TY - JOUR A1 - Pajoro, Alice A1 - Madrigal, Pedro A1 - Muino, Jose M. A1 - Tomas Matus, Jose A1 - Jin, Jian A1 - Mecchia, Martin A. A1 - Debernardi, Juan M. A1 - Palatnik, Javier F. A1 - Balazadeh, Salma A1 - Arif, Muhammad A1 - Wellmer, Frank A1 - Krajewski, Pawel A1 - Riechmann, Jose-Luis A1 - Angenent, Gerco C. A1 - Kaufmann, Kerstin T1 - Dynamics of chromatin accessibility and gene regulation by MADS-domain transcription factors in flower development JF - Genome biology : biology for the post-genomic era N2 - Background: Development of eukaryotic organisms is controlled by transcription factors that trigger specific and global changes in gene expression programs. In plants, MADS-domain transcription factors act as master regulators of developmental switches and organ specification. However, the mechanisms by which these factors dynamically regulate the expression of their target genes at different developmental stages are still poorly understood. Results: We characterized the relationship of chromatin accessibility, gene expression, and DNA binding of two MADS-domain proteins at different stages of Arabidopsis flower development. Dynamic changes in APETALA1 and SEPALLATA3 DNA binding correlated with changes in gene expression, and many of the target genes could be associated with the developmental stage in which they are transcriptionally controlled. We also observe dynamic changes in chromatin accessibility during flower development. Remarkably, DNA binding of APETALA1 and SEPALLATA3 is largely independent of the accessibility status of their binding regions and it can precede increases in DNA accessibility. These results suggest that APETALA1 and SEPALLATA3 may modulate chromatin accessibility, thereby facilitating access of other transcriptional regulators to their target genes. Conclusions: Our findings indicate that different homeotic factors regulate partly overlapping, yet also distinctive sets of target genes in a partly stage-specific fashion. By combining the information from DNA-binding and gene expression data, we are able to propose models of stage-specific regulatory interactions, thereby addressing dynamics of regulatory networks throughout flower development. Furthermore, MADS-domain TFs may regulate gene expression by alternative strategies, one of which is modulation of chromatin accessibility. KW - Flower Development KW - Floral Organ KW - Floral Meristem KW - Chromatin Accessibility KW - Growth Regulate Factor Y1 - 2014 U6 - https://doi.org/10.1186/gb-2014-15-3-r41 SN - 1465-6906 SN - 1474-760X VL - 15 PB - BioMed Central CY - London ER - TY - GEN A1 - Pajoro, Alice A1 - Madrigal, Pedro A1 - Muiño, Jose M. A1 - Matus, José Tomás A1 - Jin, Jian A1 - Mecchia, Martin A. A1 - Debernardi, Juan M. A1 - Palatnik, Javier F. A1 - Balazadeh, Salma A1 - Arif, Muhammad A1 - Ó’Maoiléidigh, Diarmuid S. A1 - Wellmer, Frank A1 - Krajewski, Pawel A1 - Riechmann, José-Luis A1 - Angenent, Gerco C. A1 - Kaufmann, Kerstin T1 - Dynamics of chromatin accessibility and gene regulation by MADS-domain transcription factors in flower development T2 - Zweitveröffentlichungen der Universität Potsdam : Mathematisch-Naturwissenschaftliche Reihe N2 - Background: Development of eukaryotic organisms is controlled by transcription factors that trigger specific and global changes in gene expression programs. In plants, MADS-domain transcription factors act as master regulators of developmental switches and organ specification. However, the mechanisms by which these factors dynamically regulate the expression of their target genes at different developmental stages are still poorly understood. Results: We characterized the relationship of chromatin accessibility, gene expression, and DNA binding of two MADS-domain proteins at different stages of Arabidopsis flower development. Dynamic changes in APETALA1 and SEPALLATA3 DNA binding correlated with changes in gene expression, and many of the target genes could be associated with the developmental stage in which they are transcriptionally controlled. We also observe