@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 R.}, 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{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 R. 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{AlseekhTohgeWendenbergetal.2015, author = {Alseekh, Saleh and Tohge, Takayuki and Wendenberg, Regina and Scossa, Federico and Omranian, Nooshin and Li, Jie and Kleessen, Sabrina and Giavalisco, Patrick and Pleban, Tzili and M{\"u}ller-R{\"o}ber, Bernd and Zamir, Dani and Nikoloski, Zoran and Fernie, Alisdair R.}, title = {Identification and Mode of Inheritance of Quantitative Trait Loci for Secondary Metabolite Abundance in Tomato}, series = {The plant cell}, volume = {27}, journal = {The plant cell}, number = {3}, publisher = {American Society of Plant Physiologists}, address = {Rockville}, issn = {1040-4651}, doi = {10.1105/tpc.114.132266}, pages = {485 -- 512}, year = {2015}, abstract = {A large-scale metabolic quantitative trait loci (mQTL) analysis was performed on the well-characterized Solanum pennellii introgression lines to investigate the genomic regions associated with secondary metabolism in tomato fruit pericarp. In total, 679 mQTLs were detected across the 76 introgression lines. Heritability analyses revealed that mQTLs of secondary metabolism were less affected by environment than mQTLs of primary metabolism. Network analysis allowed us to assess the interconnectivity of primary and secondary metabolism as well as to compare and contrast their respective associations with morphological traits. Additionally, we applied a recently established real-time quantitative PCR platform to gain insight into transcriptional control mechanisms of a subset of the mQTLs, including those for hydroxycinnamates, acyl-sugar, naringenin chalcone, and a range of glycoalkaloids. Intriguingly, many of these compounds displayed a dominant-negative mode of inheritance, which is contrary to the conventional wisdom that secondary metabolite contents decreased on domestication. We additionally performed an exemplary evaluation of two candidate genes for glycolalkaloid mQTLs via the use of virus-induced gene silencing. The combined data of this study were compared with previous results on primary metabolism obtained from the same material and to other studies of natural variance of secondary metabolism.}, language = {en} } @article{GechevBeninaObataetal.2013, author = {Gechev, Tsanko S. and Benina, Maria and Obata, Toshihiro and Tohge, Takayuki and Neerakkal, Sujeeth and Minkov, Ivan and Hille, Jacques and Temanni, Mohamed-Ramzi and Marriott, Andrew S. and Bergstr{\"o}m, Ed and Thomas-Oates, Jane and Antonio, Carla and M{\"u}ller-R{\"o}ber, Bernd and Schippers, Jos H. M. and Fernie, Alisdair R. and Toneva, Valentina}, title = {Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis}, series = {Cellular and molecular life sciences}, volume = {70}, journal = {Cellular and molecular life sciences}, number = {4}, publisher = {Springer}, address = {Basel}, issn = {1420-682X}, doi = {10.1007/s00018-012-1155-6}, pages = {689 -- 709}, year = {2013}, abstract = {Haberlea rhodopensis is a resurrection plant with remarkable tolerance to desiccation. Haberlea exposed to drought stress, desiccation, and subsequent rehydration showed no signs of damage or severe oxidative stress compared to untreated control plants. Transcriptome analysis by next-generation sequencing revealed a drought-induced reprogramming, which redirected resources from growth towards cell protection. Repression of photosynthetic and growth-related genes during water deficiency was concomitant with induction of transcription factors (members of the NAC, NF-YA, MADS box, HSF, GRAS, and WRKY families) presumably acting as master switches of the genetic reprogramming, as well as with an upregulation of genes related to sugar metabolism, signaling, and genes encoding early light-inducible (ELIP), late embryogenesis abundant (LEA), and heat shock (HSP) proteins. At the same time, genes encoding other LEA, HSP, and stress protective proteins were constitutively expressed at high levels even in unstressed controls. Genes normally involved in tolerance to salinity, chilling, and pathogens were also highly induced, suggesting a possible cross-tolerance against a number of abiotic and biotic stress factors. A notable percentage of the genes highly regulated in dehydration and subsequent rehydration were novel, with no sequence homology to genes from other plant genomes. Additionally, an extensive antioxidant gene network was identified with several gene families possessing a greater number of antioxidant genes than most other species with sequenced genomes. Two of the transcripts most abundant during all conditions encoded catalases and five more catalases were induced in water-deficient samples. Using the pharmacological inhibitor 3-aminotriazole (AT) to compromise catalase activity resulted in increased sensitivity to desiccation. Metabolome analysis by GC or LC-MS revealed accumulation of sucrose, verbascose, spermidine, and gamma-aminobutyric acid during drought, as well as particular secondary metabolites accumulating during rehydration. This observation, together with the complex antioxidant system and the constitutive expression of stress protective genes suggests that both constitutive and inducible mechanisms contribute to the extreme desiccation tolerance of H. rhodopensis.}, language = {en} } @article{WangTohgeIvakovetal.2015, author = {Wang, Ting and Tohge, Takayuki and Ivakov, Alexander and M{\"u}ller-R{\"o}ber, Bernd and Fernie, Alisdair R. and Mutwil, Marek and Schippers, Jos H. M. and Persson, Staffan}, title = {Salt-Related MYB1 Coordinates Abscisic Acid Biosynthesis and Signaling during Salt Stress in 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.15.00962}, pages = {1027 -- +}, year = {2015}, abstract = {Abiotic stresses, such as salinity, cause global yield loss of all major crop plants. Factors and mechanisms that can aid in plant breeding for salt stress tolerance are therefore of great importance for food and feed production. Here, we identified a MYB-like transcription factor, Salt-Related MYB1 (SRM1), that negatively affects Arabidopsis (Arabidopsis thaliana) seed germination under saline conditions by regulating the levels of the stress hormone abscisic acid (ABA). Accordingly, several ABA biosynthesis and signaling genes act directly downstream of SRM1, including SALT TOLERANT1/NINE-CIS-EPOXYCAROTENOID DIOXYGENASE3, RESPONSIVE TO DESICCATION26, and Arabidopsis NAC DOMAIN CONTAINING PROTEIN19. Furthermore, SRM1 impacts vegetative growth and leaf shape. We show that SRM1 is an important transcriptional regulator that directly targets ABA biosynthesis and signaling-related genes and therefore may be regarded as an important regulator of ABA-mediated salt stress 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 R. 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{LotkowskaTohgeFernieetal.2015, author = {Lotkowska, Magda E. and Tohge, Takayuki and Fernie, Alisdair R. 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} } @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 R. 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} }