@misc{BeninaRibeiroGechevetal.2015,
  author    = {Benina, Maria and Ribeiro, Dimas Mendes and Gechev, Tsanko S. and M{\"u}ller-R{\"o}ber, Bernd and Schippers, Jos H. M.},
  title     = {A cell type-specific view on the translation of mRNAs from ROS-responsive genes upon paraquat treatment of Arabidopsis thaliana leaves},
  series = {Plant, cell \& environment : cell physiology, whole-plant physiology, community physiology},
  volume    = {38},
  journal   = {Plant, cell \& environment : cell physiology, whole-plant physiology, community physiology},
  number    = {2},
  publisher = {Wiley-Blackwell},
  address   = {Hoboken},
  issn      = {0140-7791},
  doi       = {10.1111/pce.12355},
  pages     = {349 -- 363},
  year      = {2015},
  abstract  = {Oxidative stress causes dramatic changes in the expression levels of many genes. The formation of a functional protein through successful mRNA translation is central to a coordinated cellular response. To what extent the response towards reactive oxygen species (ROS) is regulated at the translational level is poorly understood. Here we analysed leaf- and tissue-specific translatomes using a set of transgenic Arabidopsis thaliana lines expressing a FLAG-tagged ribosomal protein to immunopurify polysome-bound mRNAs before and after oxidative stress. We determined transcript levels of 171 ROS-responsive genes upon paraquat treatment, which causes formation of superoxide radicals, at the whole-organ level. Furthermore, the translation of mRNAs was determined for five cell types: mesophyll, bundle sheath, phloem companion, epidermal and guard cells. Mesophyll and bundle sheath cells showed the strongest response to paraquat treatment. Interestingly, several ROS-responsive transcription factors displayed cell type-specific translation patterns, while others were translated in all cell types. In part, cell type-specific translation could be explained by the length of the 5-untranslated region (5-UTR) and the presence of upstream open reading frames (uORFs). Our analysis reveals insights into the translational regulation of ROS-responsive genes, which is important to understanding cell-specific responses and functions during oxidative stress. The study illustrates the response of different Arabidopsis thaliana leaf cells and tissues to oxidative stress at the translational level, an aspect of reactive oxygen species (ROS) biology that has been little studied in the past. Our data reveal insights into how translational regulation of ROS-responsive genes is fine-tuned at the cellular level, a phenomenon contributing to the integrated physiological response of leaves to stresses involving changes in ROS levels.},
  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{LaiDentonGilesMuellerRoeberetal.2011,
  author    = {Lai, Alvina G. and Denton-Giles, Matthew and M{\"u}ller-R{\"o}ber, Bernd and Schippers, Jos H. M. and Dijkwel, Paul P.},
  title     = {Positional information resolves structural variations and uncovers an evolutionarily divergent genetic locus in accessions of arabidopsis thaliana},
  series = {Genome biology and evolution},
  volume    = {3},
  journal   = {Genome biology and evolution},
  number    = {1-2},
  publisher = {Oxford Univ. Press},
  address   = {Oxford},
  issn      = {1759-6653},
  doi       = {10.1093/gbe/evr038},
  pages     = {627 -- 640},
  year      = {2011},
  abstract  = {Genome sequencing of closely related individuals has yielded valuable insights that link genome evolution to phenotypic variations. However, advancement in sequencing technology has also led to an escalation in the number of poor quality-drafted genomes assembled based on reference genomes that can have highly divergent or haplotypic regions. The self-fertilizing nature of Arabidopsis thaliana poses an advantage to sequencing projects because its genome is mostly homozygous. To determine the accuracy of an Arabidopsis drafted genome in less conserved regions, we performed a resequencing experiment on a similar to 371-kb genomic interval in the Landsberg erecta (Ler-0) accession. We identified novel structural variations (SVs) between Ler-0 and the reference accession Col-0 using a long-range polymerase chain reaction approach to generate an Illumina data set that has positional information, that is, a data set with reads that map to a known location. Positional information is important for accurate genome assembly and the resolution of SVs particularly in highly duplicated or repetitive regions. Sixty-one regions with misassembly signatures were identified from the Ler-0 draft, suggesting the presence of novel SVs that are not represented in the draft sequence. Sixty of those were resolved by iterative mapping using our data set. Fifteen large indels (> 100 bp) identified from this study were found to be located either within protein-coding regions or upstream regulatory regions, suggesting the formation of novel alleles or altered regulation of existing genes in Ler-0. We propose future genome-sequencing experiments to follow a clone-based approach that incorporates positional information to ultimately reveal haplotype-specific differences between accessions.},
  language  = {en}
}
@article{LaiDohertyMuellerRoeberetal.2012,
  author    = {Lai, Alvina Grace and Doherty, Colleen J. and M{\"u}ller-R{\"o}ber, Bernd and Kay, Steve A. and Schippers, Jos H. M. and Dijkwel, Paul P.},
  title     = {CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses},
  series = {Proceedings of the National Academy of Sciences of the United States of America},
  volume    = {109},
  journal   = {Proceedings of the National Academy of Sciences of the United States of America},
  number    = {42},
  publisher = {National Acad. of Sciences},
  address   = {Washington},
  issn      = {0027-8424},
  doi       = {10.1073/pnas.1209148109},
  pages     = {17129 -- 17134},
  year      = {2012},
