TY - JOUR A1 - Schmidt, Romy A1 - Mieulet, Delphine A1 - Hubberten, Hans-Michael A1 - Obata, Toshihiro A1 - Höfgen, Rainer A1 - Fernie, Alisdair R. A1 - Fisahn, Joachim A1 - Segundo, Blanca San A1 - Guiderdoni, Emmanuel A1 - Schippers, Jos H. M. A1 - Müller-Röber, Bernd T1 - Salt-responsive ERF1 regulates reactive oxygen species-dependent signaling during the initial response to salt stress in rice JF - The plant cell N2 - 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. Y1 - 2013 U6 - https://doi.org/10.1105/tpc.113.113068 SN - 1040-4651 VL - 25 IS - 6 SP - 2115 EP - 2131 PB - American Society of Plant Physiologists CY - Rockville ER - TY - JOUR A1 - Read, Betsy A. A1 - Kegel, Jessica A1 - Klute, Mary J. A1 - Kuo, Alan A1 - Lefebvre, Stephane C. A1 - Maumus, Florian A1 - Mayer, Christoph A1 - Miller, John A1 - Monier, Adam A1 - Salamov, Asaf A1 - Young, Jeremy A1 - Aguilar, Maria A1 - Claverie, Jean-Michel A1 - Frickenhaus, Stephan A1 - Gonzalez, Karina A1 - Herman, Emily K. A1 - Lin, Yao-Cheng A1 - Napier, Johnathan A1 - Ogata, Hiroyuki A1 - Sarno, Analissa F. A1 - Shmutz, Jeremy A1 - Schroeder, Declan A1 - de Vargas, Colomban A1 - Verret, Frederic A1 - von Dassow, Peter A1 - Valentin, Klaus A1 - Van de Peer, Yves A1 - Wheeler, Glen A1 - Dacks, Joel B. A1 - Delwiche, Charles F. A1 - Dyhrman, Sonya T. A1 - Glöckner, Gernot A1 - John, Uwe A1 - Richards, Thomas A1 - Worden, Alexandra Z. A1 - Zhang, Xiaoyu A1 - Grigoriev, Igor V. A1 - Allen, Andrew E. A1 - Bidle, Kay A1 - Borodovsky, M. A1 - Bowler, C. A1 - Brownlee, Colin A1 - Cock, J. Mark A1 - Elias, Marek A1 - Gladyshev, Vadim N. A1 - Groth, Marco A1 - Guda, Chittibabu A1 - Hadaegh, Ahmad A1 - Iglesias-Rodriguez, Maria Debora A1 - Jenkins, J. A1 - Jones, Bethan M. A1 - Lawson, Tracy A1 - Leese, Florian A1 - Lindquist, Erika A1 - Lobanov, Alexei A1 - Lomsadze, Alexandre A1 - Malik, Shehre-Banoo A1 - Marsh, Mary E. A1 - Mackinder, Luke A1 - Mock, Thomas A1 - Müller-Röber, Bernd A1 - Pagarete, Antonio A1 - Parker, Micaela A1 - Probert, Ian A1 - Quesneville, Hadi A1 - Raines, Christine A1 - Rensing, Stefan A. A1 - Riano-Pachon, Diego Mauricio A1 - Richier, Sophie A1 - Rokitta, Sebastian A1 - Shiraiwa, Yoshihiro A1 - Soanes, Darren M. A1 - van der Giezen, Mark A1 - Wahlund, Thomas M. A1 - Williams, Bryony A1 - Wilson, Willie A1 - Wolfe, Gordon A1 - Wurch, Louie L. T1 - Pan genome of the phytoplankton Emiliania underpins its global distribution JF - Nature : the international weekly journal of science N2 - Coccolithophores have influenced the global climate for over 200 million years(1). These marine phytoplankton can account for 20 per cent of total carbon fixation in some systems(2). They form blooms that can occupy hundreds of thousands of square kilometres and are distinguished by their elegantly sculpted calcium carbonate exoskeletons (coccoliths), rendering them visible from space(3). Although coccolithophores export carbon in the form of organic matter and calcite to the sea floor, they also release CO2 in the calcification process. Hence, they have a complex influence on the carbon cycle, driving either CO2 production or uptake, sequestration and export to the deep ocean(4). Here we report the first haptophyte reference genome, from the coccolithophore Emiliania huxleyi strain CCMP1516, and sequences from 13 additional isolates. Our analyses reveal a pan genome (core genes plus genes distributed variably between strains) probably supported by an atypical complement of repetitive sequence in the genome. Comparisons across strains demonstrate that E. huxleyi, which has long