@article{AlluBrotmanXueetal.2016,
  author    = {Allu, Annapurna Devi and Brotman, Yariv and Xue, Gang-Ping and Balazadeh, Salma},
  title     = {Transcription factor ANAC032 modulates JA/SA signalling in response to Pseudomonas syringae infection},
  series = {EMBO reports},
  volume    = {17},
  journal   = {EMBO reports},
  publisher = {Wiley-Blackwell},
  address   = {Hoboken},
  issn      = {1469-221X},
  doi       = {10.15252/embr.201642197},
  pages     = {1578 -- 1589},
  year      = {2016},
  abstract  = {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.},
  language  = {en}
}
@article{AlluSimancasBalazadehetal.2017,
  author    = {Allu, Annapurna Devi and Simancas, Barbara and Balazadeh, Salma and Munne-Bosch, Sergi},
  title     = {Defense-Related Transcriptional Reprogramming in Vitamin E-Deficient Arabidopsis Mutants Exposed to Contrasting Phosphate Availability},
  series = {Frontiers in plant science},
  volume    = {8},
  journal   = {Frontiers in plant science},
  publisher = {Frontiers Research Foundation},
  address   = {Lausanne},
  issn      = {1664-462X},
  doi       = {10.3389/fpls.2017.01396},
  pages     = {20},
  year      = {2017},
  abstract  = {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.},
  language  = {en}
}
@article{AlluSojaWuetal.2014,
  author    = {Allu, Annapurna Devi and Soja, Aleksandra Maria and Wu, Anhui and Szymanski, Jedrzej and Balazadeh, Salma},
  title     = {Salt stress and senescence: identification of cross-talk regulatory components},
  series = {Journal of experimental botany},
  volume    = {65},
  journal   = {Journal of experimental botany},
  number    = {14},
  publisher = {Oxford Univ. Press},
  address   = {Oxford},
  issn      = {0022-0957},
  doi       = {10.1093/jxb/eru173},
  pages     = {3993 -- 4008},
  year      = {2014},
  abstract  = {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.},
  language  = {en}
}
@phdthesis{Balazadeh2008,
  author    = {Balazadeh, Salma},
  title     = {Molecular and physiological analysis of leaf senescence in Arabidopsis thaliana},
  pages     = {VI, 169 S.},
  year      = {2008},
  language  = {en}
}
@unpublished{Balazadeh2014,
  author    = {Balazadeh, Salma},
  title     = {Stay-green not always stays green},
  series = {Molecular plant},
  volume    = {7},
  journal   = {Molecular plant},
  number    = {8},
  publisher = {Cell Press},
  address   = {Cambridge},
  issn      = {1674-2052},
  doi       = {10.1093/mp/ssu076},
  pages     = {1264 -- 1266},
  year      = {2014},
  language  = {en}
}
@phdthesis{Balazadeh2015,
  author    = {Balazadeh, Salma},
  title     = {New insights into the molecular mechanisms of leaf senescence},
  school      = {Universit{\"a}t Potsdam},
  year      = {2015},
  language  = {en}
}
@article{BalazadehJaspertArifetal.2012,
  author    = {Balazadeh, Salma and Jaspert, Nils and Arif, Muhammad and M{\"u}ller-R{\"o}ber, Bernd and Maurino, Veronica G.},
  title     = {Expression of ROS-responsive genes and transcription factors after metabolic formation of H2O2 in chloroplasts},
  series = {Frontiers in plant science},
  volume    = {3},
  journal   = {Frontiers in plant science},
  publisher = {Frontiers Research Foundation},
  address   = {Lausanne},
  issn      = {1664-462X},
  doi       = {10.3389/fpls.2012.00234},
  pages     = {30},
  year      = {2012},
  abstract  = {Glycolate oxidase (GO) catalyses the oxidation of glycolate to glyoxylate, thereby consuming O-2 and producing H2O2. In this work, Arabidopsis thaliana plants expressing GO in the chloroplasts (GO plants) were used to assess the expressional behavior of reactive oxygen species (ROS)-responsive genes and transcription factors (TFs) after metabolic induction of H2O2 formation in chloroplasts. In this organelle, GO uses the glycolate derived from the oxygenase activity of RubisCO. Here, to identify genes responding to an abrupt production of H2O2 in chloroplasts we used quantitative real-time PCR (qRT-PCR) to test the expression of 187 ROS-responsive genes and 1880 TFs after transferring GO and wild-type (WT) plants grown at high CO2 levels to ambient CO2 concentration. Our data revealed coordinated expression changes of genes of specific functional networks 0.5 h after metabolic induction of H2O2 production in GO plants, including the induction of indole glucosinolate and camalexin biosynthesis genes. Comparative analysis using available microarray data suggests that signals for the induction of these genes through H2O2 may originate in the chloroplast. The TF profiling indicated an up-regulation in GO plants of a group of genes involved in the regulation of proanthocyanidin and anthocyanin biosynthesis. Moreover, the upregulation of expression of IF and IF interacting proteins affecting development (e.g., cell division, stem branching, flowering time, flower development) would impact growth and reproductive capacity, resulting in altered development under conditions that promote the formation of H2O2.},
