Hans J Bohnert

Gyeongsang National University, Chinju, South Gyeongsang, South Korea

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Publications (100)553.27 Total impact

  • Source
    Article: Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis.
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    ABSTRACT: Environmental challenges to plants typically entail retardation of vegetative growth and delay or cessation of flowering. Here we report a link between the flowering time regulator, GIGANTEA (GI), and adaptation to salt stress that is mechanistically based on GI degradation under saline conditions, thus retarding flowering. GI, a switch in photoperiodicity and circadian clock control, and the SNF1-related protein kinase SOS2 functionally interact. In the absence of stress, the GI:SOS2 complex prevents SOS2-based activation of SOS1, the major plant Na(+)/H(+)-antiporter mediating adaptation to salinity. GI overexpressing, rapidly flowering, plants show enhanced salt sensitivity, whereas gi mutants exhibit enhanced salt tolerance and delayed flowering. Salt-induced degradation of GI confers salt tolerance by the release of the SOS2 kinase. The GI-SOS2 interaction introduces a higher order regulatory circuit that can explain in molecular terms, the long observed connection between floral transition and adaptive environmental stress tolerance in Arabidopsis.
    Nature Communications 01/2013; 4:1352. · 7.40 Impact Factor
  • Article: Regulation of miR399f transcription by AtMYB2 affects phosphate-starvation responses in Arabidopsis.
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    ABSTRACT: Although a role for microRNA399 (miR399) in plant responses to phosphate (Pi) starvation has been indicated, the regulatory mechanism underlying miR399 gene expression is not clear. Here we report that AtMYB2 functions as a direct transcriptional activator for miR399 in Arabidopsis Pi starvation signaling. Compared to untransformed control plants, transgenic plants constitutively overexpressing AtMYB2 showed increased miR399f expression and tissue Pi contents under high Pi growth, and exhibited elevated expression of a subset of Pi starvation-induced (PSI) genes. Pi-starvation-induced root architectural changes were more exaggerated in AtMYB2 overexpressing transgenic plants compared to wild type. AtMYB2 directly binds to a MYB-binding site in the miR399f promoter in vitro, as well as in vivo, and stimulates miR399f promoter activity in Arabidopsis protoplasts. Transcription of AtMYB2 itself is induced in response to Pi deficiency, and the tissue expression pattern of miR399f and AtMYB2 are similar. Both genes are expressed mainly in vascular tissues of cotyledons and in roots. Our results suggest that AtMYB2 regulates plant responses to Pi-starvation by regulating the expression of the miR399 gene.
    Plant physiology 11/2012; · 6.53 Impact Factor
  • Article: Overexpression of Arabidopsis YUCCA6 in potato results in high-auxin developmental phenotypes and enhanced resistance to water deficit.
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    ABSTRACT: Indole-3-acetic acid (IAA), a major plant auxin, is produced in both tryptophan-dependent and tryptophan-independent pathways. A major pathway in Arabidopsis thaliana generates IAA in two reactions from tryptophan. Step one converts tryptophan to indole-3-pyruvic acid (IPA) by tryptophan aminotransferases followed by a rate-limiting step converting IPA to IAA catalyzed by YUCCA proteins. We identified eight putative StYUC (Solanum tuberosum YUCCA) genes whose deduced amino acid sequences share 50 % to 70 % identity with those of Arabidopsis YUCCA proteins. All include canonical, conserved YUCCA sequences: FATGY motif, FMO signature sequence, and FAD-binding and NADP-binding sequences. In addition, five genes were found with ~50% amino acid sequence identity to Arabidopsis tryptophan aminotransferases. Transgenic potato (Solanum tuberosum cv Jowon) constitutively overexpressing Arabidopsis AtYUC6 displayed high auxin phenotypes such as narrow downward curled leaves, increased height, erect stature and longevity. Transgenic potato plants overexpressing AtYUC6 showed enhanced drought tolerance based on reduced water loss. The phenotype was correlated with reduced levels of reactive oxygen species in leaves. The results suggest a functional YUCCA pathway of auxin biosynthesis in potato that may be exploited to alter plant responses to the environment.
