Publications by authors named "Hans J Bohnert"

77 Publications

Metabolic Adjustment of Arabidopsis Root Suspension Cells During Adaptation to Salt Stress and Mitotic Stress Memory.

Plant Cell Physiol 2019 Mar;60(3):612-625

Institute of Agriculture & Life Science, Gyeongsang National University, Jinju, Korea.

Sessile plants reprogram their metabolic and developmental processes during adaptation to prolonged environmental stresses. To understand the molecular mechanisms underlying adaptation of plant cells to saline stress, we established callus suspension cell cultures from Arabidopsis roots adapted to high salt for an extended period of time. Adapted cells exhibit enhanced salt tolerance compared with control cells. Moreover, acquired salt tolerance is maintained even after the stress is relieved, indicating the existence of a memory of acquired salt tolerance during mitotic cell divisions, known as mitotic stress memory. Metabolite profiling using 1H-nuclear magnetic resonance (NMR) spectroscopy revealed metabolic discrimination between control, salt-adapted and stress-memory cells. Compared with control cells, salt-adapted cells accumulated higher levels of sugars, amino acids and intermediary metabolites in the shikimate pathway, such as coniferin. Moreover, adapted cells acquired thicker cell walls with higher lignin contents, suggesting the importance of adjustments of physical properties during adaptation to elevated saline conditions. When stress-memory cells were reverted to normal growth conditions, the levels of metabolites again readjusted. Whereas most of the metabolic changes reverted to levels intermediate between salt-adapted and control cells, the amounts of sugars, alanine, γ-aminobutyric acid and acetate further increased in stress-memory cells, supporting a view of their roles in mitotic stress memory. Our results provide insights into the metabolic adjustment of plant root cells during adaptation to saline conditions as well as pointing to the function of mitotic memory in acquired salt tolerance.
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http://dx.doi.org/10.1093/pcp/pcy231DOI Listing
March 2019

A comprehensive analysis of the Korean fir (Abies koreana) genes expressed under heat stress using transcriptome analysis.

Sci Rep 2018 07 6;8(1):10233. Epub 2018 Jul 6.

Division of Ecological Conservation, Bureau of Ecological Research, National Institute of Ecology, Seocheon, Republic of Korea.

Korean fir (Abies koreana), a rare species endemic to South Korea, is sensitive to climate change. Here, we used next-generation massively parallel sequencing technology and de novo transcriptome assembly to gain a comprehensive overview of the Korean fir transcriptome under heat stress. Sequencing control and heat-treated samples of Korean fir, we obtained more than 194,872,650 clean reads from each sample. After de novo assembly and quantitative assessment, 42,056 unigenes were generated with an average length of 908 bp. In total, 6,401 differentially expressed genes were detected, of which 2,958 were up-regulated and 3,443 down-regulated, between the heat-treated and control samples. A gene ontology analysis of these unigenes revealed heat-stress-related terms, such as "response to stimulus". Further, in depth analysis revealed 204 transcription factors and 189 Hsps as differentially expressed. Finally, 12 regulated candidate genes associated with heat stress were examined using quantitative real-time PCR (qRT-PCR). In this study, we present the first comprehensive characterisation of Korean fir subjected to heat stress using transcriptome analysis. It provides an important resource for future studies of Korean fir with the objective of identifying heat stress tolerant lines.
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http://dx.doi.org/10.1038/s41598-018-28552-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6035224PMC
July 2018

A Single Amino-Acid Substitution in the Sodium Transporter HKT1 Associated with Plant Salt Tolerance.

Plant Physiol 2016 07 9;171(3):2112-26. Epub 2016 May 9.

