Dirk K Hincha

Max Planck Institute of Molecular Plant Physiology, Potsdam, Brandenburg, Germany

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Publications (151)560.41 Total impact

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    ABSTRACT: Experience and memory of environmental stimuli that indicate future stress can prepare (prime) organismic stress responses even in species lacking a nervous system. The process through which such organisms prepare their phenotype for an improved response to future stress has been termed 'priming'. However, other terms are also used for this phenomenon, especially when considering priming in different types of organisms and when referring to different stressors. Here we propose a conceptual framework for priming of stress responses in bacteria, fungi and plants which allows comparison of priming with other terms, e.g. adaptation, acclimation, induction, acquired resistance and cross protection. We address spatial and temporal aspects of priming and highlight current knowledge about the mechanisms necessary for information storage which range from epigenetic marks to the accumulation of (dormant) signalling molecules. Furthermore, we outline possible patterns of primed stress responses. Finally, we link the ability of organisms to become primed for stress responses (their 'primability') with evolutionary ecology aspects and discuss which properties of an organism and its environment may favour the evolution of priming of stress responses. © 2015 Cambridge Philosophical Society.
    Biological Reviews 08/2015; DOI:10.1111/brv.12215 · 9.67 Impact Factor
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    ABSTRACT: Global climate change combined with asymmetric warming can have detrimental effects on the yield of crop plants such as rice (Oryza sativa L.). Little is known about metabolic responses of rice to high night temperature (HNT) conditions. Twelve cultivars with different HNT sensitivity were used to investigate metabolic changes in the vegetative stage under HNT compared to control conditions. Central metabolism, especially TCA cycle and amino acid biosynthesis, were strongly affected particularly in sensitive cultivars. Levels of several metabolites were correlated with HNT sensitivity. Furthermore, pool sizes of some metabolites negatively correlated with HNT sensitivity under control conditions, indicating metabolic pre-adaptation in tolerant cultivars. The polyamines putrescine, spermidine and spermine showed increased abundance in sensitive cultivars under HNT conditions. Correlations between the content of polyamines and 75 other metabolites indicated metabolic shifts from correlations with sugar-phosphates and 1-kestose under control to correlations with sugars and amino and organic acids under HNT conditions. Increased expression levels of ADC2 and ODC1, genes encoding enzymes catalysing the first committed steps of putrescine biosynthesis, were restricted to sensitive cultivars under HNT. Additionally, transcript levels of eight polyamine biosynthesis genes were correlated with HNT sensitivity. Responses to HNT in the vegetative stage result in distinct differences between differently responding cultivars with a dysregulation of central metabolism and an increase of polyamine biosynthesis restricted to sensitive cultivars under HNT conditions and a pre-adaptation of tolerant cultivars already under control conditions with higher levels of potentially protective compatible solutes. © The Author 2015. Published by Oxford University Press on behalf of the Society for Experimental Biology.
    Journal of Experimental Botany 07/2015; DOI:10.1093/jxb/erv352 · 5.53 Impact Factor
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    ABSTRACT: During low temperature exposure, Arabidopsis thaliana and many other plants from temperate climates increase in freezing tolerance in a process termed cold acclimation. However, the correct timing and rate of deacclimation, resulting in loss of freezing tolerance and initiation of growth is equally important for plant fitness and survival. While the molecular basis of cold acclimation has been investigated in detail, much less information is available about deacclimation. We have characterized the responses of 10 natural accessions of Arabidopsis thaliana that vary widely in their freezing tolerance, to deacclimation conditions. Sugar, proline and transcript levels declined sharply over three days in all accessions after transfer of cold acclimated plants to ambient temperatures, while freezing tolerance only declined in tolerant accessions. Correlations between freezing tolerance and the expression levels of COR genes and the content of glucose, fructose and sucrose, as well as many correlations among transcript and solute levels, that were highly significant in cold acclimated plants, were lost during deacclimation. Other correlations persisted, indicating that after three days of deacclimation, plant metabolism had not completely reverted back to the non-acclimated state. These data provide the basis for further molecular and genetic studies to unravel the regulation of deacclimation.
