AtGSTU19 and AtGSTU24 as Moderators of the Response of Arabidopsis thaliana to Turnip mosaic virus

Plants produce glutathione as a response to the intercellular redox state. Glutathione actively participates in the reactive oxygen species (ROS)-dependent signaling pathway, especially under biotic stress conditions. Most of the glutathione S-transferases (GSTs) are induced in cells during the defense response of plants not only through highly specific glutathione-binding abilities but also by participating in the signaling function. The tau class of GSTs has been reported to be induced as a response under stress conditions. Although several studies have focused on the role of the tau class of GSTs in plant–pathogen interactions, knowledge about their contribution to the response to virus inoculation is still inadequate. Therefore, in this study, the response of Atgstu19 and Atgstu24 knockout mutants to mechanical inoculation of Turnip mosaic virus (TuMV) was examined. The systemic infection of TuMV was more dynamically promoted in Atgstu19 mutants than in wild-type (Col-0) plants, suggesting the role of GSTU19 in TuMV resistance. However, Atgstu24 mutants displayed virus limitation and downregulation of the relative expression of TuMV capsid protein, accompanied rarely by TuMV particles only in vacuoles, and ultrastructural analyses of inoculated leaves revealed the lack of virus cytoplasmic inclusions. These findings indicated that Atgstu24 mutants displayed a resistance-like reaction to TuMV, suggesting that GSTU24 may suppress the plant resistance. In addition, these findings confirmed that GSTU1 and GSTU24 are induced and contribute to the susceptible reaction to TuMV in the Atgstu19–TuMV interaction. However, the upregulation of GSTU19 and GSTU13 highly correlated with virus limitation in the resistance-like reaction in the Atgstu24–TuMV interaction. Furthermore, the highly dynamic upregulation of GST and glutathione reductase (GR) activities resulted in significant induction (between 1 and 14 days post inoculation [dpi]) of the total glutathione pool (GSH + GSSG) in response to TuMV, which was accompanied by the distribution of active glutathione in plant cells. On the contrary, in Atgstu19, which is susceptible to TuMV interaction, upregulation of GST and GR activity only up to 7 dpi symptom development was reported, which resulted in the induction of the total glutathione pool between 1 and 3 dpi. These observations indicated that GSTU19 and GSTU24 are important factors in modulating the response to TuMV in Arabidopsis thaliana. Moreover, it was clear that glutathione is an important component of the regulatory network in resistance and susceptible response of A. thaliana to TuMV. These results help achieve a better understanding of the mechanisms regulating the Arabidopsis–TuMV pathosystem.

[1]  Jia Guo,et al.  Glutathione S-Transferase Interactions Enhance Wheat Resistance to Powdery Mildew but Not Wheat Stripe Rust. , 2022, Plant physiology.

[2]  D. Gilmer,et al.  Rhizomania: hide and seek of Polymyxa betae and the Beet necrotic yellow vein virus with Beta vulgaris. , 2022, Molecular plant-microbe interactions : MPMI.

[3]  E. Kozieł,et al.  Glutathione Modulation in PVYNTN Susceptible and Resistant Potato Plant Interactions , 2022, International journal of molecular sciences.

[4]  OUP accepted manuscript , 2022, FEMS Microbiology Reviews.

[5]  L. Puskás,et al.  Crosstalk between the redox signalling and the detoxification: GSTs under redox control? , 2021, Plant physiology and biochemistry : PPB.

[6]  E. Kozieł,et al.  Modulation of Expression of PVYNTN RNA-Dependent RNA Polymerase (NIb) and Heat Shock Cognate Host Protein HSC70 in Susceptible and Hypersensitive Potato Cultivars , 2021, Vaccines.

[7]  Eszter Balogh,et al.  Transcriptome profiling of pepper leaves by RNA-Seq during an incompatible and a compatible pepper-tobamovirus interaction , 2021, Scientific Reports.

[8]  Dongquan Guo,et al.  GmGSTU13 is related to the development of mosaic symptoms in soybean plants infected with Soybean mosaic virus. , 2021, Phytopathology.