Division of Applied Life Science (BK21 Plus Program), Gyeongsang National University, Jinju 660-701, Republic of Korea (A.A., R.A., S.K., M.J., D.B., I.U.K., S.Y.L., K.W.L., H.J.B., D.-J.Y.); Plant Biophysics, Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid, Campus de Montegancedo, Carretera M-40, km 37.7, E-28223 Pozuelo de Alarcón Madrid (N.R.);Division of Ecological Adaptation Research, National Institute of Ecology (NIE), Seocheon 325-813, Republic of Korea (H.C.P.); Department of Biology, Louisiana State University, Baton Rouge, Louisiana 70803 (D.-H.O.);Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907-2010 (R.A.B.);Department of Agriculture, University of Naples Federico II, Via Universita` 100, Portici, I-80055, Italy (A.M.);Instituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Cientificas, 41092 Sevilla, Spain (J.M.P.); College of Science, King Abdulaziz University, Jeddah 21589, KSA (H.J.B.); and Department of Plant Biology, University of Illinois, Urbana-Champaign, Urbana, Illinois 61801 (H.J.B.)

A crucial prerequisite for plant growth and survival is the maintenance of potassium uptake, especially when high sodium surrounds the root zone. The Arabidopsis HIGH-AFFINITY K(+) TRANSPORTER1 (HKT1), and its homologs in other salt-sensitive dicots, contributes to salinity tolerance by removing Na(+) from the transpiration stream. However, TsHKT1;2, one of three HKT1 copies in Thellungiella salsuginea, a halophytic Arabidopsis relative, acts as a K(+) transporter in the presence of Na(+) in yeast (Saccharomyces cerevisiae). Amino-acid sequence comparisons indicated differences between TsHKT1;2 and most other published HKT1 sequences with respect to an Asp residue (D207) in the second pore-loop domain. Two additional T salsuginea and most other HKT1 sequences contain Asn (n) in this position. Wild-type TsHKT1;2 and altered AtHKT1 (AtHKT1(N-D)) complemented K(+)-uptake deficiency of yeast cells. Mutant hkt1-1 plants complemented with both AtHKT1(N) (-) (D) and TsHKT1;2 showed higher tolerance to salt stress than lines complemented by the wild-type AtHKT1 Electrophysiological analysis in Xenopus laevis oocytes confirmed the functional properties of these transporters and the differential selectivity for Na(+) and K(+) based on the n/d variance in the pore region. This change also dictated inward-rectification for Na(+) transport. Thus, the introduction of Asp, replacing Asn, in HKT1-type transporters established altered cation selectivity and uptake dynamics. We describe one way, based on a single change in a crucial protein that enabled some crucifer species to acquire improved salt tolerance, which over evolutionary time may have resulted in further changes that ultimately facilitated colonization of saline habitats.
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http://dx.doi.org/10.1104/pp.16.00569DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4936583PMC
July 2016

A novel thiol-reductase activity of Arabidopsis YUC6 confers drought tolerance independently of auxin biosynthesis.

Nat Commun 2015 Aug 28;6:8041. Epub 2015 Aug 28.

Division of Applied Life Science (BK21Plus), PMBBRC &IALS, Gyeongsang National University, Jinju 660-701, Republic of Korea.

YUCCA (YUC) proteins constitute a family of flavin monooxygenases (FMOs), with an important role in auxin (IAA) biosynthesis. Here we report that Arabidopsis plants overexpressing YUC6 display enhanced IAA-related phenotypes and exhibit improved drought stress tolerance, low rate of water loss and controlled ROS accumulation under drought and oxidative stresses. Co-overexpression of an IAA-conjugating enzyme reduces IAA levels but drought stress tolerance is unaffected, indicating that the stress-related phenotype is not based on IAA overproduction. YUC6 contains a previously unrecognized FAD- and NADPH-dependent thiol-reductase activity (TR) that overlaps with the FMO domain involved in IAA biosynthesis. Mutation of a conserved cysteine residue (Cys-85) preserves FMO but suppresses TR activity and stress tolerance, whereas mutating the FAD- and NADPH-binding sites, that are common to TR and FMO domains, abolishes all outputs. We provide a paradigm for a single protein playing a dual role, regulating plant development and conveying stress defence responses.
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http://dx.doi.org/10.1038/ncomms9041DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4560777PMC
August 2015

Cell type-specific responses to salinity - the epidermal bladder cell transcriptome of Mesembryanthemum crystallinum.

New Phytol 2015 Aug 5;207(3):627-44. Epub 2015 May 5.

Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, 70803, USA.

