@article{SchmidtMieuletHubbertenetal.2013, author = {Schmidt, Romy and Mieulet, Delphine and Hubberten, Hans-Michael and Obata, Toshihiro and H{\"o}fgen, Rainer and Fernie, Alisdair and Fisahn, Joachim and Segundo, Blanca San and Guiderdoni, Emmanuel and Schippers, Jos H. M. and M{\"u}ller-R{\"o}ber, Bernd}, title = {Salt-responsive ERF1 regulates reactive oxygen species-dependent signaling during the initial response to salt stress in rice}, series = {The plant cell}, volume = {25}, journal = {The plant cell}, number = {6}, publisher = {American Society of Plant Physiologists}, address = {Rockville}, issn = {1040-4651}, doi = {10.1105/tpc.113.113068}, pages = {2115 -- 2131}, year = {2013}, abstract = {Early detection of salt stress is vital for plant survival and growth. Still, the molecular processes controlling early salt stress perception and signaling are not fully understood. Here, we identified SALT-RESPONSIVE ERF1 (SERF1), a rice (Oryza sativa) transcription factor (TF) gene that shows a root-specific induction upon salt and hydrogen peroxide (H2O2) treatment. Loss of SERF1 impairs the salt-inducible expression of genes encoding members of a mitogen-activated protein kinase (MAPK) cascade and salt tolerance-mediating TFs. Furthermore, we show that SERF1-dependent genes are H2O2 responsive and demonstrate that SERF1 binds to the promoters of MAPK KINASE KINASE6 (MAP3K6), MAPK5, DEHYDRATION-RESPONSIVE ELEMENT BINDING2A (DREB2A), and ZINC FINGER PROTEIN179 (ZFP179) in vitro and in vivo. SERF1 also directly induces its own gene expression. In addition, SERF1 is a phosphorylation target of MAPK5, resulting in enhanced transcriptional activity of SERF1 toward its direct target genes. In agreement, plants deficient for SERF1 are more sensitive to salt stress compared with the wild type, while constitutive overexpression of SERF1 improves salinity tolerance. We propose that SERF1 amplifies the reactive oxygen species-activated MAPK cascade signal during the initial phase of salt stress and translates the salt-induced signal into an appropriate expressional response resulting in salt tolerance.}, language = {en} } @article{WatanabeBalazadehTohgeetal.2013, author = {Watanabe, Mutsumi and Balazadeh, Salma and Tohge, Takayuki and Erban, Alexander and Giavalisco, Patrick and Kopka, Joachim and M{\"u}ller-R{\"o}ber, Bernd and Fernie, Alisdair and H{\"o}fgen, Rainer}, title = {Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in arabidopsis}, series = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants}, volume = {162}, 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.113.217380}, pages = {1290 -- 1310}, year = {2013}, abstract = {Developmental senescence is a coordinated physiological process in plants and is critical for nutrient redistribution from senescing leaves to newly formed sink organs, including young leaves and developing seeds. Progress has been made concerning the genes involved and the regulatory networks controlling senescence. The resulting complex metabolome changes during senescence have not been investigated in detail yet. Therefore, we conducted a comprehensive profiling of metabolites, including pigments, lipids, sugars, amino acids, organic acids, nutrient ions, and secondary metabolites, and determined approximately 260 metabolites at distinct stages in leaves and siliques during senescence in Arabidopsis (Arabidopsis thaliana). This provided an extensive catalog of metabolites and their spatiotemporal cobehavior with progressing senescence. Comparison with silique data provides clues to source-sink relations. Furthermore, we analyzed the metabolite distribution within single leaves along the basipetal sink-source transition trajectory during senescence. Ceramides, lysolipids, aromatic amino acids, branched chain amino acids, and stress-induced amino acids accumulated, and an imbalance of asparagine/aspartate, glutamate/glutamine, and nutrient ions in the tip region of leaves was detected. Furthermore, the spatiotemporal distribution of tricarboxylic acid cycle intermediates was already changed in the presenescent leaves, and glucosinolates, raffinose, and galactinol accumulated in the base region of leaves with preceding senescence. These results are discussed in the context of current models of the metabolic shifts occurring during developmental and environmentally induced senescence. As senescence processes are correlated to crop yield, the metabolome data and the approach provided here can serve as a blueprint for the analysis of traits and conditions linking crop yield and senescence.