  language  = {en}
}
@article{BalazadehKwasniewskiCaldanaetal.2011,
  author    = {Balazadeh, Salma and Kwasniewski, Miroslaw and Caldana, Camila and Mehrnia, Mohammad and Zanor, Maria Ines and Xue, Gang-Ping and M{\"u}ller-R{\"o}ber, Bernd},
  title     = {ORS1, an H2O2-Responsive NAC Transcription Factor, Controls Senescence in Arabidopsis thaliana},
  series = {Molecular plant},
  volume    = {4},
  journal   = {Molecular plant},
  number    = {2},
  publisher = {Oxford Univ. Press},
  address   = {Oxford},
  issn      = {1674-2052},
  doi       = {10.1093/mp/ssq080},
  pages     = {346 -- 360},
  year      = {2011},
  abstract  = {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.},
  language  = {en}
}
@misc{BalazadehMuellerRoeber2018,
  author    = {Balazadeh, Salma and M{\"u}ller-R{\"o}ber, Bernd},
  title     = {A balance to death},
  series = {Nature plants},
  volume    = {4},
  journal   = {Nature plants},
  number    = {11},
  publisher = {Nature Publ. Group},
  address   = {London},
  issn      = {2055-026X},
  doi       = {10.1038/s41477-018-0279-6},
  pages     = {863 -- 864},
  year      = {2018},
  abstract  = {Leaf senescence plays a crucial role in nutrient recovery in late-stage plant development and requires vast transcriptional reprogramming by transcription factors such as ORESARA1 (ORE1). A proteolytic mechanism is now found to control ORE1 degradation, and thus senescence, during nitrogen starvation.},
  language  = {en}
}
@article{BalazadehSchildhauerAraujoetal.2014,
  author    = {Balazadeh, Salma and Schildhauer, Joerg and Araujo, Wagner L. and Munne-Bosch, Sergi and Fernie, Alisdair R. and Proost, Sebastian and Humbeck, Klaus and M{\"u}ller-R{\"o}ber, Bernd},
  title     = {Reversal of senescence by N resupply to N-starved Arabidopsis thaliana: transcriptomic and metabolomic consequences},
  series = {Journal of experimental botany},
  volume    = {65},
  journal   = {Journal of experimental botany},
  number    = {14},
  publisher = {Oxford Univ. Press},
  address   = {Oxford},
  issn      = {0022-0957},
  doi       = {10.1093/jxb/eru119},
  pages     = {3975 -- 3992},
  year      = {2014},
  abstract  = {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.},
  language  = {en}
}
@article{BalazadehSiddiquiAlluetal.2010,
  author    = {Balazadeh, Salma and Siddiqui, Hamad and Allu, Annapurna Devi and Matallana-Ramirez, Lilian Paola and Caldana, Camila and Mehrnia, Mohammad and Zanor, Maria-In{\´e}s and Koehler, Barbara and M{\"u}ller-R{\"o}ber, Bernd},
  title     = {A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence},
  issn      = {0960-7412},
  doi       = {10.1111/j.1365-313X.2010.04151.x},
  year      = {2010},
  abstract  = {P>The onset and progression of senescence are under genetic and environmental control. The Arabidopsis thaliana NAC transcription factor ANAC092 (also called AtNAC2 and ORE1) has recently been shown to control age-dependent senescence, but its mode of action has not been analysed yet. To explore the regulatory network administered by ANAC092 we performed microarray-based expression profiling using estradiol-inducible ANAC092 overexpression lines. Approximately 46\% of the 170 genes up-regulated upon ANAC092 induction are known senescence-associated genes, suggesting that the NAC factor exerts its role in senescence through a regulatory network that includes many of the genes previously reported to be senescence regulated. We selected 39 candidate genes and confirmed their time-dependent response to enhanced ANAC092 expression by quantitative RT-PCR. We also found that the majority of them (24 genes) are up-regulated by salt stress, a major promoter of plant senescence, in a manner similar to that of ANAC092, which itself is salt responsive. Furthermore, 24 genes like ANAC092 turned out to be stage-dependently expressed during seed growth with low expression at early and elevated expression at late stages of seed development. Disruption of ANAC092 increased the rate of seed germination under saline conditions, whereas the opposite occurred in respective overexpression plants. We also detected a delay of salinity-induced chlorophyll loss in detached anac092-1 mutant leaves. Promoter-reporter (GUS) studies revealed transcriptional control of ANAC092 expression during leaf and flower ageing and in response to salt stress. We conclude that ANAC092 exerts its functions during senescence and seed germination through partly overlapping target gene sets.},
