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 - Omidbakhshfard, Mohammad Amin A1 - Fujikura, Ushio A1 - Olas, Justyna Jadwiga A1 - Xue, Gang-Ping A1 - Balazadeh, Salma A1 - Mueller-Roeber, Bernd T1 - GROWTH-REGULATING FACTOR 9 negatively regulates arabidopsis leaf growth by controlling ORG3 and restricting cell proliferation in leaf primordia JF - PLoS Genetics : a peer-reviewed, open-access journal N2 - Leaf growth is a complex process that involves the action of diverse transcription factors (TFs) and their downstream gene regulatory networks. In this study, we focus on the functional characterization of the Arabidopsis thaliana TF GROWTH-REGULATING FACTOR9 (GRF9) and demonstrate that it exerts its negative effect on leaf growth by activating expression of the bZIP TF OBP3-RESPONSIVE GENE 3 (ORG3). While grf9 knockout mutants produce bigger incipient leaf primordia at the shoot apex, rosette leaves and petals than the wild type, the sizes of those organs are reduced in plants overexpressing GRF9 (GRF9ox). Cell measurements demonstrate that changes in leaf size result from alterations in cell numbers rather than cell sizes. Kinematic analysis and 5-ethynyl-2'-deoxyuridine (EdU) incorporation assay revealed that GRF9 restricts cell proliferation in the early developing leaf. Performing in vitro binding site selection, we identified the 6-base motif 5'-CTGACA-3' as the core binding site of GRF9. By global transcriptome profiling, electrophoretic mobility shift assay (EMSA) and chromatin immunoprecipitation (ChIP) we identified ORG3 as a direct downstream, and positively regulated target of GRF9. Genetic analysis of grf9 org3 and GRF9ox org3 double mutants reveals that both transcription factors act in a regulatory cascade to control the final leaf dimensions by restricting cell number in the developing leaf. Y1 - 2018 U6 - https://doi.org/10.1371/journal.pgen.1007484 SN - 1553-7404 VL - 14 IS - 7 PB - PLoS CY - San Fransisco 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 - 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 - 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 - 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 - 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 - Balazadeh, Salma A1 - Kwasniewski, Miroslaw A1 - Caldana, Camila A1 - Mehrnia, Mohammad A1 - Zanor, Maria Ines A1 - Xue, Gang-Ping A1 - Müller-Röber, Bernd T1 - ORS1, an H2O2-Responsive NAC Transcription Factor, Controls Senescence in Arabidopsis thaliana JF - Molecular plant N2 - We report here that ORS1, a previously uncharacterized member of the NAC transcription factor family, controls leaf senescence in Arabidopsis thaliana. Overexpression of ORS1 accelerates senescence in transgenic plants, whereas its inhibition delays it. Genes acting downstream of ORS1 were identified by global expression analysis using transgenic plants producing dexamethasone-inducible ORS1-GR fusion protein. Of the 42 up-regulated genes, 30 (similar to 70%) were previously shown to be up-regulated during age-dependent senescence. We also observed that 32 (similar to 76%) of the ORS1-dependent genes were induced by long-term (4 d), but not short-term (6 h) salinity stress (150 mM NaCl). Furthermore, expression of 16 and 24 genes, respectively, was induced after 1 and 5 h of treatment with hydrogen peroxide (H2O2), a reactive oxygen species known to accumulate during salinity stress. ORS1 itself was found to be rapidly and strongly induced by H2O2 treatment in both leaves and roots. Using in vitro binding site selection, we determined the preferred binding motif of ORS1 and found it to be present in half of the ORS1-dependent genes. ORS1 is a paralog of ORE1/ANAC092/AtNAC2, a previously reported regulator of leaf senescence. Phylogenetic footprinting revealed evolutionary conservation of the ORS1 and ORE1 promoter sequences in different Brassicaceae species, indicating strong positive selection acting on both genes. We conclude that ORS1, similarly to ORE1, triggers expression of senescence-associated genes through a regulatory network that may involve cross-talk with salt- and H2O2-dependent signaling pathways. KW - NAC transcription factor KW - leaf senescence KW - gene expression KW - gene regulatory network KW - hydrogen peroxide Y1 - 2011 U6 - https://doi.org/10.1093/mp/ssq080 SN - 1674-2052 VL - 4 IS - 2 SP - 346 EP - 360 PB - Oxford Univ. Press CY - Oxford ER - TY - JOUR A1 - Wu, Anhui A1 - Allu, Annapurna Devi A1 - Garapati, Prashanth A1 - Siddiqui, Hamad