}, language = {en} } @article{SchmidtSchippersMieuletetal.2013, author = {Schmidt, Romy and Schippers, Jos H. M. and Mieulet, Delphine and Obata, Toshihiro and Fernie, Alisdair and Guiderdoni, Emmanuel and M{\"u}ller-R{\"o}ber, Bernd}, title = {Multipass, a rice R2R3-type MYB transcription factor, regulates adaptive growth by integrating multiple hormonal pathways}, series = {The plant journal}, volume = {76}, journal = {The plant journal}, number = {2}, publisher = {Wiley-Blackwell}, address = {Hoboken}, issn = {0960-7412}, doi = {10.1111/tpj.12286}, pages = {258 -- 273}, year = {2013}, abstract = {Growth regulation is an important aspect of plant adaptation during environmental perturbations. Here, the role of MULTIPASS (OsMPS), an R2R3-type MYB transcription factor of rice, was explored. OsMPS is induced by salt stress and expressed in vegetative and reproductive tissues. Over-expression of OsMPS reduces growth under non-stress conditions, while knockdown plants display increased biomass. OsMPS expression is induced by abscisic acid and cytokinin, but is repressed by auxin, gibberellin and brassinolide. Growth retardation caused by OsMPS over-expression is partially restored by auxin application. Expression profiling revealed that OsMPS negatively regulates the expression of EXPANSIN (EXP) and cell-wall biosynthesis as well as phytohormone signaling genes. Furthermore, the expression of OsMPS-dependent genes is regulated by auxin, cytokinin and abscisic acid. Moreover, we show that OsMPS is a direct upstream regulator of OsEXPA4, OsEXPA8, OsEXPB2, OsEXPB3, OsEXPB6 and the endoglucanase genes OsGLU5 and OsGLU14. The multiple responses of OsMPS and its target genes to various hormones suggest an integrative function of OsMPS in the cross-talk between phytohormones and the environment to regulate adaptive growth.}, language = {en} } @article{RibeiroAraujoFernieetal.2012, author = {Ribeiro, Dimas M. and Araujo, Wagner L. and Fernie, Alisdair and Schippers, Jos H. M. and M{\"u}ller-R{\"o}ber, Bernd}, title = {Action of Gibberellins on growth and metabolism of arabidopsis plants Associated with high concentration of carbon dioxide}, series = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants}, volume = {160}, journal = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants}, number = {4}, publisher = {American Society of Plant Physiologists}, address = {Rockville}, issn = {0032-0889}, doi = {10.1104/pp.112.204842}, pages = {1781 -- 1794}, year = {2012}, abstract = {Although the positive effect of elevated CO2 concentration [CO2] on plant growth is well known, it remains unclear whether global climate change will positively or negatively affect crop yields. In particular, relatively little is known about the role of hormone pathways in controlling the growth responses to elevated [CO2]. Here, we studied the impact of elevated [CO2] on plant biomass and metabolism in Arabidopsis (Arabidopsis thaliana) in relation to the availability of gibberellins (GAs). Inhibition of growth by the GA biosynthesis inhibitor paclobutrazol (PAC) at ambient [CO2] (350 mu mol CO2 mol(-1)) was reverted by elevated [CO2] (750 mu mol CO2 mol(-1)). Thus, we investigated the metabolic adjustment and modulation of gene expression in response to changes in growth of plants imposed by varying the GA regime in ambient and elevated [CO2]. In the presence of PAC (low-GA regime), the activities of enzymes involved in photosynthesis and inorganic nitrogen assimilation were markedly increased at elevated [CO2], whereas the activities of enzymes of organic acid metabolism were decreased. Under ambient [CO2], nitrate, amino acids, and protein accumulated upon PAC treatment; however, this was not the case when plants were grown at elevated [CO2]. These results suggest that only under ambient [CO2] is GA required for the integration of carbohydrate and nitrogen metabolism underlying optimal biomass determination. Our results have implications concerning the action of the Green Revolution genes in future environmental conditions.}, language = {en} } @article{RibeiroAraujoFernieetal.2012, author = {Ribeiro, Dimas M. and Araujo, Wagner L. and Fernie, Alisdair and Schippers, Jos H. M. and M{\"u}ller-R{\"o}ber, Bernd}, title = {Translatome and metabolome effects triggered by gibberellins during rosette growth in Arabidopsis}, series = {Journal of experimental botany}, volume = {63}, journal = {Journal of experimental botany}, number = {7}, publisher = {Oxford Univ. Press}, address = {Oxford}, issn = {0022-0957}, doi = {10.1093/jxb/err463}, pages = {2769 -- 2786}, year = {2012}, abstract = {Although gibberellins (GAs) are well known for their growth control function, little is known about their effects on primary metabolism. Here the modulation of gene expression and metabolic adjustment in response to changes in plant (Arabidopsis thaliana) growth imposed on varying the gibberellin regime were evaluated. Polysomal mRNA populations were profiled following treatment of plants with paclobutrazol (PAC), an inhibitor of GA biosynthesis, and gibberellic acid (GA(3)) to monitor translational regulation of mRNAs globally. Gibberellin levels did not affect levels of carbohydrates in plants treated with PAC and/or GA(3). However, the tricarboxylic acid cycle intermediates malate and fumarate, two alternative carbon storage molecules, accumulated upon PAC treatment. Moreover, an increase in nitrate and in the levels of the amino acids was observed in plants grown under a low GA regime. Only minor changes in amino acid levels were detected in plants treated with GA(3) alone, or PAC plus GA(3). Comparison of the molecular changes at the transcript and metabolite levels demonstrated that a low GA level mainly affects growth by uncoupling growth from carbon availability. These observations, together with the translatome changes, reveal an interaction between energy metabolism and GA-mediated control of growth to coordinate cell wall extension, secondary metabolism, and lipid metabolism.