Mesembryanthemum crystallinum (ice plant) exhibits extreme tolerance to salt. Epidermal bladder cells (EBCs), developing on the surface of aerial tissues and specialized in sodium sequestration and other protective functions, are critical for the plant's stress adaptation. We present the first transcriptome analysis of EBCs isolated from intact plants, to investigate cell type-specific responses during plant salt adaptation. We developed a de novo assembled, nonredundant EBC reference transcriptome. Using RNAseq, we compared the expression patterns of the EBC-specific transcriptome between control and salt-treated plants. The EBC reference transcriptome consists of 37 341 transcript-contigs, of which 7% showed significantly different expression between salt-treated and control samples. We identified significant changes in ion transport, metabolism related to energy generation and osmolyte accumulation, stress signalling, and organelle functions, as well as a number of lineage-specific genes of unknown function, in response to salt treatment. The salinity-induced EBC transcriptome includes active transcript clusters, refuting the view of EBCs as passive storage compartments in the whole-plant stress response. EBC transcriptomes, differing from those of whole plants or leaf tissue, exemplify the importance of cell type-specific resolution in understanding stress adaptive mechanisms.
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http://dx.doi.org/10.1111/nph.13414DOI Listing
August 2015

AtGGM2014, an Arabidopsis gene co-expression network for functional studies.

Sci China Life Sci 2015 Mar 14;58(3):276-86. Epub 2015 Feb 14.

Department of Plant Biology and the Genome Center, College of Biological Sciences, University of California, Davis, CA, 95616, USA,

Gene co-expression networks provide an important tool for systems biology studies. Using microarray data from the ArrayExpress database, we constructed an Arabidopsis gene co-expression network, termed AtGGM2014, based on the graphical Gaussian model, which contains 102,644 co-expression gene pairs among 18,068 genes. The network was grouped into 622 gene co-expression modules. These modules function in diverse house-keeping, cell cycle, development, hormone response, metabolism, and stress response pathways. We developed a tool to facilitate easy visualization of the expression patterns of these modules either in a tissue context or their regulation under different treatment conditions. The results indicate that at least six modules with tissue-specific expression pattern failed to record modular regulation under various stress conditions. This discrepancy could be best explained by the fact that experiments to study plant stress responses focused mainly on leaves and less on roots, and thus failed to recover specific regulation pattern in other tissues. Overall, the modular structures revealed by our network provide extensive information to generate testable hypotheses about diverse plant signaling pathways. AtGGM2014 offers a constructive tool for plant systems biology studies.
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http://dx.doi.org/10.1007/s11427-015-4803-xDOI Listing
March 2015

Pathogen associated molecular pattern (PAMP)-triggered immunity is compromised under C-limited growth.

Mol Cells 2015 Jan 12;38(1):40-50. Epub 2014 Nov 12.

Division of Applied Life Science (BK21 Plus Program) and Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju 660-701, Korea.

In the interaction between plants and pathogens, carbon (C) resources provide energy and C skeletons to maintain, among many functions, the plant immune system. However, variations in C availability on pathogen associated molecular pattern (PAMP) triggered immunity (PTI) have not been systematically examined. Here, three types of starch mutants with enhanced susceptibility to Pseudomonas syringae pv. tomato DC3000 hrcC were examined for PTI. In a dark period-dependent manner, the mutants showed compromised induction of a PTI marker, and callose accumulation in response to the bacterial PAMP flagellin, flg22. In combination with weakened PTI responses in wild type by inhibition of the TCA cycle, the experiments determined the necessity of C-derived energy in establishing PTI. Global gene expression analyses identified flg22 responsive genes displaying C supply-dependent patterns. Nutrient recycling-related genes were regulated similarly by C-limitation and flg22, indicating re-arrangements of expression programs to redirect resources that establish or strengthen PTI. Ethylene and NAC transcription factors appear to play roles in these processes. Under C-limitation, PTI appears compromised based on suppression of genes required for continued biosynthetic capacity and defenses through flg22. Our results provide a foundation for the intuitive perception of the interplay between plant nutrition status and pathogen defense.
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http://dx.doi.org/10.14348/molcells.2015.2165DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4314131PMC
January 2015

Genome structures and transcriptomes signify niche adaptation for the multiple-ion-tolerant extremophyte Schrenkiella parvula.