been considered a single species, harbours extensive genome variability reflected in different metabolic repertoires. Genome variability within this species complex seems to underpin its capacity both to thrive in habitats ranging from the equator to the subarctic and to form large-scale episodic blooms under a wide variety of environmental conditions. Y1 - 2013 U6 - https://doi.org/10.1038/nature12221 SN - 0028-0836 SN - 1476-4687 VL - 499 IS - 7457 SP - 209 EP - 213 PB - Nature Publ. Group CY - London ER - TY - JOUR A1 - Scarpeci, Telma E. A1 - Zanor, Maria I. A1 - Müller-Röber, Bernd A1 - Valle, Estela M. T1 - Overexpression of AtWRKY30 enhances abiotic stress tolerance during early growth stages in Arabidopsis thaliana JF - PLANT MOLECULAR BIOLOGY N2 - AtWRKY30 belongs to a higher plant transcription factor superfamily, which responds to pathogen attack. In previous studies, the AtWRKY30 gene was found to be highly and rapidly induced in Arabidopsis thaliana leaves after oxidative stress treatment. In this study, electrophoretic mobility shift assays showed that AtWRKY30 binds with high specificity and affinity to the WRKY consensus sequence (W-box), and also to its own promoter. Analysis of the AtWRKY30 expression pattern by qPCR and using transgenic Arabidopsis lines carrying AtWRKY30 promoter-beta-glucuronidase fusions showed transcriptional activity in leaves subjected to biotic or abiotic stress. Transgenic Arabidopsis plants constitutively overexpressing AtWRKY30 (35S::W30 lines) were more tolerant than wild-type plants to oxidative and salinity stresses during seed germination. The results presented here show that AtWRKY30 is responsive to several stress conditions either from abiotic or biotic origin, suggesting that AtWRKY30 could have a role in the activation of defence responses at early stages of Arabidopsis growth by binding to W-boxes found in promoters of many stress/developmentally regulated genes. KW - Antioxidant response KW - Chloroplast KW - Germination KW - Oxidative stress KW - Stress signaling Y1 - 2013 U6 - https://doi.org/10.1007/s11103-013-0090-8 SN - 0167-4412 VL - 83 IS - 3 SP - 265 EP - 277 PB - SPRINGER CY - DORDRECHT 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 - Omranian, Nooshin A1 - Klie, Sebastian A1 - Müller-Röber, Bernd A1 - Nikoloski, Zoran T1 - Network-based segmentation of biological multivariate time series JF - PLoS one N2 - Molecular phenotyping technologies (e.g., transcriptomics, proteomics, and metabolomics) offer the possibility to simultaneously obtain multivariate time series (MTS) data from different levels of information processing and metabolic conversions in biological systems. As a result, MTS data capture the dynamics of biochemical processes and components whose couplings may involve different scales and exhibit temporal changes. Therefore, it is important to develop methods for determining the time segments in MTS data, which may correspond to critical biochemical events reflected in the coupling of the system's components. Here we provide a novel network-based formalization of the MTS segmentation problem based on temporal dependencies and the covariance structure of the data. We demonstrate that the problem of partitioning MTS data into k segments to maximize a distance function, operating on polynomially computable network properties, often used in analysis of biological network, can be efficiently solved. To enable biological interpretation, we also propose a breakpoint-penalty (BP-penalty) formulation for determining MTS segmentation which combines a distance