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      Sulfate supply influences compartment specific glutathione metabolism and confers enhanced resistance to Tobacco mosaic virus during a hypersensitive response

      a , 1 , a , 1 , b , b , a , b , a , b ,

      Plant Physiology and Biochemistry

      Elsevier Science

      Cysteine, Glutathione, Nicotiana tabacum, Salicylic acid, Sulfur induced resistance, Tobacco mosaic virus, APR, adenosine 5′-phosphosulfate reductase, BSA, bovine serum albumin, CATSAB, salicylic acid-binding catalase, CP, coat protein, dpi, days post inoculation, GSH1, γ-glutamyl cysteine synthetase, GSH2, glutathione synthetase, GSTTau1, Tau class glutathione S-transferase, HR, hypersensitive response, PBS, phosphate buffered saline, PCD, programmed cell death, ROS, reactive oxygen species, S, sulfate, SIR, sulfur induced resistance, SED, sulfur enhanced defense, TMV, Tobacco mosaic virus

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          Abstract

          Sufficient sulfate supply has been linked to the development of sulfur induced resistance or sulfur enhanced defense (SIR/SED) in plants. In this study we investigated the effects of sulfate (S) supply on the response of genetically resistant tobacco ( Nicotiana tabacum cv. Samsun NN) to Tobacco mosaic virus (TMV). Plants grown with sufficient sulfate (+S plants) developed significantly less necrotic lesions during a hypersensitive response (HR) when compared to plants grown without sulfate (−S plants). In +S plants reduced TMV accumulation was evident on the level of viral RNA. Enhanced virus resistance correlated with elevated levels of cysteine and glutathione and early induction of a Tau class glutathione S-transferase and a salicylic acid-binding catalase gene. These data indicate that the elevated antioxidant capacity of +S plants was able to reduce the effects of HR, leading to enhanced virus resistance. Expression of pathogenesis-related genes was also markedly up-regulated in +S plants after TMV-inoculation. On the subcellular level, comparison of TMV-inoculated +S and −S plants revealed that +S plants contained 55–132 % higher glutathione levels in mitochondria, chloroplasts, nuclei, peroxisomes and the cytosol than −S plants. Interestingly, mitochondria were the only organelles where TMV-inoculation resulted in a decrease of glutathione levels when compared to mock-inoculated plants. This was particularly obvious in −S plants, where the development of necrotic lesions was more pronounced. In summary, the overall higher antioxidative capacity and elevated activation of defense genes in +S plants indicate that sufficient sulfate supply enhances a preexisting plant defense reaction resulting in reduced symptom development and virus accumulation.

          Highlights

          ► Sulfate as possible enhancer of plant defense during virus infection. ► Sulfate fertilization reduces symptom severity and virus contents. ► Enhanced cysteine and glutathione metabolism up-regulates defense gene expression. ► Sulfate fertilization enhances plant defense during virus infection.

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          Most cited references 73

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          Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes.

          Sulfur is required for growth of all organisms and is present in a wide variety of metabolites having distinctive biological functions. Sulfur is cycled in ecosystems in nature where conversion of sulfate to organic sulfur compounds is primarily dependent on sulfate uptake and reduction pathways in photosynthetic organisms and microorganisms. In vascular plant species, transport proteins and enzymes in this pathway are functionally diversified to have distinct biochemical properties in specific cellular and subcellular compartments. Recent findings indicate regulatory processes of sulfate transport and metabolism are tightly connected through several modes of transcriptional and posttranscriptional mechanisms. This review provides up-to-date knowledge in functions and regulations of sulfur assimilation in plants and algae, focusing on sulfate transport systems and metabolic pathways for sulfate reduction and synthesis of downstream metabolites with diverse biological functions.
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            Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health.

            Glutathione S-transferases (GSTs) are abundant proteins encoded by a highly divergent, ancient gene family. Soluble GSTs form dimers, each subunit of which contains active sites that bind glutathione and hydrophobic ligands. Plant GSTs attach glutathione to electrophilic xenobiotics, which tags them for vacuolar sequestration. The role of GSTs in metabolism is unclear, although their complex regulation by environmental stimuli implies that they have important protective functions. Recent studies show that GSTs catalyse glutathione-depend-ent isomerizations and the reduction of toxic organic hydroperoxides. GSTs might also have non-catalytic roles as carriers for phytochemicals.
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              Production of reactive oxygen species, alteration of cytosolic ascorbate peroxidase, and impairment of mitochondrial metabolism are early events in heat shock-induced programmed cell death in tobacco Bright-Yellow 2 cells.

              To gain some insight into the mechanisms by which plant cells die as a result of abiotic stress, we exposed tobacco (Nicotiana tabacum) Bright-Yellow 2 cells to heat shock and investigated cell survival as a function of time after heat shock induction. Heat treatment at 55 degrees C triggered processes leading to programmed cell death (PCD) that was complete after 72 h. In the early phase, cells undergoing PCD showed an immediate burst in hydrogen peroxide (H2O2) and superoxide (O2*-) anion production. Consistently, death was prevented by the antioxidants ascorbate (ASC) and superoxide dismutase (SOD). Actinomycin D and cycloheximide, inhibitors of transcription and translation, respectively, also prevented cell death, but with a lower efficiency. Induction of PCD resulted in gradual oxidation of endogenous ASC; this was accompanied by a decrease in both the amount and the specific activity of the cytosolic ASC peroxidase (cAPX). A reduction in cAPX gene expression was also found in the late PCD phase. Moreover, changes of cAPX kinetic properties were found in PCD cells. Production of ROS in PCD cells was accompanied by early inhibition of glucose (Glc) oxidation, with a strong impairment of mitochondrial function as shown by an increase in cellular NAD(P)H fluorescence, and by failure of mitochondria isolated from cells undergoing PCD to generate membrane potential and to oxidize succinate in a manner controlled by ADP. Thus, we propose that in the early phase of tobacco Bright-Yellow 2 cell PCD, ROS production occurs, perhaps because of damage of the cell antioxidant system, with impairment of the mitochondrial oxidative phosphorylation.
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                Author and article information

                Journal
                Plant Physiol Biochem
                Plant Physiol. Biochem
                Plant Physiology and Biochemistry
                Elsevier Science
                0981-9428
                1873-2690
                October 2012
                October 2012
                : 59
                : C
                : 44-54
                Affiliations
                [a ]Plant Protection Institute, Hungarian Academy of Sciences, P.O. Box 102, 1525 Budapest, Hungary
                [b ]University of Graz, Institute of Plant Sciences, Schubertstrasse 51, 8010 Graz, Austria
                Author notes
                []Corresponding author. Tel.: +43 316 380 5635; fax: +43 316 380 9880. bernd.zechmann@ 123456uni-graz.at
                [1]

                Lóránt Király and András Künstler contributed equally to this work and are considered co-first authors.

                Article
                PLAPHY3255
                10.1016/j.plaphy.2011.10.020
                3458214
                22122784
                © 2012 Elsevier Masson SAS.

                This document may be redistributed and reused, subject to certain conditions.

                Categories
                Research Article

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