Plant Physiol 2014 Apr 21;164(4):2123-38. Epub 2014 Feb 21.

Department of Biology, Louisiana State University, Baton Rouge, Louisiana 70803.

Schrenkiella parvula (formerly Thellungiella parvula), a close relative of Arabidopsis (Arabidopsis thaliana) and Brassica crop species, thrives on the shores of Lake Tuz, Turkey, where soils accumulate high concentrations of multiple-ion salts. Despite the stark differences in adaptations to extreme salt stresses, the genomes of S. parvula and Arabidopsis show extensive synteny. S. parvula completes its life cycle in the presence of Na⁺, K⁺, Mg²⁺, Li⁺, and borate at soil concentrations lethal to Arabidopsis. Genome structural variations, including tandem duplications and translocations of genes, interrupt the colinearity observed throughout the S. parvula and Arabidopsis genomes. Structural variations distinguish homologous gene pairs characterized by divergent promoter sequences and basal-level expression strengths. Comparative RNA sequencing reveals the enrichment of ion-transport functions among genes with higher expression in S. parvula, while pathogen defense-related genes show higher expression in Arabidopsis. Key stress-related ion transporter genes in S. parvula showed increased copy number, higher transcript dosage, and evidence for subfunctionalization. This extremophyte offers a framework to identify the requisite adjustments of genomic architecture and expression control for a set of genes found in most plants in a way to support distinct niche adaptation and lifestyles.
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http://dx.doi.org/10.1104/pp.113.233551DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3982767PMC
April 2014

Incorporating motif analysis into gene co-expression networks reveals novel modular expression pattern and new signaling pathways.

PLoS Genet 2013 3;9(10):e1003840. Epub 2013 Oct 3.

Department of Plant Biology and the Genome Center, College of Biological Sciences, University of California, Davis, Davis, California, United States of America.

Understanding of gene regulatory networks requires discovery of expression modules within gene co-expression networks and identification of promoter motifs and corresponding transcription factors that regulate their expression. A commonly used method for this purpose is a top-down approach based on clustering the network into a range of densely connected segments, treating these segments as expression modules, and extracting promoter motifs from these modules. Here, we describe a novel bottom-up approach to identify gene expression modules driven by known cis-regulatory motifs in the gene promoters. For a specific motif, genes in the co-expression network are ranked according to their probability of belonging to an expression module regulated by that motif. The ranking is conducted via motif enrichment or motif position bias analysis. Our results indicate that motif position bias analysis is an effective tool for genome-wide motif analysis. Sub-networks containing the top ranked genes are extracted and analyzed for inherent gene expression modules. This approach identified novel expression modules for the G-box, W-box, site II, and MYB motifs from an Arabidopsis thaliana gene co-expression network based on the graphical Gaussian model. The novel expression modules include those involved in house-keeping functions, primary and secondary metabolism, and abiotic and biotic stress responses. In addition to confirmation of previously described modules, we identified modules that include new signaling pathways. To associate transcription factors that regulate genes in these co-expression modules, we developed a novel reporter system. Using this approach, we evaluated MYB transcription factor-promoter interactions within MYB motif modules.
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http://dx.doi.org/10.1371/journal.pgen.1003840DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3789834PMC
March 2014

Using Arabidopsis-related model species (ARMS): growth, genetic transformation, and comparative genomics.

Methods Mol Biol 2014 ;1062:27-51

CNR-IGV Institute of Plant Genetics, Portici, Italy.

The Arabidopsis-related model species (ARMS) Thellungiella salsuginea and Thellungiella parvula have generated broad interest in salt stress research. While general growth characteristics of these species are similar to Arabidopsis, some aspects of their life cycle require particular attention in order to obtain healthy plants, with a large production of seeds in a relatively short time. This chapter describes basic procedures for growth, maintenance, and Agrobacterium-mediated transformation of ARMS. Where appropriate, differences in requirements between Thellungiella spp. and Arabidopsis are highlighted, along with basic growth requirements of other less studied candidate model species. Current techniques for comparative genomics analysis between Arabidopsis and ARMS are also described in detail.
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http://dx.doi.org/10.1007/978-1-62703-580-4_2DOI Listing
April 2014

Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis.