  language  = {en}
}
@article{BrotmanLandauPninietal.2012,
  author    = {Brotman, Yariv and Landau, Udi and Pnini, Smadar and Lisec, Jan and Balazadeh, Salma and M{\"u}ller-R{\"o}ber, Bernd and Zilberstein, Aviah and Willmitzer, Lothar and Chet, Ilan and Viterbo, Ada},
  title     = {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},
  series = {Molecular plant},
  volume    = {5},
  journal   = {Molecular plant},
  number    = {5},
  publisher = {Oxford Univ. Press},
  address   = {Oxford},
  issn      = {1674-2052},
  doi       = {10.1093/mp/sss021},
  pages     = {1113 -- 1124},
  year      = {2012},
  abstract  = {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.},
  language  = {en}
}
@article{CzarnockaVanDerKelenWillemsetal.2017,
  author    = {Czarnocka, Weronika and Van Der Kelen, Katrien and Willems, Patrick and Szechynska-Hebda, Magdalena and Shahnejat-Bushehri, Sara and Balazadeh, Salma and Rusaczonek, Anna and M{\"u}ller-R{\"o}ber, Bernd and Van Breusegem, Frank and Karpinski, Stanislaw},
  title     = {The dual role of LESION SIMULATING DISEASE 1 as a condition-dependent scaffold protein and transcription regulator},
  series = {Plant, cell \& environment : cell physiology, whole-plant physiology, community physiology},
  volume    = {40},
  journal   = {Plant, cell \& environment : cell physiology, whole-plant physiology, community physiology},
  publisher = {Wiley},
  address   = {Hoboken},
  issn      = {0140-7791},
  doi       = {10.1111/pce.12994},
  pages     = {2644 -- 2662},
  year      = {2017},
  abstract  = {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.},
  language  = {en}
}
@article{DevkarThirumalaikumarXueetal.2019,
  author    = {Devkar, Vikas and Thirumalaikumar, Venkatesh P. and Xue, Gang-Ping and Vallarino, Jose G. and Tureckova, Veronika and Strnad, Miroslav and Fernie, Alisdair R. and Hoefgen, Rainer and Mueller-Roeber, Bernd and Balazadeh, Salma},
  title     = {Multifaceted regulatory function of tomato SlTAF1 in the response to salinity stress},
  series = {New phytologist : international journal of plant science},
  volume    = {225},
  journal   = {New phytologist : international journal of plant science},
  number    = {4},
  publisher = {Wiley},
  address   = {Hoboken},
  issn      = {0028-646X},
  doi       = {10.1111/nph.16247},
  pages     = {1681 -- 1698},
  year      = {2019},
  abstract  = {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.},
  language  = {en}
}
@article{EbrahimianMotlaghRiboneThirumalaikumaretal.2017,
  author    = {Ebrahimian-Motlagh, Saghar and Ribone, Pamela A. and Thirumalaikumar, Venkatesh P. and Allu, Annapurna Devi and Chan, Raquel L. and Mueller-Roeber, Bernd and Balazadeh, Salma},
  title     = {JUNGBRUNNEN1 Confers Drought Tolerance Downstream of the HD-Zip I Transcription Factor AtHB13},
  series = {Frontiers in plant science},
  volume    = {8},
  journal   = {Frontiers in plant science},
  publisher = {Frontiers Research Foundation},
  address   = {Lausanne},
  issn      = {1664-462X},
  doi       = {10.3389/fpls.2017.02118},
  pages     = {12},
  year      = {2017},
  abstract  = {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.},
  language  = {en}
}
@article{EngqvistSchmitzGertzmannetal.2015,
  author    = {Engqvist, Martin K. M. and Schmitz, Jessica and Gertzmann, Anke and Florian, Alexandra and Jaspert, Nils and Arif, Muhammad and Balazadeh, Salma and M{\"u}ller-R{\"o}ber, Bernd and Fernie, Alisdair R. and Maurino, Veronica G.},
  title     = {GLYCOLATE OXIDASE3, a Glycolate Oxidase Homolog of Yeast L-Lactate Cytochrome c Oxidoreductase, Supports L-Lactate Oxidation in Roots of Arabidopsis},
  series = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants},
  volume    = {169},
  journal   = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants},
  number    = {2},
  publisher = {American Society of Plant Physiologists},
  address   = {Rockville},
  issn      = {0032-0889},
  doi       = {10.1104/pp.15.01003},
  pages     = {1042 -- 1061},
  year      = {2015},
  abstract  = {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.},
  language  = {en}
