as well as substrate toxicity tests using GOX3 loss-of-function and overexpressor plants indicate that L-lactate is metabolized in vivo by GOX3. Moreover, GOX3 rescues the lethal growth phenotype of a yeast strain lacking CYB2, which cannot grow on L-lactate as a sole carbon source. GOX3 is predominantly present in roots and mature to aging leaves but is largely absent from young photosynthetic leaves, indicating that it plays a role predominantly in heterotrophic rather than autotrophic tissues, at least under standard growth conditions. In roots of plants grown under normoxic conditions, loss of function of GOX3 induces metabolic rearrangements that mirror wild-type responses under hypoxia. Thus, we identified GOX3 as the enzyme that metabolizes L-lactate to pyruvate in vivo and hypothesize that it may ensure the sustainment of low levels of L-lactate after its formation under normoxia.
Y1  - 2015
U6  - https://doi.org/10.1104/pp.15.01003
SN  - 0032-0889
SN  - 1532-2548
VL  - 169
IS  - 2
SP  - 1042
EP  - 1061
PB  - American Society of Plant Physiologists
CY  - Rockville
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  - Pajoro, Alice
A1  - Madrigal, Pedro
A1  - Muino, Jose M.
A1  - Tomas Matus, Jose
A1  - Jin, Jian
A1  - Mecchia, Martin A.
A1  - Debernardi, Juan M.
A1  - Palatnik, Javier F.
A1  - Balazadeh, Salma
A1  - Arif, Muhammad
A1  - Wellmer, Frank
A1  - Krajewski, Pawel
A1  - Riechmann, Jose-Luis
A1  - Angenent, Gerco C.
A1  - Kaufmann, Kerstin
T1  - Dynamics of chromatin accessibility and gene regulation by MADS-domain transcription factors in flower development
JF  - Genome biology : biology for the post-genomic era
N2  - Background: Development of eukaryotic organisms is controlled by transcription factors that trigger specific and global changes in gene expression programs. In plants, MADS-domain transcription factors act as master regulators of developmental switches and organ specification. However, the mechanisms by which these factors dynamically regulate the expression of their target genes at different developmental stages are still poorly understood.
 Results: We characterized the relationship of chromatin accessibility, gene expression, and DNA binding of two MADS-domain proteins at different stages of Arabidopsis flower development. Dynamic changes in APETALA1 and SEPALLATA3 DNA binding correlated with changes in gene expression, and many of the target genes could be associated with the developmental stage in which they are transcriptionally controlled. We also observe dynamic changes in chromatin accessibility during flower development. Remarkably, DNA binding of APETALA1 and SEPALLATA3 is largely independent of the accessibility status of their binding regions and it can precede increases in DNA accessibility. These results suggest that APETALA1 and SEPALLATA3 may modulate chromatin accessibility, thereby facilitating access of other transcriptional regulators to their target genes.
 Conclusions: Our findings indicate that different homeotic factors regulate partly overlapping, yet also distinctive sets of target genes in a partly stage-specific fashion. By combining the information from DNA-binding and gene expression data, we are able to propose models of stage-specific regulatory interactions, thereby addressing dynamics of regulatory networks throughout flower development. Furthermore, MADS-domain TFs may regulate gene expression by alternative strategies, one of which is modulation of chromatin accessibility.
KW  - Flower Development
KW  - Floral Organ
KW  - Floral Meristem
KW  - Chromatin Accessibility
KW  - Growth Regulate Factor
Y1  - 2014
U6  - https://doi.org/10.1186/gb-2014-15-3-r41
SN  - 1465-6906
SN  - 1474-760X
VL  - 15
PB  - BioMed Central
CY  - London
ER  - 
TY  - JOUR
A1  - Müller-Röber, Bernd
A1  - Balazadeh, Salma
T1  - Auxin and its role in plant senescence
JF  - Journal of plant growth regulation
N2  - Leaf senescence represents a key developmental process through which resources trapped in the photosynthetic organ are degraded in an organized manner and transported away to sustain the growth of other organs including newly forming leaves, roots, seeds, and fruits. The optimal timing of the initiation and progression of senescence are thus prerequisites for controlled plant growth, biomass accumulation, and evolutionary success through seed dispersal. Recent research has uncovered a multitude of regulatory factors including transcription factors, micro-RNAs, protein kinases, and others that constitute the molecular networks that regulate senescence in plants. The timing of senescence is affected by environmental conditions and abiotic or biotic stresses typically trigger a faster senescence. Various phytohormones, including for example ethylene, abscisic acid, and salicylic acid, promote senescence, whereas cytokinins delay it. Recently, several reports have indicated an involvement of auxin in the control of senescence, however, its mode of action and point of interference with senescence control mechanisms remain vaguely defined at present and contrasting observations regarding the effect of auxin on senescence have so far hindered the establishment of a coherent model. Here, we summarize recent studies on auxin-related genes that affect senescence in plants and highlight how these findings might be integrated into current molecular-regulatory models of senescence.
KW  - ARF
KW  - Auxin
KW  - Chloroplast
KW  - Development
KW  - Leaf
KW  - SAUR
KW  - Senescence
KW  - Signaling
KW  - Transcription factor
KW  - YUCCA
Y1  - 2014
U6  - https://doi.org/10.1007/s00344-013-9398-5
SN  - 0721-7595
SN  - 1435-8107
VL  - 33
IS  - 1
SP  - 21
EP  - 33
PB  - Springer
CY  - New York
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  -