Nat Commun 2013 ;4:1352

Division of Applied Life Science (BK21 Program), Plant Molecular Biology and Biotechnology Research Center, Graduate School of Gyeongsang National University, Jinju 660-701, South Korea.

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.
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http://dx.doi.org/10.1038/ncomms2357DOI Listing
June 2013

Regulation of miR399f transcription by AtMYB2 affects phosphate starvation responses in Arabidopsis.

Plant Physiol 2013 Jan 15;161(1):362-73. Epub 2012 Nov 15.

Division of Applied Life Science-BK21 Program, Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju 660-701, Korea.

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 (Arabidopsis thaliana) Pi starvation signaling. Compared with 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 genes. Pi starvation-induced root architectural changes were more exaggerated in AtMYB2-overexpressing transgenic plants compared with the 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 patterns 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.
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http://dx.doi.org/10.1104/pp.112.205922DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3532267PMC
January 2013

Overexpression of Arabidopsis YUCCA6 in potato results in high-auxin developmental phenotypes and enhanced resistance to water deficit.

Mol Plant 2013 Mar 17;6(2):337-49. Epub 2012 Sep 17.

Department of Biochemistry, Purdue University, West Lafayette, IN 47907, USA.

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%-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.
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http://dx.doi.org/10.1093/mp/sss100DOI Listing
March 2013

Discovery of stress responsive DNA regulatory motifs in Arabidopsis.

PLoS One 2012 13;7(8):e43198. Epub 2012 Aug 13.

Department of Plant Biology and the Genome Center, College of Biological Sciences, University of California Davis, Davis, California, United States of America.

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.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0043198PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3418279PMC
May 2013

Insights into salt tolerance from the genome of Thellungiella salsuginea.

Proc Natl Acad Sci U S A 2012 Jul 9;109(30):12219-24. Epub 2012 Jul 9.

State Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China.

Thellungiella salsuginea, a close relative of Arabidopsis, represents an extremophile model for abiotic stress tolerance studies. We present the draft sequence of the T. salsuginea genome, assembled based on ~134-fold coverage to seven chromosomes with a coding capacity of at least 28,457 genes. This genome provides resources and evidence about the nature of defense mechanisms constituting the genetic basis underlying plant abiotic stress tolerance. Comparative genomics and experimental analyses identified genes related to cation transport, abscisic acid signaling, and wax production prominent in T. salsuginea as possible contributors to its success in stressful environments.
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http://dx.doi.org/10.1073/pnas.1209954109DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3409768PMC
July 2012

Life at the extreme: lessons from the genome.

Genome Biol 2012 ;13(3):241

Department of Plant Biology, University of Illinois at Urbana-Champaign, 61801, USA.

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.
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http://dx.doi.org/10.1186/gb-2012-13-3-241DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3439964PMC
September 2012

TsHKT1;2, a HKT1 homolog from the extremophile Arabidopsis relative Thellungiella salsuginea, shows K(+) specificity in the presence of NaCl.

Plant Physiol 2012 Mar 11;158(3):1463-74. Epub 2012 Jan 11.

Division of Applied Life Science (Brain Korea 21 Program) and Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju 660-701, Korea.

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.
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http://dx.doi.org/10.1104/pp.111.193110DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3291249PMC
March 2012

SUMO and SUMOylation in plants.

Mol Cells 2011 Oct 9;32(4):305-16. Epub 2011 Sep 9.

Division of Applied Life Science (Brain Korea 21 Program), and Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju 660-701, Korea.

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.
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http://dx.doi.org/10.1007/s10059-011-0122-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3887640PMC
October 2011

The genome of the extremophile crucifer Thellungiella parvula.

Nat Genet 2011 Aug 7;43(9):913-8. Epub 2011 Aug 7.

Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA.

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.
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http://dx.doi.org/10.1038/ng.889DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3586812PMC
August 2011

Identification and molecular properties of SUMO-binding proteins in Arabidopsis.

Mol Cells 2011 Aug 20;32(2):143-51. Epub 2011 May 20.