dynamic changes in chromatin accessibility during flower development. Remarkably, DNA binding of APETALA1 and SEPALLATA3 is largely independent of the accessibility status of their binding regions and it can precede increases in DNA accessibility. These results suggest that APETALA1 and SEPALLATA3 may modulate chromatin accessibility, thereby facilitating access of other transcriptional regulators to their target genes. Conclusions: Our findings indicate that different homeotic factors regulate partly overlapping, yet also distinctive sets of target genes in a partly stage-specific fashion. By combining the information from DNA-binding and gene expression data, we are able to propose models of stage-specific regulatory interactions, thereby addressing dynamics of regulatory networks throughout flower development. Furthermore, MADS-domain TFs may regulate gene expression by alternative strategies, one of which is modulation of chromatin accessibility. T3 - Zweitveröffentlichungen der Universität Potsdam : Mathematisch-Naturwissenschaftliche Reihe - 1327 KW - flower development KW - floral organ KW - floral meristem KW - chromatin accessibility KW - growth regulate factor Y1 - 2014 U6 - http://nbn-resolving.de/urn/resolver.pl?urn:nbn:de:kobv:517-opus4-431139 SN - 1866-8372 VL - 15 ER - TY - JOUR A1 - Balazadeh, Salma A1 - Jaspert, Nils A1 - Arif, Muhammad A1 - Müller-Röber, Bernd A1 - Maurino, Veronica G. T1 - Expression of ROS-responsive genes and transcription factors after metabolic formation of H2O2 in chloroplasts JF - Frontiers in plant science N2 - 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. KW - glycolate oxidase KW - H2O2 KW - ROS-responsive genes KW - transcription factors Y1 - 2012 U6 - https://doi.org/10.3389/fpls.2012.00234 SN - 1664-462X VL - 3 PB - Frontiers Research Foundation CY - Lausanne ER - TY - JOUR A1 - Engqvist, Martin K. M. A1 - Schmitz, Jessica A1 - Gertzmann, Anke A1 - Florian, Alexandra A1 - Jaspert, Nils A1 - Arif, Muhammad A1 - Balazadeh, Salma A1 - Müller-Röber, Bernd A1 - Fernie, Alisdair R. A1 - Maurino, Veronica G. T1 - GLYCOLATE OXIDASE3, a Glycolate Oxidase Homolog of Yeast L-Lactate Cytochrome c Oxidoreductase, Supports L-Lactate Oxidation in Roots of Arabidopsis JF - Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants N2 - 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. Y1 - 2015 U6 - https://doi.org/10.1104/pp.15.01003 SN - 0032-0889 SN - 1532-2548 VL - 169 IS - 2 SP - 1042 EP - 1061 PB - American Society of Plant Physiologists CY - Rockville ER - TY - JOUR A1 - Rauf, Mamoona A1 - Arif, Muhammad A1 - Fisahn, Joachim A1 - Xue, Gang-Ping A1 - Balazadeh, Salma A1 - Müller-Röber, Bernd T1 - NAC transcription factor speedy hyponastic growth regulates flooding-induced leaf movement in arabidopsis JF - The plant cell N2 - In rosette plants, root flooding (waterlogging) triggers rapid upward (hyponastic) leaf movement representing an important architectural stress response that critically determines plant performance in natural habitats. The directional growth is based on localized longitudinal cell expansion at the lower (abaxial) side of the leaf petiole and involves the volatile phytohormone ethylene (ET). We report the existence of a transcriptional core unit underlying directional petiole growth in Arabidopsis thaliana, governed by the NAC transcription factor SPEEDY HYPONASTIC GROWTH (SHYG). Overexpression of SHYG in transgenic Arabidopsis thaliana enhances waterlogging-triggered hyponastic leaf movement and cell expansion in abaxial cells of the basal petiole region, while both responses are largely diminished in shyg knockout mutants. Expression of several EXPANSIN and XYLOGLUCAN ENDOTRANSGLYCOSYLASE/HYDROLASE genes encoding cell wall-loosening proteins was enhanced in SHYG overexpressors but lowered in shyg. We identified ACC OXIDASE5 (ACO5), encoding a key enzyme of ET biosynthesis, as a direct transcriptional output gene of SHYG and found a significantly reduced leaf movement in response to root flooding in aco5 T-DNA insertion