    Molecular Plant 09/2012; · 5.55 Impact Factor
  • Article: Ubiquitin and Ubiquitin-like Modifiers in Plants
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    ABSTRACT: Posttranslational modifications of proteins by small polypeptides including ubiquitination, neddylation (related to ubiquitin (RUB) conjugation), and sumoylation are implicated in plant growth and development, and they regulate protein degradation, location, and interaction with other proteins. Ubiquitination mediates the selective degradation of proteins by the ubiquitin (Ub)/proteasome pathway. The ubiquitin-like protein RUB is conjugated to cullins, which are part of a ubiquitin E3 ligase complex that is involved in auxin hormonal signaling. Sumoylation, by contrast, is known for its involvement in guiding protein interactions related to abiotic and biotic stresses and in the regulation of flowering time. ATG8/ATG12-mediated autophagy influences degradation and recycling of cellular components. Other ubiquitin-like modifiers (ULPs) such as homology to Ub-1, ubiquitin-fold modifier 1, and membrane-anchored Ub-fold are also found in Arabidopsis. ULPs share similar three-dimensional structures and a conjugation system, including E1 activating enzymes, E2 conjugation enzymes, and E3 ligases, as well as proteases for deconjugation and recycling of the tags. However, each of the ULP posttranslational modifications possesses its own specific enzymes and modifies its specific targets selectively. This review discusses recent findings on ubiquitination and ubiquitin-like modifier processes and their roles in the posttranslational modification of proteins in Arabidopsis. Keywords Arabidopsis –Posttranslational modification–Ubiquitination–Ubiquitin-like modifiers
    Journal of Plant Biology 04/2012; 54(5):275-285. · 1.07 Impact Factor
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    Article: Stress-adapted extremophiles provide energy without interference with food production
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    ABSTRACT: How to wean humanity off the use of fossil fuels continues to receive much attention but how to replace these fuels with renewable sources of energy has become a contentious field of debate as well as research, which often reflects economic and political factors rather than scientific good sense. It is clear that not every advertized energy source can lead to a sustainable, humane and environment-friendly path out of a future energy crisis. Our proposal is based on two assertions: that the use of food crops for biofuels is immoral, and that for this purpose using land suitable for growing crops productively is to be avoided. We advocate a focus on new “extremophile” crops. These would either be wild species adapted to extreme environments which express genes, developmental processes and metabolic pathways that distinguish them from traditional crops or existing crops genetically modified to withstand extreme environments. Such extremophile energy crops (EECs), will be less susceptible to stresses in a changing global environment and provide higher yields than existing crops. Moreover, they will grow on land that has never been valuable for agriculture or is no longer so, owing to centuries or millennia of imprudent exploitation. Such a policy will contribute to striking a balance between ecosystem protection and human resource management. Beyond that, rather than bulk liquid fuel generation, combustion of various biomass sources including extremophiles for generating electrical energy, and photovoltaics-based capture of solar energy, are superbly suitable candidates for powering the world in the future. Generating electricity and efficient storage capacity is quite possibly the only way for a sustainable post-fossil and, indeed, post-biofuel fuel economy. KeywordsAlternative crops–Bioenergy generation–Extremophiles–Abiotic stress tolerance–Food or fuel
    Food Security 04/2012; 3(1):93-105. · 1.97 Impact Factor
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    Article: Life at the extreme: lessons from the genome.
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    ABSTRACT: Extremophile plants thrive in places where most plant species cannot survive. Recent developments in high-throughput technologies and comparative genomics are shedding light on the evolutionary mechanisms leading to their adaptation.
    Genome biology 03/2012; 13(3):241. · 6.63 Impact Factor
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    Article: TsHKT1;2, a HKT1 homolog from the extremophile Arabidopsis relative Thellungiella salsuginea, shows K(+) specificity in the presence of NaCl.
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    ABSTRACT: Cellular Na(+)/K(+) ratio is a crucial parameter determining plant salinity stress resistance. We tested the function of plasma membrane Na(+)/K(+) cotransporters in the High-affinity K(+) Transporter (HKT) family from the halophytic Arabidopsis (Arabidopsis thaliana) relative Thellungiella salsuginea. T. salsuginea contains at least two HKT genes. TsHKT1;1 is expressed at very low levels, while the abundant TsHKT1;2 is transcriptionally strongly up-regulated by salt stress. TsHKT-based RNA interference in T. salsuginea resulted in Na(+) sensitivity and K(+) deficiency. The athkt1 mutant lines overexpressing TsHKT1;2 proved less sensitive to Na(+) and showed less K(+) deficiency than lines overexpressing AtHKT1. TsHKT1;2 ectopically expressed in yeast mutants lacking Na(+) or K(+) transporters revealed strong K(+) transporter activity and selectivity for K(+) over Na(+). Altering two amino acid residues in TsHKT1;2 to mimic the AtHKT1 sequence resulted in enhanced sodium uptake and loss of the TsHKT1;2 intrinsic K(+) transporter activity. We consider the maintenance of K(+) uptake through TsHKT1;2 under salt stress an important component supporting the halophytic lifestyle of T. salsuginea.