    Scientific Reports 07/2015; 5:12199. DOI:10.1038/srep12199 · 5.58 Impact Factor
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    ABSTRACT: Cruciferous plants synthesize a large variety of tryptophan-derived phytoalexins in response to pathogen infection, UV irradiation, or high dosages of heavy metals. The major phytoalexins of Eutrema salsugineum (Thellungiella salsuginea), which has recently been established as an extremophile model plant, are probably derivatives of indole glucosinolates, in contrast to Arabidopsis, which synthesizes characteristic camalexin from the glucosinolate precursor indole-3-acetaldoxime. The transcriptional response of E. salsugineum to UV irradiation and AgNO3 was monitored by RNAseq and microarray analysis. Most transcripts (respectively 70% and 78%) were significantly differentially regulated and a large overlap between the two treatments was observed (54% of total). While core genes of the biosynthesis of aliphatic glucosinolates were repressed, tryptophan and indole glucosinolate biosynthetic genes, as well as defence-related WRKY transcription factors, were consistently upregulated. The putative Eutrema WRKY33 ortholog was functionally tested and shown to complement camalexin deficiency in Atwrky33 mutant. In E. salsugineum, UV irradiation or heavy metal application resulted in substantial transcriptional reprogramming. Consistently induced genes of indole glucosinolate biosynthesis and modification will serve as candidate genes for the biosynthesis of Eutrema-specific phytoalexins.
    BMC Plant Biology 06/2015; 15(1):137. DOI:10.1186/s12870-015-0506-5 · 3.81 Impact Factor

  • Physical Chemistry Chemical Physics 06/2015; Submitted. · 4.49 Impact Factor
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    ABSTRACT: The accumulation of Late Embryogenesis Abundant (LEA) proteins in plants is associated with tolerance against stresses such as freezing and desiccation. Two main functions have been attributed to LEA proteins: membrane stabilization and enzyme protection. We have hypothesized previously that LEA7 from Arabidopsis thaliana may stabilize membranes because it interacts with liposomes in the dry state. Here we show that LEA7, contrary to this expectation, did not stabilize liposomes during drying and rehydration. Instead, it partially preserved the activity of the enzyme lactate dehydrogenase (LDH) during drying and freezing. Fourier-transform infrared (FTIR) spectroscopy showed no evidence of aggregation of LDH in the dry or rehydrated state under conditions that lead to complete loss of activity. To approximate the complex influence of intracellular conditions on the protective effects of a LEA protein in a convenient in-vitro assay, we measured the activity of two Arabidopsis enzymes (glucose-6-P dehydrogenase and ADP-glucose pyrophosphorylase) in total soluble leaf protein extract (Arabidopsis soluble proteome, ASP) after drying and rehydration or freezing and thawing. LEA7 partially preserved the activity of both enzymes under these conditions, suggesting its role as an enzyme protectant in vivo. Further FTIR analyses indicated the partial reversibility of protein aggregation in the dry ASP during rehydration. Similarly, aggregation in the dry ASP was strongly reduced by LEA7. In addition, mixtures of LEA7 with sucrose or verbascose reduced aggregation more than the single additives, presumably through the effects of the protein on the H-bonding network of the sugar glasses. Copyright © 2015. Published by Elsevier B.V.
    Biochimica et Biophysica Acta 05/2015; 1854(10 Pt A). DOI:10.1016/j.bbapap.2015.05.002 · 4.66 Impact Factor
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    ABSTRACT: Heat and drought stress are projected to become major challenges to sustain rice (Oryza sativa L.) yields with global climate change. Both stresses lead to yield losses when they coincide with flowering. A significant knowledge gap exists in the mechanistic understanding of the responses of rice floral organs that determine reproductive success under stress. Our work connects the metabolomic and transcriptomic changes in anthers, pistils before pollination and pollinated pistils in a heat tolerant (N22) and a heat sensitive (Moroberekan) cultivar. Systematic analysis of the floral organs revealed contrasts in metabolic profiles across anthers and pistils. Constitutive metabolic markers were identified that can define reproductive success in rice under stress. Six out of nine candidate metabolites identified by intersection analysis of stressed anthers were differentially accumulated in N22 compared to Moroberekan under non-stress conditions. Sugar metabolism was identified to be the crucial metabolic and transcriptional component that differentiated floral organ tolerance or susceptibility to stress. While susceptible Moroberekan specifically showed high expression of the Carbon Starved Anthers (CSA) gene under combined heat and drought, tolerant N22 responded with high expression of genes encoding a sugar transporter (MST8) and a cell wall invertase (INV4) as markers of high sink strength. This article is protected by copyright. All rights reserved.