function with the number/length of segments. Our empirical analyses of synthetic benchmark data as well as time-resolved transcriptomics data from the metabolic and cell cycles of Saccharomyces cerevisiae demonstrate that the proposed method accurately infers the phases in the temporal compartmentalization of biological processes. In addition, through comparison on the same data sets, we show that the results from the proposed formalization of the MTS segmentation problem match biological knowledge and provide more rigorous statistical support in comparison to the contending state-of-the-art methods. Y1 - 2013 U6 - https://doi.org/10.1371/journal.pone.0062974 SN - 1932-6203 VL - 8 IS - 5 PB - PLoS CY - San Fransisco 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 - 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 - TY - JOUR A1 - Schmidt, Romy A1 - Schippers, Jos H. M. A1 - Mieulet, Delphine A1 - Obata, Toshihiro A1 - Fernie, Alisdair R. A1 - Guiderdoni, Emmanuel A1 - Müller-Röber, Bernd T1 - Multipass, a rice R2R3-type MYB transcription factor, regulates adaptive growth by integrating multiple hormonal pathways JF - The plant journal N2 - 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. KW - development KW - expansin KW - transcription KW - Oryza sativa KW - hormone KW - abiotic stress Y1 - 2013 U6 - https://doi.org/10.1111/tpj.12286 SN - 0960-7412 SN - 1365-313X VL - 76 IS - 2 SP - 258 EP - 273 PB - Wiley-Blackwell CY - Hoboken ER - TY - JOUR A1 - Gechev, Tsanko S. A1 - Benina, Maria A1 - Obata, Toshihiro A1 - Tohge, Takayuki A1 - Neerakkal, Sujeeth A1 - Minkov, Ivan A1 - Hille, Jacques A1 - Temanni, Mohamed-Ramzi A1 - Marriott, Andrew S. A1 - Bergström, Ed A1 - Thomas-Oates, Jane A1 - Antonio, Carla A1 - Müller-Röber, Bernd A1 - Schippers, Jos H. M. A1 - Fernie, Alisdair R. A1 - Toneva, Valentina T1 - Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis JF - Cellular and molecular life sciences N2 - 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. KW - Antioxidant genes KW - Catalase KW - Desiccation tolerance KW - Drought stress KW - Metabolome analysis KW - Resurrection plants Y1 - 2013 U6 - https://doi.org/10.1007/s00018-012-1155-6 SN - 1420-682X VL - 70 IS - 4 SP - 689 EP - 709 PB - Springer CY - Basel ER - TY - JOUR A1 - Lukoszek, Radoslaw A1 - Müller-Röber, Bernd A1 - Ignatova, Zoya T1 - Interplay between polymerase II- and polymerase III-assisted expression of overlapping genes JF - FEBS letters : the journal for rapid publication of short reports in molecular biosciences N2 - Up to 15% of the genes in different genomes overlap. This architecture, although beneficial for the genome size, represents an obstacle for simultaneous transcription of both genes. Here we analyze the interference between RNA-polymerase II (Pol II) and RNA-polymerase III (Pol III) when transcribing their target genes encoded on opposing strands within the same DNA fragment in Arabidopsis thaliana. The expression of a Pol II-dependent protein-coding gene negatively correlated with the transcription of a Pol III-dependent, tRNA-coding gene set. We suggest that the architecture of the overlapping genes introduces an additional layer of control of gene expression. (C) 2013 Federation of European Biochemical Societies. Published by Elsevier B.V. All rights reserved. KW - Gene expression KW - Transcription KW - tRNA KW - Nested and overlapping genes KW - Arabidopsis thaliana Y1 - 2013 U6 - https://doi.org/10.1016/j.febslet.2013.09.033 SN - 0014-5793 SN - 1873-3468 VL - 587 IS - 22 SP - 3692 EP - 3695 PB - Elsevier CY - Amsterdam ER -