    Plant physiology 03/2012; 158(3):1463-74. · 6.53 Impact Factor
  • Article: Discovery of stress responsive DNA regulatory motifs in Arabidopsis.
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    ABSTRACT: The discovery of DNA regulatory motifs in the sequenced genomes using computational methods remains challenging. Here, we present MotifIndexer--a comprehensive strategy for de novo identification of DNA regulatory motifs at a genome level. Using word-counting methods, we indexed the existence of every 8-mer oligo composed of bases A, C, G, T, r, y, s, w, m, k, n or 12-mer oligo composed of A, C, G, T, n, in the promoters of all predicted genes of Arabidopsis thaliana genome and of selected stress-induced co-expressed genes. From this analysis, we identified number of over-represented motifs. Among these, major critical motifs were identified using a position filter. We used a model based on uniform distribution and the z-scores derived from this model to describe position bias. Interestingly, many motifs showed position bias towards the transcription start site. We extended this model to show biased distribution of motifs in the genomes of both A. thaliana and rice. We also used MotifIndexer to identify conserved motifs in co-expressed gene groups from two Arabidopsis species, A. thaliana and A. lyrata. This new comparative genomics method does not depend on alignments of homologous gene promoter sequences.
    PLoS ONE 01/2012; 7(8):e43198. · 4.09 Impact Factor
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    Article: Biotechnology for mechanisms that counteract salt stress in extremophile species: a genome-based view.
    Plant Biotechnology Reports 01/2012; · 1.19 Impact Factor
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    Article: SUMO and SUMOylation in plants.
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    ABSTRACT: The traditional focus on the central dogma of molecular biology, from gene through RNA to protein, has now been replaced by the recognition of an additional mechanism. The new regulatory mechanism, post-translational modifications to proteins, can actively alter protein function or activity introducing additional levels of functional complexity by altering cellular and sub-cellular location, protein interactions and the outcome of biochemical reaction chains. Modifications by ubiquitin (Ub) and ubiquitin-like modifiers systems are conserved in all eukaryotic organisms. One of them, small ubiquitin-like modifier (SUMO) is present in plants. The SUMO mechanism includes several isoforms of proteins that are involved in reactions of sumoylation and de-sumoylation. Sumoylation affects several important processes in plants. Outstanding among those are responses to environmental stresses. These may be abiotic stresses, such as phosphate deficiency, heat, low temperature, and drought, or biotic stressses, as well including defense reactions to pathogen infection. Also, the regulations of flowering time, cell growth and development, and nitrogen assimilation have recently been added to this list. Identification of SUMO targets is material to characterize the function of sumoylation or desumoylation. Affinity purification and mass spectrometric identification have been done lately in plants. Further SUMO noncovalent binding appears to have function in other model organisms and SUMO interacting proteins in plants will be of interest to plant biologists who dissect the dynamic function of SUMO. This review will discuss results of recent insights into the role of sumoylation in plants.
    Molecules and Cells 09/2011; 32(4):305-16. · 2.18 Impact Factor
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    Article: The genome of the extremophile crucifer Thellungiella parvula.
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    ABSTRACT: Thellungiella parvula is related to Arabidopsis thaliana and is endemic to saline, resource-poor habitats, making it a model for the evolution of plant adaptation to extreme environments. Here we present the draft genome for this extremophile species. Exclusively by next generation sequencing, we obtained the de novo assembled genome in 1,496 gap-free contigs, closely approximating the estimated genome size of 140 Mb. We anchored these contigs to seven pseudo chromosomes without the use of maps. We show that short reads can be assembled to a near-complete chromosome level for a eukaryotic species lacking prior genetic information. The sequence identifies a number of tandem duplications that, by the nature of the duplicated genes, suggest a possible basis for T. parvula's extremophile lifestyle. Our results provide essential background for developing genomically influenced testable hypotheses for the evolution of environmental stress tolerance.