    Plant Cell and Environment 03/2015; 38(10). DOI:10.1111/pce.12545 · 6.96 Impact Factor

  • Plant Cell and Environment 03/2015; · 6.96 Impact Factor
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    ABSTRACT: Climate models predict an increased likelihood of seasonal droughts for many areas of the world. Breeding for drought tolerance could be accelerated by marker-assisted selection. As a basis for marker identification, we studied genetic variance, predictability of field performance, and potential costs of tolerance in potato (Solanum tuberosum L.). Potato produces high calories per unit water invested, but is drought-sensitive. In 14 independent pot or field trials, 34 potato cultivars were grown under optimal and reduced water supply to determine starch yield. In an artificial data set, we tested several stress indices for their power to distinguish tolerant and sensitive genotypes independent of their yield potential. We identified DRYM (deviation of relative starch yield from its experimental median) as the most efficient index. DRYM corresponded qualitatively to the partial least square-model based metric of drought stress tolerance in a stress effect model. The DRYM identified significant tolerance variation in the European potato cultivar population to allow tolerance breeding and marker identification. Tolerance results from pot trials correlated with those from field trials, but predicted field performance worse than field growth parameters. Drought tolerance correlated negatively with yield under optimal conditions in the field. The distribution of yield data versus DRYM indicated that tolerance can be combined with average yield potentials, thus circumventing potential yield penalties in tolerance breeding.
    Functional Plant Biology 03/2015; 42(7):655-667. DOI:10.1071/FP15013 · 3.15 Impact Factor
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    ABSTRACT: In plants from temperate climates such as Arabidopsis thaliana low, non-freezing temperatures lead to increased freezing tolerance in a process termed cold acclimation. During cold acclimation, massive changes in gene expression and in the content of primary metabolites and lipids have been observed. Here, we have analyzed the influence of cold acclimation on flavonol and anthocyanin content and on the expression of genes related to flavonoid metabolism in 54 Arabidopsis accessions covering a wide range of freezing tolerance. Most flavonols and anthocyanins accumulated upon cold exposure, but the extent of accumulation varied strongly among the accessions. This was also true for most of the investigated transcripts. Correlation analyses revealed a high degree of coordination among metabolites and among transcripts, but only little correlation between metabolites and transcripts, indicating an important role of post-transcriptional regulation in flavonoid metabolism. Similarly, levels of many flavonoid biosynthesis genes were correlated with freezing tolerance after cold acclimation, but only the pool sizes of a few flavonols and anthocyanins. Collectively, our data provide evidence for an important role of flavonoid metabolism in Arabidopsis freezing tolerance and point to the importance of post-transcriptional mechanisms in the regulation of flavonoid metabolism in response to cold. This article is protected by copyright. All rights reserved.
    Plant Cell and Environment 02/2015; 38(8). DOI:10.1111/pce.12518 · 6.96 Impact Factor

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    ABSTRACT: As multifaceted molecules, reactive oxygen species (ROS) are known to accumulate in response to various stresses. Ozone (O3) is an air pollutant with detrimental effect on plants, and O3 can also be used as a tool to study the role of ROS in signaling. Genetic variation of O3 sensitivity in different Arabidopsis accessions highlights the complex genetic architecture of plant responses to ROS. To investigate the genetic basis of O3 sensitivity, a recombinant inbred line (RIL) population between two Arabidopsis accessions with distinct O3 sensitivity, C24 (O3 tolerant) and Te (O3 sensitive), was used for quantitative trait loci (QTL) mapping. Through analysis of QTL mapping combined with transcriptome changes in response to O3, we identified three causal QTLs and several potential candidate genes regulating the response to O3. Based on gene expression data, water loss and stomatal conductance measurement, we found that a combination of relatively low stomatal conductance and constitutive activation of salicylic acid (SA) mediated defense signaling were responsible for the O3 tolerance in C24. Application of exogenous SA prior to O3 exposure can mimic the constitutive SA signaling in C24, and could attenuate O3 induced leaf damage in the sensitive Arabidopsis accessions Te and Cvi-0.
