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
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  - GEN
A1  - Ma, Xuemin
A1  - Zhang, Youjun
A1  - Turečková, Veronika
A1  - Xue, Gang-Ping
A1  - Fernie, Alisdair
A1  - Müller-Röber, Bernd
A1  - Balazadeh, Salma
T1  - The NAC transcription factor SlNAP2 regulates leaf senescence and fruit yield in tomato
T2  - Postprints der Universität Potsdam Mathematisch-Naturwissenschaftliche Reihe
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.
T3  - Zweitveröffentlichungen der Universität Potsdam : Mathematisch-Naturwissenschaftliche Reihe - 787 
KW  - abscisic-acid
KW  - arabidopsis-thaliana
KW  - chlorophyll degradation
KW  - aba biosynthesis
KW  - oryza-sativa
KW  - rice leaves
KW  - genes
KW  - expression
KW  - metabolism
KW  - protein
Y1  - 2019
U6  - http://nbn-resolving.de/urn/resolver.pl?urn:nbn:de:kobv:517-opus4-437643
SN  - 1866-8372
IS  - 787
ER  - 
TY  - JOUR
A1  - Ma, Xuemin
A1  - Zhang, Youjun
A1  - Tureckova, Veronika
A1  - Xue, Gang-Ping
A1  - Fernie, Alisdair
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  -