    Nature Genetics 08/2011; 43(9):913-8. · 35.53 Impact Factor
  • Article: Identification and molecular properties of SUMO-binding proteins in Arabidopsis.
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    ABSTRACT: Reversible conjugation of the small ubiquitin modifier (SUMO) peptide to proteins (SUMOylation) plays important roles in cellular processes in animals and yeasts. However, little is known about plant SUMO targets. To identify SUMO substrates in Arabidopsis and to probe for biological functions of SUMO proteins, we constructed 6xHis-3xFLAG fused AtSUMO1 (HFAtSUMO1) controlled by the CaMV35S promoter for transformation into Arabidopsis Col-0. After heat treatment, an increased sumoylation pattern was detected in the transgenic plants. SUMO1-modified proteins were selected after two-dimensional gel electrophoresis (2-DE) image analysis and identified using matrix-assisted laser-desorption ionization time-of-flight mass spectrometry (MALDI-TOF MS). We identified 27 proteins involved in a variety of processes such as nucleic acid metabolism, signaling, metabolism, and including proteins of unknown functions. Binding and sumoylation patterns were confirmed independently. Surprisingly, MCM3 (At5G46280), a DNA replication licensing factor, only interacted with and became sumoylated by AtSUMO1, but not by SUMO1ΔGG or AtSUMO3. The results suggest specific interactions between sumoylation targets and particular sumoylation enzymes.
    Molecules and Cells 05/2011; 32(2):143-51. · 2.18 Impact Factor
  • Article: SIZ1 regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation.
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    ABSTRACT: Phosphate (Pi) limitation causes plants to modulate the architecture of their root systems to facilitate the acquisition of Pi. Previously, we reported that the Arabidopsis (Arabidopsis thaliana) SUMO E3 ligase SIZ1 regulates root architecture remodeling in response to Pi limitation; namely, the siz1 mutations cause the inhibition of primary root (PR) elongation and the promotion of lateral root (LR) formation. Here, we present evidence that SIZ1 is involved in the negative regulation of auxin patterning to modulate root system architecture in response to Pi starvation. The siz1 mutations caused greater PR growth inhibition and LR development of seedlings in response to Pi limitation. Similar root phenotypes occurred if Pi-deficient wild-type seedlings were supplemented with auxin. N-1-Naphthylphthalamic acid, an inhibitor of auxin efflux activity, reduced the Pi starvation-induced LR root formation of siz1 seedlings to a level equivalent to that seen in the wild type. Monitoring of the auxin-responsive reporter DR5::uidA indicated that auxin accumulates in PR tips at early stages of the Pi starvation response. Subsequently, DR5::uidA expression was observed in the LR primordia, which was associated with LR elongation. The time-sequential patterning of DR5::uidA expression occurred earlier in the roots of siz1 as compared with the wild type. In addition, microarray analysis revealed that several other auxin-responsive genes, including genes involved in cell wall loosening and biosynthesis, were up-regulated in siz1 relative to wild-type seedlings in response to Pi starvation. Together, these results suggest that SIZ1 negatively regulates Pi starvation-induced root architecture remodeling through the control of auxin patterning.
    Plant physiology 02/2011; 155(2):1000-12. · 6.53 Impact Factor
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    Article: Transcription strength and halophytic lifestyle.
    Trends in Plant Science 01/2011; 16(1):1-3. · 11.05 Impact Factor
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    Article: NKS1, Na(+)- and K(+)-sensitive 1, regulates ion homeostasis in an SOS-independent pathway in Arabidopsis.
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    ABSTRACT: An Arabidopsis thaliana mutant, nks1-1, exhibiting enhanced sensitivity to NaCl was identified in a screen of a T-DNA insertion population in the genetic background of Col-0 gl1sos3-1. Analysis of the genome sequence in the region flanking the T-DNA left border indicated two closely linked mutations in the gene encoded at locus At4g30996. A second allele, nks1-2, was obtained from the Arabidopsis Biological Resource Center. NKS1 mRNA was detected in all parts of wild-type plants but was not detected in plants of either mutant, indicating inactivation by the mutations. Both mutations in NKS1 were associated with increased sensitivity to NaCl and KCl, but not to LiCl or mannitol. NaCl sensitivity was associated with nks1 mutations in Arabidopsis lines expressing either wild type or null alleles of SOS1, SOS2 or SOS3. The NaCl-sensitive phenotype of the nks1-2 mutant was complemented by expression of a full-length NKS1 allele from the CaMV35S promoter. When grown in medium containing NaCl, nks1 mutants accumulated more Na(+) than wild type and K(+)/Na(+) homeostasis was perturbed. It is proposed NKS1, a plant-specific gene encoding a 19kDa endomembrane-localized protein of unknown function, is part of an ion homeostasis regulation pathway that is independent of the SOS pathway.