[9]  Aiming Wang,et al.  Research Advances in Potyviruses: From the Laboratory Bench to the Field. , 2021, Annual review of phytopathology.

[10]  H. Garcia-Ruiz,et al.  Changes in Subcellular Localization of Host Proteins Induced by Plant Viruses , 2021, Viruses.

[11]  K. Dietz,et al.  Shifting paradigms and novel players in Cys-based redox regulation and ROS signaling in plants - and where to go next , 2020, Biological chemistry.

[12]  M. Torres,et al.  Respiratory Burst Oxidase Homologs RBOHD and RBOHF as Key Modulating Components of Response in Turnip Mosaic Virus—Arabidopsis thaliana (L.) Heyhn System , 2020, International journal of molecular sciences.

[13]  B. Zechmann Subcellular Roles of Glutathione in Mediating Plant Defense during Biotic Stress , 2020, Plants.

[14]  S. K. Grewal,et al.  Role of glutathione in methylglyoxal detoxification pathway during yellow mosaic virus (YMV) infection in black gram (Vigna mungo (L.) Hepper) , 2020 .

[15]  E. Horváth,et al.  Compensation of Mutation in Arabidopsis glutathione transferase (AtGSTU) Genes under Control or Salt Stress Conditions , 2020, International journal of molecular sciences.

[16]  E. Kozieł,et al.  Modifications in Tissue and Cell Ultrastructure as Elements of Immunity-Like Reaction in Chenopodium quinoa against Prune Dwarf Virus (PDV) , 2020, Cells.

[17]  B. Lockhart,et al.  The Expression of Potato Expansin A3 (StEXPA3) and Extensin4 (StEXT4) Genes with Distribution of StEXPAs and HRGPs-Extensin Changes as an Effect of Cell Wall Rebuilding in Two Types of PVYNTN–Solanum tuberosum Interactions , 2020, Viruses.

[18]  K. Ohshima,et al.  Phylogenetic relationships and genetic structure of populations of turnip mosaic virus in Turkey , 2019, European Journal of Plant Pathology.

[19]  A. Enyedi,et al.  Glutathione Can Compensate for Salicylic Acid Deficiency in Tobacco to Maintain Resistance to Tobacco Mosaic Virus , 2019, Front. Plant Sci..

[20]  Ajit Ghosh,et al.  Genome-wide identification of glutathione S-transferase gene family in pepper, its classification, and expression profiling under different anatomical and environmental conditions , 2019, Scientific Reports.

[21]  Simon R. Law,et al.  Functional, Structural and Biochemical Features of Plant Serinyl-Glutathione Transferases , 2019, Front. Plant Sci..

[22]  V. Pande,et al.  Rice (Oryza sativa L.) tau class glutathione S-transferase (OsGSTU30) overexpression in Arabidopsis thaliana modulates a regulatory network leading to heavy metal and drought stress tolerance. , 2019, Metallomics : integrated biometal science.

[23]  E. Horváth,et al.  Plant Glutathione Transferases and Light , 2019, Front. Plant Sci..

[24]  P. Schröder,et al.  Glutathione S-Transferase Enzymes in Plant-Pathogen Interactions , 2018, Front. Plant Sci..

[25]  E. Kozieł,et al.  Ultrastructural Analysis of Prune Dwarf Virus Intercellular Transport and Pathogenesis , 2018, International journal of molecular sciences.

[26]  C. Harmon,et al.  Comparison of genus-specific primers in RT-PCR for the broad-spectrum detection of viruses in the genus Potyvirus by plant diagnostic laboratories. , 2018, Journal of virological methods.

[27]  L. Szabados,et al.  Comprehensive analysis of antioxidant mechanisms in Arabidopsis glutathione peroxidase-like mutants under salt- and osmotic stress reveals organ-specific significance of the AtGPXL’s activities , 2018, Environmental and Experimental Botany.