    Plant Cell and Environment 12/2014; DOI:10.1111/pce.12499 · 6.96 Impact Factor
  • Anja Thalhammer · Dirk K Hincha ·
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    ABSTRACT: Abstract Plants as sessile organisms are strongly challenged by environmental stresses. Many plants species are able to cold-acclimate, acquiring higher freezing tolerance upon exposure to low but non-freezing temperatures. Among a plethora of adaptational processes, this involves the accumulation of cold regulated (COR) proteins that are assumed to stabilize and protect cellular structures during freezing. However, their molecular functions are largely unknown. We recently reported a comprehensive study of two intrinsically disordered cold regulated chloroplast proteins, COR15A and COR15B from Arabidopsis thaliana. They are necessary for full cold acclimation. During freezing, they stabilize leaf cells through folding and binding to chloroplast membranes. Contrary to evidence from in-vitro experiments, they play no role in enzyme stabilization in vivo. Elucidating these major functional and structural characteristics and estimation of protein abundance allow us to propose a detailed model for the mode of action of the two COR15 proteins.
    Plant signaling & behavior 12/2014; 9(12). DOI:10.4161/15592324.2014.977722
  • Mai Q Le · Majken Pagter · Dirk K Hincha ·
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    ABSTRACT: During cold acclimation plants increase in freezing tolerance in response to low non-freezing temperatures. This is accompanied by many physiological, biochemical and molecular changes that have been extensively investigated. In addition, plants of many species, including Arabidopsis thaliana, become more freezing tolerant during exposure to mild, non-damaging sub-zero temperatures after cold acclimation. There is hardly any information available about the molecular basis of this adaptation. Here, we have used microarrays and a qRT-PCR primer platform covering 1,880 genes encoding transcription factors (TFs) to monitor changes in gene expression in the Arabidopsis accessions Columbia-0, Rschew and Tenela during the first 3 days of sub-zero acclimation at -3 °C. The results indicate that gene expression during sub-zero acclimation follows a tighly controlled time-course. Especially AP2/EREBP and WRKY TFs may be important regulators of sub-zero acclimation, although the CBF signal transduction pathway seems to be less important during sub-zero than during cold acclimation. Globally, we estimate that approximately 5 % of all Arabidopsis genes are regulated during sub-zero acclimation. Particularly photosynthesis-related genes are down-regulated and genes belonging to the functional classes of cell wall biosynthesis, hormone metabolism and RNA regulation of transcription are up-regulated. Collectively, these data provide the first global analysis of gene expression during sub-zero acclimation and allow the identification of candidate genes for forward and reverse genetic studies into the molecular mechanisms of sub-zero acclimation.
    Plant Molecular Biology 10/2014; 87(1-2). DOI:10.1007/s11103-014-0256-z · 4.26 Impact Factor
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    ABSTRACT: Alkaline/neutral invertases (A/N-Invs) are now recognized as essential proteins in plant life. They catalyze the irreversible break-down of sucrose into glucose and fructose and thus supply the cells with energy as well as signaling molecules. In this study we report on a mechanism that affects the activity of the cytosolic invertase AtCINV1 (At-A/N-InvG or AT1G35580). We demonstrate that Ser547 at the extreme C-terminus of the AtCINV1 protein is a substrate of calcium-dependent kinases (CPK3 and 21) and that phosphorylation creates a high-affinity binding site for 14-3-3 proteins. The invertase as such has basal activity, but we provide evidence that interaction with 14-3-3 proteins enhances its activity. The analysis of three quadruple 14-3-3 mutants generated from six T-DNA insertion mutants of the non-epsilon family shows both specificity as well as redundancy for this function of 14-3-3 proteins. The strong reduction in hexose levels in the roots of one 14-3-3 quadruple mutant plant is in line with the activating function of 14-3-3 proteins. The physiological relevance of this mechanism that affects A/N invertase activity is underscored by the light induced activation and is another example of the central role of 14-3-3 proteins in mediating dark/light signaling. The nature of the light induced signal that travels from the shoot to root and the question whether this signal is transmitted via cytosolic Ca++ changes that activate calcium-dependent kinases, await further study.This article is protected by copyright. All rights reserved.