    Phytochemistry 01/2011; 72(4-5):330-6. · 3.35 Impact Factor
  • Chapter: Molecular Biology and Physiological Genomics of Dehydration Stress
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    ABSTRACT: The loss of water, leading to dehydration and, in severe instances, desiccation affects cellular homeostasis and ultimately generates organismal stress with every aspect of plant anatomy, morphology, physiology, and biochemistry adversely affected. Growth and yield are, and survival may be, compromised. Only in one part of the life cycle of most angiosperms, seed maturation – a no-growth developmental process – can natural drought adaptation strategies be observed. With the genomics and bioinformatics resources that are increasingly becoming available for a number of model plant species, and increasingly now also for crop species, we can begin to ask basic questions that address the genetic basis for dehydration tolerance in unprecedented detail. Significantly, genomics datasets let us ask questions that do not strictly require working with a desiccation-tolerant species. Arabidopsis thaliana, as the most completely developed model plant, provides sufficient complexity, including many ecotypes and related species. To investigate the regulatory mechanisms underlying elements of dehydration tolerances that vary by degree and depend on developmental windows, genomics tools with a justifiable claim to being all-encompassing can now be applied. The reactions of resurrection plants, which seem to apply different strategies to the drought survival and re-hydration problem, can provide valuable lessons that may be tested in sufficiently developed model species. We will include discussions about physiological markers that can now be understood in the context of genes and their concerted functioning. Furthermore, it is appropriate to contrast the fast dehydration stress experiments on which most of our knowledge is based with the drying that characterizes plants in their natural habitats. Although individual components of stress response systems have been studied under conditions of water deficiency, the overall “network logic” of the components and pathways that exist and which must be operational to bring about dehydration tolerance remain largely unknown, but, we think, not for much longer.
    12/2010: pages 255-287;
  • Chapter: Physiological Roles for the PIP Family of Plant Aquaporins
    Rosario Vera-Estrella, Hans J. Bohnert
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    ABSTRACT: Aquaporins are a class of intrinsic membrane proteins that are primarily associated with water movement across membranes. In plants, biophysical studies indicated that water fluxes could not be explained by simple diffusive movement. The discovery of aquaporins that facilitate water movement across membranes in other organisms rapidly led to the identification of this class of proteins in plants. The large number of aquaporin genes identified in plant genomes compared to those from other organisms suggests that they play a major role in plant water relations. However, plant aquaporins also facilitate the transport of small solutes such as glycerol, silicon, ammonium, urea, boric acid, CO2, arsenite, and hydrogen peroxide within and between cells. Here, the aquaporin-like proteins that function on the plant plasma membrane are reviewed in the context of their apparent role in plant adaptive evolution.
    11/2010: pages 193-222;
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    Article: Comparative transcriptomics for mangrove species: an expanding resource.
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    ABSTRACT: We present here the Mangrove Transcriptome Database (MTDB), an integrated, web-based platform providing transcript information from all 28 mangrove species for which information is available. Sequences are annotated, and when possible, GO clustered and assigned to KEGG pathways, making MTDB a valuable resource for approaching mangrove or other extremophile biology from the transcriptomic level. As one example outlining the potential of MTDB, we highlight the analysis of mangrove microRNA (miRNA) precursor sequences, miRNA target sites, and their conservation and divergence compared with model plants. MTDB is available at http://mangrove.illinois.edu .
    Functional & Integrative Genomics 11/2010; 10(4):523-32. · 3.83 Impact Factor
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    Article: Genome structures and halophyte-specific gene expression of the extremophile Thellungiella parvula in comparison with Thellungiella salsuginea (Thellungiella halophila) and Arabidopsis.