[28]  B. Lockhart,et al.  Plant Cell Wall Dynamics in Compatible and Incompatible Potato Response to Infection Caused by Potato Virus Y (PVYNTN) , 2018, International journal of molecular sciences.

[29]  Zihao Xia,et al.  Transcriptome analysis of watermelon (Citrullus lanatus) fruits in response to Cucumber green mottle mosaic virus (CGMMV) infection , 2017, Scientific Reports.

[30]  L. Király,et al.  The Signaling Roles of Glutathione in Plant Disease Resistance , 2017 .

[31]  P. Schulze-Lefert,et al.  Glutathione Transferase U13 Functions in Pathogen-Triggered Glucosinolate Metabolism1 , 2017, Plant Physiology.

[32]  I. Rahman,et al.  Genome-wide identification and expression analysis of glutathione S-transferase gene family in tomato: Gaining an insight to their physiological and stress-specific roles , 2017, PloS one.

[33]  A. Paradiso,et al.  Chemistry, Biosynthesis, and Antioxidative Function of Glutathione in Plants , 2017 .

[34]  A. Papageorgiou,et al.  Characterization and functional analysis of a recombinant tau class glutathione transferase GmGSTU2-2 from Glycine max. , 2017, International journal of biological macromolecules.

[35]  S. Kanakala,et al.  Transcriptomic and proteomic analysis of yellow mosaic diseased soybean , 2016, Journal of Plant Biochemistry and Biotechnology.

[36]  Feng Sun,et al.  RNA-seq-based digital gene expression analysis reveals modification of host defense responses by rice stripe virus during disease symptom development in Arabidopsis , 2016, Virology Journal.

[37]  M. Reichelt,et al.  A Chinese cabbage (Brassica campetris subsp. Chinensis) τ-type glutathione-S-transferase stimulates Arabidopsis development and primes against abiotic and biotic stress , 2016, Plant Molecular Biology.

[38]  P. Trost,et al.  Protein S-nitrosylation in photosynthetic organisms: A comprehensive overview with future perspectives. , 2016, Biochimica et biophysica acta.

[39]  B. Zechmann,et al.  Compartment-specific investigations of antioxidants and hydrogen peroxide in leaves of Arabidopsis thaliana during dark-induced senescence , 2016, Acta Physiologiae Plantarum.

[40]  C. Foyer,et al.  Stress-triggered redox signalling: what's in pROSpect? , 2016, Plant, cell & environment.

[41]  P. Díaz‐Vivancos,et al.  Oxidative stress and antioxidative responses in plant-virus interactions , 2016 .

[42]  B. Jha,et al.  Functional Characterization of the Tau Class Glutathione-S-Transferases Gene (SbGSTU) Promoter of Salicornia brachiata under Salinity and Osmotic Stress , 2016, PloS one.

[43]  R. Peng,et al.  Over-expression of AtGSTU19 provides tolerance to salt, drought and methyl viologen stresses in Arabidopsis. , 2016, Physiologia plantarum.

[44]  A. Paradiso,et al.  Cellular Redox Homeostasis as Central Modulator in Plant Stress Response , 2016 .

[45]  Guiyan Yang,et al.  In planta characterization of a tau class glutathione S-transferase gene from Juglans regia (JrGSTTau1) involved in chilling tolerance , 2015, Plant Cell Reports.

[46]  A. Tsaftaris,et al.  Tobacco plants over-expressing the sweet orange tau glutathione transferases (CsGSTUs) acquire tolerance to the diphenyl ether herbicide fluorodifen and to salt and drought stresses. , 2015, Phytochemistry.

[47]  J. Carrington,et al.  Roles and Programming of Arabidopsis ARGONAUTE Proteins during Turnip Mosaic Virus Infection , 2015, PLoS pathogens.

[48]  A. Papageorgiou,et al.  Catalytic features and crystal structure of a tau class glutathione transferase from Glycine max specifically upregulated in response to soybean mosaic virus infections. , 2015, Biochimica et biophysica acta.