    The Plant Journal 09/2014; 80(5). DOI:10.1111/tpj.12677 · 5.97 Impact Factor
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    Anja Thalhammer · Gary Bryant · Ronan Sulpice · Dirk K Hincha ·
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    ABSTRACT: Freezing can severely damage plants, limiting geographical distribution of natural populations and leading to major agronomical losses. Plants native to cold climates acquire increased freezing tolerance during exposure to low non-freezing temperatures in a process termed cold acclimation. This involves many adaptative responses, including global changes in metabolite content and gene expression, and the accumulation of cold regulated (COR) proteins, whose functions are largely unknown. Here we report that the chloroplast proteins COR15A and COR15B are necessary for full cold acclimation in Arabidopsis thaliana. They protect cell membranes, as indicated by electrolyte leakage and chlorophyll fluorescence measurements. Recombinant COR15 proteins stabilize lactate dehydrogenase during freezing in vitro. However, a transgenic approach shows that they have no influence on the stability of selected plastidic enzymes in vivo, although cold acclimation results in increased enzyme stability. This indicates that enzymes are stabilized by other mechanisms. Recombinant COR15 proteins are disordered in water, but fold into amphipathic α-helices at high osmolyte concentrations in the presence of membranes, a condition mimicking molecular crowding induced by dehydration during freezing. X-ray scattering experiments indicate protein-membrane interactions specifically under such crowding conditions. The COR15-membrane interactions lead to liposome stabilization during freezing. Collectively, our data demonstrate the requirement for COR15 accumulation for full cold acclimation of Arabidopsis. The function of these intrinsically disordered proteins is the stabilization of chloroplast membranes during freezing through a folding and binding mechanism, but not the stabilization of chloroplastic enzymes. This indicates a high functional specificity of these disordered plant proteins.
    Plant physiology 08/2014; 166(1). DOI:10.1104/pp.114.245399 · 6.84 Impact Factor
  • Dirk K Hincha · Ellen Zuther ·
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    ABSTRACT: This introductory chapter provides a brief overview of plant freezing tolerance and cold acclimation and describes the basic concepts and approaches that are currently followed to investigate these phenomena. We highlight the multidisciplinary nature of these investigations and the necessity to use methodologies from different branches of science, such as ecology, genetics, physiology, biochemistry, and biophysics, to come to a complete understanding of the complex adaptive mechanisms underlying plant cold acclimation.
    Methods in molecular biology (Clifton, N.J.) 05/2014; 1166:1-6. DOI:10.1007/978-1-4939-0844-8_1 · 1.29 Impact Factor
  • Anja Thalhammer · Dirk K Hincha · Ellen Zuther ·
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    ABSTRACT: Quantitative assessment of freezing tolerance is essential to unravel plant adaptations to cold temperatures. Not only the survival of whole plants but also impairment of detached leaves after a freeze-thaw cycle can be used to accurately quantify plant freezing tolerance in terms of LT50 values. Here we describe two methods to determine the freezing tolerance of detached leaves using different physiological parameters. Firstly, we illustrate how to assess the integrity of (predominantly) the plasma membrane during freezing using an electrolyte leakage assay. Secondly, we provide a chlorophyll fluorescence imaging protocol to determine the freezing tolerance of the photosynthetic apparatus.