Division of Applied Life Science (Brain Korea 21 Program), and Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju 660-701, Korea.

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.
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http://dx.doi.org/10.1007/s10059-011-2297-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3887670PMC
August 2011

NKS1, Na(+)- and K(+)-sensitive 1, regulates ion homeostasis in an SOS-independent pathway in Arabidopsis.

Phytochemistry 2011 Apr 10;72(4-5):330-6. Epub 2011 Jan 10.

Division of Applied Life Science (BK21 Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju 660-701, Republic of Korea.

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.
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http://dx.doi.org/10.1016/j.phytochem.2010.12.005DOI Listing
April 2011

SIZ1 regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation.

Plant Physiol 2011 Feb 14;155(2):1000-12. Epub 2010 Dec 14.

Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba 305-8572, Japan.

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.
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http://dx.doi.org/10.1104/pp.110.165191DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3032448PMC
February 2011

Genome structures and halophyte-specific gene expression of the extremophile Thellungiella parvula in comparison with Thellungiella salsuginea (Thellungiella halophila) and Arabidopsis.

Plant Physiol 2010 Nov 10;154(3):1040-52. Epub 2010 Sep 10.

Department of Plant Biology , University of Illinois, Urbana, Illinois 61801, USA.

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.
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http://dx.doi.org/10.1104/pp.110.163923DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2971586PMC
November 2010

A comparative study of salt tolerance parameters in 11 wild relatives of Arabidopsis thaliana.

J Exp Bot 2010 Aug 1;61(13):3787-98. Epub 2010 Jul 1.

Department of Agro-environmental Sciences and Technologies, University of Bologna, Viale Fanin 44, I-40127 Bologna, Italy.

Salinity is an abiotic stress that limits both yield and the expansion of agricultural crops to new areas. In the last 20 years our basic understanding of the mechanisms underlying plant tolerance and adaptation to saline environments has greatly improved owing to active development of advanced tools in molecular, genomics, and bioinformatics analyses. However, the full potential of investigative power has not been fully exploited, because the use of halophytes as model systems in plant salt tolerance research is largely neglected. The recent introduction of halophytic Arabidopsis-Relative Model Species (ARMS) has begun to compare and relate several unique genetic resources to the well-developed Arabidopsis model. In a search for candidates to begin to understand, through genetic analyses, the biological bases of salt tolerance, 11 wild relatives of Arabidopsis thaliana were compared: Barbarea verna, Capsella bursa-pastoris, Hirschfeldia incana, Lepidium densiflorum, Malcolmia triloba, Lepidium virginicum, Descurainia pinnata, Sisymbrium officinale, Thellungiella parvula, Thellungiella salsuginea (previously T. halophila), and Thlaspi arvense. Among these species, highly salt-tolerant (L. densiflorum and L. virginicum) and moderately salt-tolerant (M. triloba and H. incana) species were identified. Only T. parvula revealed a true halophytic habitus, comparable to the better studied Thellungiella salsuginea. Major differences in growth, water transport properties, and ion accumulation are observed and discussed to describe the distinctive traits and physiological responses that can now be studied genetically in salt stress research.
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http://dx.doi.org/10.1093/jxb/erq188DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2921208PMC
August 2010

Sulphate as a xylem-borne chemical signal precedes the expression of ABA biosynthetic genes in maize roots.

J Exp Bot 2010 Jul 21;61(12):3395-405. Epub 2010 Jun 21.

Donald Danforth Plant Science Center, 975 North Warson Rd, St Louis, MO 63132, USA.