}
@article{GarapatiFeilLunnetal.2015,
  author    = {Garapati, Prashanth and Feil, Regina and Lunn, John Edward and Van Dijck, Patrick and Balazadeh, Salma and M{\"u}ller-R{\"o}ber, Bernd},
  title     = {Transcription Factor Arabidopsis Activating Factor1 Integrates Carbon Starvation Responses with Trehalose Metabolism},
  series = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants},
  volume    = {169},
  journal   = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants},
  number    = {1},
  publisher = {American Society of Plant Physiologists},
  address   = {Rockville},
  issn      = {0032-0889},
  doi       = {10.1104/pp.15.00917},
  pages     = {379 -- 390},
  year      = {2015},
  abstract  = {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.},
  language  = {en}
}
@article{GarapatiXueMunneBoschetal.2015,
  author    = {Garapati, Prashanth and Xue, Gang-Ping and Munne-Bosch, Sergi and Balazadeh, Salma},
  title     = {Transcription Factor ATAF1 in Arabidopsis Promotes Senescence by Direct Regulation of Key Chloroplast Maintenance and Senescence Transcriptional Cascades},
  series = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants},
  volume    = {168},
  journal   = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants},
  number    = {3},
  publisher = {American Society of Plant Physiologists},
  address   = {Rockville},
  issn      = {0032-0889},
  doi       = {10.1104/pp.15.00567},
  pages     = {1122 -- +},
  year      = {2015},
  abstract  = {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.},
  language  = {en}
}
@article{GliwickaBalazadehCaldanaetal.2009,
  author    = {Gliwicka, Marta and Balazadeh, Salma and Caldana, Camila and M{\"u}ller-R{\"o}ber, Bernd and Gaj, Malgorzata D.},
  title     = {The use of multi-qPCR platform and tan1 mutant in identification of TF genes involved in somatic embryogenesis in Arabidopsis},
  issn      = {0001-5296},
  year      = {2009},
  language  = {en}
}
@article{GliwickaNowakBalazadehetal.2013,
  author    = {Gliwicka, Marta and Nowak, Katarzyna and Balazadeh, Salma and M{\"u}ller-R{\"o}ber, Bernd and Gaj, Malgorzata D.},
  title     = {Extensive Modulation of the Transcription Factor Transcriptome during Somatic Embryogenesis in Arabidopsis thaliana},
  series = {PLoS one},
  volume    = {8},
  journal   = {PLoS one},
  number    = {7},
  publisher = {PLoS},
  address   = {San Fransisco},
  issn      = {1932-6203},
  doi       = {10.1371/journal.pone.0069261},
  pages     = {20},
  year      = {2013},
  abstract  = {Molecular mechanisms controlling plant totipotency are largely unknown and studies on somatic embryogenesis (SE), the process through which already differentiated cells reverse their developmental program and become embryogenic, provide a unique means for deciphering molecular mechanisms controlling developmental plasticity of somatic cells. Among various factors essential for embryogenic transition of somatic cells transcription factors (TFs), crucial regulators of genetic programs, are believed to play a central role. Herein, we used quantitative real-time polymerase chain reaction (qRT-PCR) to identify TF genes affected during SE induced by in vitro culture in Arabidopsis thaliana. Expression profiles of 1,880 TFs were evaluated in the highly embryogenic Col-0 accession and the non-embryogenic tanmei/emb2757 mutant. Our study revealed 729 TFs whose expression changes during the 10-days incubation period of SE; 141 TFs displayed distinct differences in expression patterns in embryogenic versus non-embryogenic cultures. The embryo-induction stage of SE occurring during the first 5 days of culture was associated with a robust and dramatic change of the TF transcriptome characterized by the drastic up-regulation of the expression of a great majority (over 80\%) of the TFs active during embryogenic culture. In contrast to SE induction, the advanced stage of embryo formation showed attenuation and stabilization of transcript levels of many TFs. In total, 519 of the SE-modulated TFs were functionally annotated and transcripts related with plant development, phytohormones and stress responses were found to be most abundant. The involvement of selected TFs in SE was verified using T-DNA insertion lines and a significantly reduced embryogenic response was found for the majority of them. This study provides comprehensive data focused on the expression of TF genes during SE and suggests directions for further research on functional genomics of SE.},
  language  = {en}
}