[49]  C. Foyer,et al.  Low glutathione regulates gene expression and the redox potentials of the nucleus and cytosol in Arabidopsis thaliana. , 2015, Plant, cell & environment.

[50]  T. Rausch,et al.  Imposed glutathione-mediated redox switch modulates the tobacco wound-induced protein kinase and salicylic acid-induced protein kinase activation state and impacts on defence against Pseudomonas syringae , 2015, Journal of experimental botany.

[51]  P. Díaz‐Vivancos,et al.  Sharka: how do plants respond to Plum pox virus infection? , 2015, Journal of experimental botany.

[52]  E. Horváth,et al.  Glutathione transferase supergene family in tomato: Salt stress-regulated expression of representative genes from distinct GST classes in plants primed with salicylic acid. , 2014, Plant physiology and biochemistry : PPB.

[53]  J. Potts,et al.  Arabidopsis Glutathione Transferases U24 and U25 Exhibit a Range of Detoxification Activities with the Environmental Pollutant and Explosive, 2,4,6-Trinitrotoluene1[C][W][OPEN] , 2014, Plant Physiology.

[54]  Z. Han,et al.  Comparative proteomic analysis of the plant-virus interaction in resistant and susceptible ecotypes of maize infected with sugarcane mosaic virus. , 2013, Journal of proteomics.

[55]  B. Koffler,et al.  High Resolution Imaging of Temporal and Spatial Changes of Subcellular Ascorbate, Glutathione and H2O2 Distribution during Botrytis cinerea Infection in Arabidopsis , 2013, PloS one.

[56]  G. Arrigoni,et al.  Biochemical and quantitative proteomics investigations in Arabidopsis ggt1 mutant leaves reveal a role for the gamma‐glutamyl cycle in plant's adaptation to environment , 2013, Proteomics.

[57]  Y. Hsu,et al.  The glutathione transferase of Nicotiana benthamiana NbGSTU4 plays a role in regulating the early replication of Bamboo mosaic virus , 2013, The New phytologist.

[58]  G. Queval,et al.  Functional analysis of Arabidopsis mutants points to novel roles for glutathione in coupling H(2)O(2) to activation of salicylic acid accumulation and signaling. , 2013, Antioxidants & redox signaling.

[59]  Yong-guan Zhu,et al.  Arsenite Elicits Anomalous Sulfur Starvation Responses in Barley1[W] , 2013, Plant Physiology.

[60]  N. Fernández-García,et al.  Chloroplast protection in plum pox virus-infected peach plants by L-2-oxo-4-thiazolidine-carboxylic acid treatments: effect in the proteome. , 2013, Plant, cell & environment.

[61]  S. Kikuchi,et al.  Gene expression responses to Rice tungro spherical virus in susceptible and resistant near-isogenic rice plants. , 2013, Virus research.

[62]  Q. Zeng,et al.  Functional Divergence of the Glutathione S-Transferase Supergene Family in Physcomitrella patens Reveals Complex Patterns of Large Gene Family Evolution in Land Plants1[W][OA] , 2012, Plant Physiology.

[63]  C. Petri,et al.  Modulation of tobacco bacterial disease resistance using cytosolic ascorbate peroxidase and Cu,Zn‐superoxide dismutase , 2012 .

[64]  Maria Müller,et al.  Sulfate supply influences compartment specific glutathione metabolism and confers enhanced resistance to Tobacco mosaic virus during a hypersensitive response , 2012, Plant physiology and biochemistry : PPB.

[65]  M. Barón,et al.  Analysis of the antioxidant response of Nicotiana benthamiana to infection with two strains of Pepper mild mottle virus , 2012, Journal of experimental botany.

[66]  K. Ogawa,et al.  Overexpression of GSH1 gene mimics transcriptional response to low temperature during seed vernalization treatment of Arabidopsis. , 2012, Plant & cell physiology.

[67]  R. Edwards,et al.  The Arabidopsis phi class glutathione transferase AtGSTF2: binding and regulation by biologically active heterocyclic ligands. , 2011, The Biochemical journal.