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    ABSTRACT: The genome of Thellungiella parvula, a halophytic relative of Arabidopsis (Arabidopsis thaliana), is being assembled using Roche-454 sequencing. Analyses of a 10-Mb scaffold revealed synteny with Arabidopsis, with recombination and inversion and an uneven distribution of repeat sequences. T. parvula genome structure and DNA sequences were compared with orthologous regions from Arabidopsis and publicly available bacterial artificial chromosome sequences from Thellungiella salsuginea (previously Thellungiella halophila). The three-way comparison of sequences, from one abiotic stress-sensitive species and two tolerant species, revealed extensive sequence conservation and microcolinearity, but grouping Thellungiella species separately from Arabidopsis. However, the T. parvula segments are distinguished from their T. salsuginea counterparts by a pronounced paucity of repeat sequences, resulting in a 30% shorter DNA segment with essentially the same gene content in T. parvula. Among the genes is SALT OVERLY SENSITIVE1 (SOS1), a sodium/proton antiporter, which represents an essential component of plant salinity stress tolerance. Although the SOS1 coding region is highly conserved among all three species, the promoter regions show conservation only between the two Thellungiella species. Comparative transcript analyses revealed higher levels of basal as well as salt-induced SOS1 expression in both Thellungiella species as compared with Arabidopsis. The Thellungiella species and other halophytes share conserved pyrimidine-rich 5' untranslated region proximal regions of SOS1 that are missing in Arabidopsis. Completion of the genome structure of T. parvula is expected to highlight distinctive genetic elements underlying the extremophile lifestyle of this species.
    Plant physiology 11/2010; 154(3):1040-52. · 6.53 Impact Factor
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    Article: Functional characterization of the SIZ/PIAS-type SUMO E3 ligases, OsSIZ1 and OsSIZ2 in rice.
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    ABSTRACT: Sumoylation is a post-translational regulatory process in diverse cellular processes in eukaryotes, involving conjugation/deconjugation of small ubiquitin-like modifier (SUMO) proteins to other proteins thus modifying their function. The PIAS [protein inhibitor of activated signal transducers and activators of transcription (STAT)] and SAP (scaffold attachment factor A/B/acinus/PIAS)/MIZ (SIZ) proteins exhibit SUMO E3-ligase activity that facilitates the conjugation of SUMO proteins to target substrates. Here, we report the isolation and molecular characterization of Oryza sativa SIZ1 (OsSIZ1) and SIZ2 (OsSIZ2), rice homologs of Arabidopsis SIZ1. The rice SIZ proteins are localized to the nucleus and showed sumoylation activities in a tobacco system. Our analysis showed increased amounts of SUMO conjugates associated with environmental stresses such as high and low temperature, NaCl and abscisic acid (ABA) in rice plants. The expression of OsSIZ1 and OsSIZ2 in siz1-2 Arabidopsis plants partially complemented the morphological mutant phenotype and enhanced levels of SUMO conjugates under heat shock conditions. In addition, ABA-hypersensitivity of siz1-2 seed germination was partially suppressed by OsSIZ1 and OsSIZ2. The results suggest that rice SIZ1 and SIZ2 are able to functionally complement Arabidopsis SIZ1 in the SUMO conjugation pathway. Their effects on the Arabidopsis mutant suggest a function for these genes related to stress responses and stress adaptation.
    Plant Cell and Environment 11/2010; 33(11):1923-34. · 5.22 Impact Factor

Institutions

  • 2007–2013
    • Gyeongsang National University
      • Plant Molecular Biology and Biotechnology Research Center
      Chinju, South Gyeongsang, South Korea
  • 2012
    • Molecular and Cellular Biology Program
      Seattle, WA, USA
  • 2004–2012
    • University of Illinois, Urbana-Champaign
      • Department of Plant Biology
      Urbana, IL, USA
  • 2000–2012
    • Purdue University
      • • Department of Biochemistry
      • • Center for Plant Environmental Stress Physiology
      West Lafayette, IN, USA
    • University of Nevada, Reno
      Reno, NV, USA
  • 2008
    • University of Vienna
      Vienna, Vienna, Austria
  • 2006–2008
    • Virginia Polytechnic Institute and State University
      • • Department of Plant Pathology, Physiology, and Weed Science
      • • Department of Computer Science
      Blacksburg, VA, USA
  • 1986–2006
    • The University of Arizona
      • • Department of Chemistry and Biochemistry (College of Science)
      • • School of Plant Sciences
      • • Department of Molecular and Cellular Biology
      Tucson, AZ, USA
  • 1988
    • Universität Würzburg
      Würzburg, Bavaria, Germany