mutants. Expression of SHYG in shoot tissue is triggered by root flooding and treatment with ET, constituting an intrinsic ET-SHYG-ACO5 activator loop for rapid petiole cell expansion upon waterlogging. Y1 - 2013 U6 - https://doi.org/10.1105/tpc.113.117861 SN - 1040-4651 SN - 1532-298X VL - 25 IS - 12 SP - 4941 EP - 4955 PB - American Society of Plant Physiologists CY - Rockville ER - TY - JOUR A1 - Rauf, Mamoona A1 - Arif, Muhammad A1 - Dortay, Hakan A1 - Matallana-Ramirez, Lilian P. A1 - Waters, Mark T. A1 - Nam, Hong Gil A1 - Lim, Pyung-Ok A1 - Müller-Röber, Bernd A1 - Balazadeh, Salma T1 - ORE1 balances leaf senescence against maintenance by antagonizing G2-like-mediated transcription JF - EMBO reports N2 - Leaf senescence is a key physiological process in all plants. Its onset is tightly controlled by transcription factors, of which NAC factor ORE1 (ANAC092) is crucial in Arabidopsis thaliana. Enhanced expression of ORE1 triggers early senescence by controlling a downstream gene network that includes various senescence-associated genes. Here, we report that unexpectedly ORE1 interacts with the G2-like transcription factors GLK1 and GLK2, which are important for chloroplast development and maintenance, and thereby for leaf maintenance. ORE1 antagonizes GLK transcriptional activity, shifting the balance from chloroplast maintenance towards deterioration. Our finding identifies a new mechanism important for the control of senescence by ORE1. KW - transcription factor KW - senescence KW - chloroplast KW - protein-protein interaction Y1 - 2013 U6 - https://doi.org/10.1038/embor.2013.24 SN - 1469-221X VL - 14 IS - 4 SP - 382 EP - 388 PB - Nature Publ. Group CY - London ER - TY - JOUR A1 - Köslin-Findeklee, Fabian A1 - Rizi, Vajiheh Safavi A1 - Becker, Martin A. A1 - Parra-Londono, Sebastian A1 - Arif, Muhammad A1 - Balazadeh, Salma A1 - Müller-Röber, Bernd A1 - Kunze, Reinhard A1 - Horst, Walter J. T1 - Transcriptomic analysis of nitrogen starvation- and cultivar-specific leaf senescence in winter oilseed rape (Brassica napus L.) JF - Plant science : an international journal of experimental plant biology N2 - High nitrogen (N) efficiency, characterized by high grain yield under N limitation, is an important agricultural trait in Brassica napus L. cultivars related to delayed senescence of older leaves during reproductive growth (a syndrome called stay-green). The aim of this study was thus to identify genes whose expression is specifically altered during N starvation-induced leaf senescence and that can be used as markers to distinguish cultivars at early stages of senescence prior to chlorophyll loss. To this end, the transcriptomes of leaves of two B. napus cultivars differing in stay-green characteristics and N efficiency were analyzed 4 days after the induction of senescence by either N starvation, leaf shading or detaching. In addition to N metabolism genes, N starvation mostly (and specifically) repressed genes related to photosynthesis, photorespiration and cell-wall structure, while genes related to mitochondrial electron transport and flavonoid biosynthesis were predominately up-regulated. A kinetic study over a period of 12 days with four B. napus cultivars differing in their stay-green characteristics confirmed the cultivar-specific regulation of six genes in agreement with their senescence behavior: the senescence regulator ANAC029, the anthocyanin synthesis-related genes ANS and DFR-like1, the ammonium transporter AMT1:4, the ureide transporter UPSS, and SPS1 involved in sucrose biosynthesis. The identified genes represent markers for the detection of cultivar-specific differences in N starvation-induced leaf senescence and can thus be employed as valuable tools in B. napus breeding. (C) 2015 Elsevier Ireland Ltd. All rights reserved. KW - Brassica napus KW - Genotypic differences KW - Leaf senescence KW - Molecular marker KW - N efficiency KW - Stay-green Y1 - 2015 U6 - https://doi.org/10.1016/j.plantsci.2014.11.018 SN - 0168-9452 VL - 233 SP - 174 EP - 185 PB - Elsevier CY - Clare ER -