    Methods in molecular biology (Clifton, N.J.) 05/2014; 1166:15-24. DOI:10.1007/978-1-4939-0844-8_3 · 1.29 Impact Factor
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    ABSTRACT: Main conclusion: Expression of eight LEA genes enhanced desiccation tolerance in yeast, including two LEA_2 genes encoding atypical, stably folded proteins. The recombinant proteins showed enzyme, but not membrane protection during drying. To screen for possible functions of late embryogenesis abundant (LEA) proteins in cellular stress tolerance, 15 candidate genes from six Arabidopsis thaliana LEA protein families were expressed in Saccharomyces cerevisiae as a genetically amenable eukaryotic model organism. Desiccation stress experiments showed that eight of the 15 LEA proteins significantly enhanced yeast survival. While none of the proteins belonging to the LEA_1, LEA_5 or AtM families provided protection to yeast cells, two of three LEA_2 proteins, all three LEA_4 proteins and three of four dehydrins were effective. However, no significantly enhanced tolerance toward freezing, salt, osmotic or oxidative stress was observed. While most LEA proteins are highly hydrophilic and intrinsically disordered, LEA_2 proteins are "atypical", since they are more hydrophobic and possess a stable folded structure in solution. Because nothing was known about the functional properties of LEA_2 proteins, we expressed the three Arabidopsis proteins LEA1, LEA26 and LEA27 in Escherichia coli. The bacteria expressed all three proteins in inclusion bodies from which they could be purified and refolded. Correct folding was ascertained by Fourier transform Infrared (FTIR) spectroscopy. None of the proteins was able to stabilize liposomes during freezing or drying, but they were all able to protect the enzyme lactate dehydrogenase (LDH) from inactivation during freezing. Significantly, only LEA1 and LEA27, which also protected yeast cells during drying, were able to stabilize LDH during desiccation and subsequent rehydration.
    Planta 05/2014; 240(2). DOI:10.1007/s00425-014-2089-z · 3.26 Impact Factor
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    Phuc T Do · Oliver Drechsel · Arnd G Heyer · Dirk K Hincha · Ellen Zuther ·
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    ABSTRACT: Soil salinity affects a large proportion of rural area and limits agricultural productivity. To investigate differential adaptation to soil salinity, we studied salt tolerance of 18 varieties of Oryza sativa using a hydroponic culture system. Based on visual inspection and photosynthetic parameters, cultivars were classified according to their tolerance level. Additionally, biomass parameters were correlated with salt tolerance. Polyamines have frequently been demonstrated to be involved in plant stress responses and therefore soluble leaf polyamines were measured. Under salinity, putrescine (Put) content was unchanged or increased in tolerant, while dropped in sensitive cultivars. Spermidine (Spd) content was unchanged at lower NaCl concentrations in all, while reduced at 100 mM NaCl in sensitive cultivars. Spermine (Spm) content was increased in all cultivars. A comparison with data from 21 cultivars under long-term, moderate drought stress revealed an increase of Spm under both stress conditions. While Spm became the most prominent polyamine under drought, levels of all three polyamines were relatively similar under salt stress. Put levels were reduced under both, drought and salt stress, while changes in Spd were different under drought (decrease) or salt (unchanged) conditions. Regulation of polyamine metabolism at the transcript level during exposure to salinity was studied for genes encoding enzymes involved in the biosynthesis of polyamines and compared to expression under drought stress. Based on expression profiles, investigated genes were divided into generally stress-induced genes (ADC2, SPD/SPM2, SPD/SPM3), one generally stress-repressed gene (ADC1), constitutively expressed genes (CPA1, CPA2, CPA4, SAMDC1, SPD/SPM1), specifically drought-induced genes (SAMDC2, AIH), one specifically drought-repressed gene (CPA3) and one specifically salt-stress repressed gene (SAMDC4), revealing both overlapping and specific stress responses under these conditions.
    Frontiers in Plant Science 05/2014; 5:182. DOI:10.3389/fpls.2014.00182 · 3.95 Impact Factor

Publication Stats

4k Citations
560.41 Total Impact Points


  • 2001-2015
    • Max Planck Institute of Molecular Plant Physiology
      • Division of Molecular Physiology
      Potsdam, Brandenburg, Germany
  • 2013
    • RWTH Aachen University
      • Institute for Biology II (Zoology)
      Aachen, North Rhine-Westphalia, Germany
  • 2010
    • Universität Potsdam
      Potsdam, Brandenburg, Germany
  • 1986-2006
    • University of Wuerzburg
      • Julius-von-Sachs-Institut of Biosciences
      Würzburg, Bavaria, Germany
  • 2000-2002
    • University of California, Davis
      • Department of Molecular and Cellular Biology
      Davis, California, United States
  • 1992-2001
    • Freie Universität Berlin
      • Institute of Biology
      Berlín, Berlin, Germany