  abstract  = {Organisms have evolved endogenous biological clocks as internal timekeepers to coordinate metabolic processes with the external environment. Here, we seek to understand the mechanism of synchrony between the oscillator and products of metabolism known as Reactive Oxygen Species (ROS) in Arabidopsis thaliana. ROS-responsive genes exhibit a time-of-day-specific phase of expression under diurnal and circadian conditions, implying a role of the circadian clock in transcriptional regulation of these genes. Hydrogen peroxide production and scavenging also display time-of-day phases. Mutations in the core-clock regulator, CIRCADIAN CLOCK ASSOCIATED 1 (CCA1), affect the transcriptional regulation of ROS-responsive genes, ROS homeostasis, and tolerance to oxidative stress. Mis-expression of EARLY FLOWERING 3, LUX ARRHYTHMO, and TIMING OF CAB EXPRESSION 1 affect ROS production and transcription, indicating a global effect of the clock on the ROS network. We propose CCA1 as a master regulator of ROS homeostasis through association with the Evening Element in promoters of ROS genes in vivo to coordinate time-dependent responses to oxidative stress. We also find that ROS functions as an input signal that affects the transcriptional output of the clock, revealing an important link between ROS signaling and circadian output. Temporal coordination of ROS signaling by CCA1 and the reciprocal control of circadian output by ROS reveal a mechanistic link that allows plants to master oxidative stress responses.},
  language  = {en}
}
@article{LuWangPerssonetal.2014,
  author    = {Lu, Dandan and Wang, Ting and Persson, Staffan and M{\"u}ller-R{\"o}ber, Bernd and Schippers, Jos H. M.},
  title     = {Transcriptional control of ROS homeostasis by KUODA1 regulates cell expansion during leaf development},
  series = {Nature Communications},
  volume    = {5},
  journal   = {Nature Communications},
  publisher = {Nature Publ. Group},
  address   = {London},
  issn      = {2041-1723},
  doi       = {10.1038/ncomms4767},
  pages     = {9},
  year      = {2014},
  abstract  = {The final size of an organism, or of single organs within an organism, depends on an intricate coordination of cell proliferation and cell expansion. Although organism size is of fundamental importance, the molecular and genetic mechanisms that control it remain far from understood. Here we identify a transcription factor, KUODA1 (KUA1), which specifically controls cell expansion during leaf development in Arabidopsis thaliana. We show that KUA1 expression is circadian regulated and depends on an intact clock. Furthermore, KUA1 directly represses the expression of a set of genes encoding for peroxidases that control reactive oxygen species (ROS) homeostasis in the apoplast. Disruption of KUA1 results in increased peroxidase activity and smaller leaf cells. Chemical or genetic interference with the ROS balance or peroxidase activity affects cell size in a manner consistent with the identified KUA1 function. Thus, KUA1 modulates leaf cell expansion and final organ size by controlling ROS homeostasis.},
  language  = {en}
}
@article{NguyenSchippersGoniRamosetal.2013,
  author    = {Nguyen, Hung M. and Schippers, Jos H. M. and Goni-Ramos, Oscar and Christoph, Mathias P. and Dortay, Hakan and van der Hoorn, Renier A. L. and M{\"u}ller-R{\"o}ber, Bernd},
  title     = {An upstream regulator of the 26S proteasome modulates organ size in Arabidopsis thaliana},
  series = {The plant journal},
  volume    = {74},
  journal   = {The plant journal},
  number    = {1},
  publisher = {Wiley-Blackwell},
  address   = {Hoboken},
  issn      = {0960-7412},
  doi       = {10.1111/tpj.12097},
  pages     = {25 -- 36},
  year      = {2013},
  abstract  = {In both animal and plant kingdoms, body size is a fundamental but still poorly understood attribute of biological systems. Here we report that the Arabidopsis NAC transcription factor Regulator of Proteasomal Gene Expression' (RPX) controls leaf size by positively modulating proteasome activity. We further show that the cis-element recognized by RPX is evolutionarily conserved between higher plant species. Upon over-expression of RPX, plants exhibit reduced growth, which may be reversed by a low concentration of the pharmacological proteasome inhibitor MG132. These data suggest that the rate of protein turnover during growth is a critical parameter for determining final organ size.},
  language  = {en}
}
@article{RibeiroAraujoFernieetal.2012,
  author    = {Ribeiro, Dimas M. and Araujo, Wagner L. and Fernie, Alisdair R. 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 R. 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}
}
@misc{SchippersNguyenLuetal.2012,
  author    = {Schippers, Jos H. M. and Nguyen, Hung M. and Lu, Dandan and Schmidt, Romy and M{\"u}ller-R{\"o}ber, Bernd},
  title     = {ROS homeostasis during development: an evolutionary conserved strategy},
  series = {Cellular and molecular life sciences},
  volume    = {69},
  journal   = {Cellular and molecular life sciences},
  number    = {19},
  publisher = {Springer},
  address   = {Basel},
  issn      = {1420-682X},
  doi       = {10.1007/s00018-012-1092-4},
  pages     = {3245 -- 3257},
  year      = {2012},
  abstract  = {The balance between cellular proliferation and differentiation is a key aspect of development in multicellular organisms. Recent studies on Arabidopsis roots revealed distinct roles for different reactive oxygen species (ROS) in these processes. Modulation of the balance between ROS in proliferating cells and elongating cells is controlled at least in part at the transcriptional level. The effect of ROS on proliferation and differentiation is not specific for plants but appears to be conserved between prokaryotic and eukaryotic life forms. The ways in which ROS is received and how it affects cellular functioning is discussed from an evolutionary point of view. The different redox-sensing mechanisms that evolved ultimately result in the activation of gene regulatory networks that control cellular fate and decision-making. This review highlights the potential common origin of ROS sensing, indicating that organisms evolved similar strategies for utilizing ROS during development, and discusses ROS as an ancient universal developmental regulator.},
  language  = {en}
}
@article{SchmidtMieuletHubbertenetal.2013,
  author    = {Schmidt, Romy and Mieulet, Delphine and Hubberten, Hans-Michael and Obata, Toshihiro and H{\"o}fgen, Rainer and Fernie, Alisdair R. 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}
}