Recent reports suggest that early sensing of soil water stress by plant roots and the concomitant reduction in stomatal conductance may not be mediated by root-sourced abscisic acid (ABA), but that other xylem-borne chemicals may be the primary stress signal(s). To gain more insight into the role of root-sourced ABA, the timing and location of the expression of genes for key enzymes involved in ABA biosynthesis in Zea mays roots was measured and a comprehensive analysis of root xylem sap constituents from the early to the later stages of water stress was conducted. Xylem sap and roots were sampled from plants at an early stage of water stress when only a reduction in leaf conductance was measured, as well as at later stages when leaf xylem pressure potential decreased. It was found that the majority of ABA biosynthetic genes examined were only significantly expressed in the elongation region of roots at a later stage of water stress. Apart from ABA, sulphate was the only xylem-borne chemical that consistently showed significantly higher concentrations from the early to the later stages of stress. Moreover, there was an interactive effect of ABA and sulphate in decreasing maize transpiration rate and Vicia faba stomatal aperture, as compared to ABA alone. The expression of a sulphate transporter gene was also analysed and it was found that it had increased in the elongation region of roots from the early to the later stages of water stress. Our results support the suggestion that in the early stage of water stress, increased levels of ABA in xylem sap may not be due to root biosynthesis, ABA glucose ester catabolism or pH-mediated redistribution, but may be due to shoot biosynthesis and translocation to the roots. The analysis of xylem sap mineral content and bioassays indicate that the anti-transpirant effect of the ABA reaching the stomata at the early stages of water stress may be enhanced by the increased concentrations of sulphate in the xylem which is also transported from the roots to the leaves.
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http://dx.doi.org/10.1093/jxb/erq160DOI Listing
July 2010

Functional characterization of the SIZ/PIAS-type SUMO E3 ligases, OsSIZ1 and OsSIZ2 in rice.

Plant Cell Environ 2010 Nov;33(11):1923-34

Division of Applied Life Science (BK21 program), Plant Molecular Biology and Biotechnology Research Center and Environmental Biotechnology National Core Research Center, Gyeongsang National University, Jinju 660-701, Korea.

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.
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http://dx.doi.org/10.1111/j.1365-3040.2010.02195.xDOI Listing
November 2010

Consequences of SOS1 deficiency: intracellular physiology and transcription.

Plant Signal Behav 2010 Jun 1;5(6):766-8. Epub 2010 Jun 1.

Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA.

As much as there is known about the function of the sodium/proton antiporter SOS1 in plants, recent studies point towards a more general role for this protein. The crucial involvement in salt stress protection is clearly one of its functions -confined to the N-terminus, but the modular structure of the protein includes a segment with several domains that are functionally not studied but comprise more than half of the protein's length. Additional functions of the protein appear to be an influence on vesicle trafficking, vacuolar pH and general ion homeostasis during salt stress. Eliminating SOS1 leads to the expression of genes that are not strictly salinity stress related. Functions that are regulated in sos1 mutants included pathogen responses, and effects on circadian rhythm.
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http://dx.doi.org/10.1093/jxb/erp391.DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3001585PMC
June 2010

Structural and functional studies of SIZ1, a PIAS-type SUMO E3 ligase from Arabidopsis.

Plant Signal Behav 2010 May 20;5(5):567-9. Epub 2010 Apr 20.

Division of Applied Life Science (BK21 program), PMBBRC, EB-NCRC, Gyeongsang National University, Jinju, Korea.

Small ubiquitin-like modifier (SUMO) is a post-translational modifier peptide that is involved in several biological processes in eukaryotes. Arabidopsis SIZ1, a SUMO E3 ligase, is an ortholog of the mammalian PIAS (Protein Inhibitor of Activated STAT) and yeast SIZ (SAP/Miz) proteins. SIZ1 contains all of the typical domains of PIAS/SIZ-type proteins, such as the PINIT, SAP, SP-RING, and plant-specific PHD domains. SIZ1 plays a pivotal role in controlling SUMOylation, and disruption of its function has been reported to affect stress responses, growth, and development. We performed a structural and functional analysis of SIZ1 by determining the phenotypes of siz1 knockout mutants transformed with SIZ1 alleles carrying point mutations in predicted SIZ1 domains. This study establishes that the diverse properties characteristic of SIZ1 are associated with specific domains and that they can be separated.
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http://dx.doi.org/10.4161/psb.11426DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7080486PMC
May 2010

Comparative transcriptomics for mangrove species: an expanding resource.

Funct Integr Genomics 2010 Nov 27;10(4):523-32. Epub 2010 Jan 27.

Department of Plant Biology, University of Illinois, 505 S Goodwin Ave, Urbana, IL 61801, USA.

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 .
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http://dx.doi.org/10.1007/s10142-009-0156-5DOI Listing
November 2010
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