}, language = {en} } @article{WuAlluGarapatietal.2012, author = {Wu, Anhui and Allu, Annapurna Devi and Garapati, Prashanth and Siddiqui, Hamad and Dortay, Hakan and Zanor, Maria-Ines and Asensi-Fabado, Maria Amparo and Munne-Bosch, Sergi and Antonio, Carla and Tohge, Takayuki and Fernie, Alisdair and Kaufmann, Kerstin and Xue, Gang-Ping and M{\"u}ller-R{\"o}ber, Bernd and Balazadeh, Salma}, title = {Jungbrunnen1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in arabidopsis}, series = {The plant cell}, volume = {24}, journal = {The plant cell}, number = {2}, publisher = {American Society of Plant Physiologists}, address = {Rockville}, issn = {1040-4651}, doi = {10.1105/tpc.111.090894}, pages = {482 -- 506}, year = {2012}, abstract = {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.}, language = {en} } @article{RohrmannTohgeAlbaetal.2011, author = {Rohrmann, Johannes and Tohge, Takayuki and Alba, Rob and Osorio, Sonia and Caldana, Camila and McQuinn, Ryan and Arvidsson, Samuel Janne and van der Merwe, Margaretha J. and Riano-Pachon, Diego Mauricio and M{\"u}ller-R{\"o}ber, Bernd and Fei, Zhangjun and Nesi, Adriano Nunes and Giovannoni, James J. and Fernie, Alisdair}, title = {Combined transcription factor profiling, microarray analysis and metabolite profiling reveals the transcriptional control of metabolic shifts occurring during tomato fruit development}, series = {The plant journal}, volume = {68}, journal = {The plant journal}, number = {6}, publisher = {Wiley-Blackwell}, address = {Malden}, issn = {0960-7412}, doi = {10.1111/j.1365-313X.2011.04750.x}, pages = {999 -- 1013}, year = {2011}, abstract = {Maturation of fleshy fruits such as tomato (Solanum lycopersicum) is subject to tight genetic control. Here we describe the development of a quantitative real-time PCR platform that allows accurate quantification of the expression level of approximately 1000 tomato transcription factors. In addition to utilizing this novel approach, we performed cDNA microarray analysis and metabolite profiling of primary and secondary metabolites using GC-MS and LC-MS, respectively. We applied these platforms to pericarp material harvested throughout fruit development, studying both wild-type Solanum lycopersicum cv. Ailsa Craig and the hp1 mutant. This mutant is functionally deficient in the tomato homologue of the negative regulator of the light signal transduction gene DDB1 from Arabidopsis, and is furthermore characterized by dramatically increased pigment and phenolic contents. We choose this particular mutant as it had previously been shown to have dramatic alterations in the content of several important fruit metabolites but relatively little impact on other ripening phenotypes. The combined dataset was mined in order to identify metabolites that were under the control of these transcription factors, and, where possible, the respective transcriptional regulation underlying this control. The results are discussed in terms of both programmed fruit ripening and development and the transcriptional and metabolic shifts that occur in parallel during these processes.}, language = {en} } @article{LotkowskaTohgeFernieetal.2015, author = {Lotkowska, Magda E. and Tohge, Takayuki and Fernie, Alisdair and Xue, Gang-Ping and Balazadeh, Salma and M{\"u}ller-R{\"o}ber, Bernd}, title = {The Arabidopsis Transcription Factor MYB112 Promotes Anthocyanin Formation during Salinity and under High Light Stress}, 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 = {3}, publisher = {American Society of Plant Physiologists}, address = {Rockville}, issn = {0032-0889}, doi = {10.1104/pp.15.00605}, pages = {1862 -- 1880}, year = {2015}, abstract = {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.}, language = {en} } @article{BalazadehSchildhauerAraujoetal.2014, author = {Balazadeh, Salma and Schildhauer, Joerg and Araujo, Wagner L. and Munne-Bosch, Sergi and Fernie, Alisdair 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} } @misc{OmranianKleessenTohgeetal.2015, author = {Omranian, Nooshin and Kleessen, Sabrina and Tohge, Takayuki and Klie, Sebastian and Basler, Georg and M{\"u}ller-R{\"o}ber, Bernd and Fernie, Alisdair and Nikoloski, Zoran}, title = {Differential metabolic and coexpression networks of plant metabolism}, series = {Trends in plant science}, volume = {20}, journal = {Trends in plant science}, number = {5}, publisher = {Elsevier}, address = {London}, issn = {1360-1385}, doi = {10.1016/j.tplants.2015.02.002}, pages = {266 -- 268}, year = {2015}, abstract = {Recent analyses have demonstrated that plant metabolic networks do not differ in their structural properties and that genes involved in basic metabolic processes show smaller coexpression than genes involved in specialized metabolism. By contrast, our analysis reveals differences in the structure of plant metabolic networks and patterns of coexpression for genes in (non)specialized metabolism. Here we caution that conclusions concerning the organization of plant metabolism based on network-driven analyses strongly depend on the computational approaches used.}, language = {en} }