A1 - Dortay, Hakan A1 - Zanor, Maria-Ines A1 - Asensi-Fabado, Maria Amparo A1 - Munne-Bosch, Sergi A1 - Antonio, Carla A1 - Tohge, Takayuki A1 - Fernie, Alisdair R. A1 - Kaufmann, Kerstin A1 - Xue, Gang-Ping A1 - Müller-Röber, Bernd A1 - Balazadeh, Salma T1 - Jungbrunnen1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in arabidopsis JF - The plant cell N2 - The transition from juvenility through maturation to senescence is a complex process that involves the regulation of longevity. Here, we identify JUNGBRUNNEN1 (JUB1), a hydrogen peroxide (H2O2)-induced NAC transcription factor, as a central longevity regulator in Arabidopsis thaliana. JUB1 overexpression strongly delays senescence, dampens intracellular H2O2 levels, and enhances tolerance to various abiotic stresses, whereas in jub1-1 knockdown plants, precocious senescence and lowered abiotic stress tolerance are observed. A JUB1 binding site containing a RRYGCCGT core sequence is present in the promoter of DREB2A, which plays an important role in abiotic stress responses. JUB1 transactivates DREB2A expression in mesophyll cell protoplasts and transgenic plants and binds directly to the DREB2A promoter. Transcriptome profiling of JUB1 overexpressors revealed elevated expression of several reactive oxygen species-responsive genes, including heat shock protein and glutathione S-transferase genes, whose expression is further induced by H2O2 treatment. Metabolite profiling identified elevated Pro and trehalose levels in JUB1 overexpressors, in accordance with their enhanced abiotic stress tolerance. We suggest that JUB1 constitutes a central regulator of a finely tuned control system that modulates cellular H2O2 level and primes the plants for upcoming stress through a gene regulatory network that involves DREB2A. Y1 - 2012 U6 - https://doi.org/10.1105/tpc.111.090894 SN - 1040-4651 VL - 24 IS - 2 SP - 482 EP - 506 PB - American Society of Plant Physiologists CY - Rockville ER - TY - JOUR A1 - Matallana-Ramirez, Lilian P. A1 - Rauf, Mamoona A1 - Farage-Barhom, Sarit A1 - Dortay, Hakan A1 - Xue, Gang-Ping A1 - Droege-Laser, Wolfgang A1 - Lers, Amnon A1 - Balazadeh, Salma A1 - Müller-Röber, Bernd T1 - NAC Transcription Factor ORE1 and Senescence-Induced BIFUNCTIONAL NUCLEASE1 (BFN1) Constitute a Regulatory Cascade in Arabidopsis JF - Molecular plant N2 - The NAC transcription factor ORE1 is a key regulator of senescence in Arabidopsis thaliana. Here, we demonstrate that senescence-induced and cell death-associated BIFUNCTIONAL NUCLEASE1 (BFN1) is a direct downstream target of ORE1, revealing a previously unknown regulatory cascade.Senescence is a highly regulated process that involves the action of a large number of transcription factors. The NAC transcription factor ORE1 (ANAC092) has recently been shown to play a critical role in positively controlling senescence in Arabidopsis thaliana; however, no direct target gene through which it exerts its molecular function has been identified previously. Here, we report that BIFUNCTIONAL NUCLEASE1 (BFN1), a well-known senescence-enhanced gene, is directly regulated by ORE1. We detected elevated expression of BFN1 already 2 h after induction of ORE1 in estradiol-inducible ORE1 overexpression lines and 6 h after transfection of Arabidopsis mesophyll cell protoplasts with a 35S:ORE1 construct. ORE1 and BFN1 expression patterns largely overlap, as shown by promoterreporter gene (GUS) fusions, while BFN1 expression in senescent leaves and the abscission zones of maturing flower organs was virtually absent in ore1 mutant background. In vitro binding site assays revealed a bipartite ORE1 binding site, similar to that of ORS1, a paralog of ORE1. A bipartite ORE1 binding site was identified in the BFN1 promoter; mutating the cis-element within the context of the full-length BFN1 promoter drastically reduced ORE1-mediated transactivation capacity in transiently transfected Arabidopsis mesophyll cell protoplasts. Furthermore, chromatin immunoprecipitation (ChIP) demonstrates in vivo binding of ORE1 to the BFN1 promoter. We also demonstrate binding of ORE1 in vivo to the promoters of two other senescence-associated genes, namely SAG29/SWEET15 and SINA1, supporting the central role of ORE1 during senescence. KW - Arabidopsis thaliana KW - senescence KW - transcription factor KW - ORE1 KW - BFN1 KW - promoter Y1 - 2013 U6 - https://doi.org/10.1093/mp/sst012 SN - 1674-2052 VL - 6 IS - 5 SP - 1438 EP - 1452 PB - Oxford Univ. Press CY - Oxford ER -