[68]  R. MacDiarmid,et al.  Identification and validation of reference genes for normalization of transcripts from virus-infected Arabidopsis thaliana. , 2011, Molecular plant-microbe interactions : MPMI.

[69]  F. Pallardó,et al.  A nuclear glutathione cycle within the cell cycle. , 2010, The Biochemical journal.

[70]  R. Edwards,et al.  Roles for glutathione transferases in plant secondary metabolism. , 2010, Phytochemistry.

[71]  E. Paplomatas,et al.  Ethylene perception via ETR1 is required in Arabidopsis infection by Verticillium dahliae. , 2010, Molecular plant pathology.

[72]  Ligia Toro,et al.  Quantitative determination of spatial protein-protein correlations in fluorescence confocal microscopy. , 2010, Biophysical journal.

[73]  Robert Edwards,et al.  Glutathione Transferases , 2010, The arabidopsis book.

[74]  D. Kolb,et al.  Cadmium induced changes in subcellular glutathione contents within glandular trichomes of Cucurbita pepo L. , 2009, Protoplasma.

[75]  Robert Edwards,et al.  Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily , 2009, Journal of experimental botany.

[76]  Maria Müller,et al.  Effects of zucchini yellow mosaic virus infection on the subcellular distribution of glutathione and its precursors in a highly tolerant Cucurbita pepo cultivar , 2008 .

[77]  T. Chu,et al.  Global Analysis of Arabidopsis Gene Expression Uncovers a Complex Array of Changes Impacting Pathogen Response and Cell Cycle during Geminivirus Infection1[W][OA] , 2008, Plant Physiology.

[78]  E. Olmos,et al.  Alteration in the chloroplastic metabolism leads to ROS accumulation in pea plants in response to plum pox virus , 2008, Journal of experimental botany.

[79]  Martin J. Mueller,et al.  General Detoxification and Stress Responses Are Mediated by Oxidized Lipids through TGA Transcription Factors in Arabidopsis[W] , 2008, The Plant Cell Online.

[80]  A. Nuñez,et al.  Proteome changes in sugar beet in response to Beet necrotic yellow vein virus , 2008 .

[81]  K. Ohshima,et al.  Turnip mosaic virus. , 2008 .

[82]  M. Sánchez-Pina,et al.  Oxidative stress induction by Prunus necrotic ringspot virus infection in apricot seeds. , 2007, Physiologia plantarum.

[83]  G. Zellnig,et al.  Virus-induced changes in the subcellular distribution of glutathione precursors in Cucurbita pepo (L.). , 2007, Plant biology.

[84]  Rebecca L Poole The TAIR database. , 2007, Methods in molecular biology.

[85]  G. Zellnig,et al.  Artificial elevation of glutathione affects symptom development in ZYMV-infected Cucurbita pepo L. plants , 2006, Archives of Virology.

[86]  Stephen Chivasa,et al.  Identification of Arabidopsis salt and osmotic stress responsive proteins using two‐dimensional difference gel electrophoresis and mass spectrometry , 2005, Proteomics.

[87]  G. Loake,et al.  Cauliflower mosaic virus, a Compatible Pathogen of Arabidopsis, Engages Three Distinct Defense-Signaling Pathways and Activates Rapid Systemic Generation of Reactive Oxygen Species1 , 2005, Plant Physiology.

[88]  Martin J. Mueller,et al.  Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. , 2005, Molecular plant-microbe interactions : MPMI.

[89]  C. Foyer,et al.  Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context , 2005 .

[90]  T. Hsiang,et al.  Induction of glutathione S-transferase genes of Nicotiana benthamiana following infection by Colletotrichum destructivum and C. orbiculare and involvement of one in resistance. , 2005, Journal of experimental botany.

[91]  J. Schnoor,et al.  Gene Expression and Microscopic Analysis of Arabidopsis Exposed to Chloroacetanilide Herbicides and Explosive Compounds. A Phytoremediation Approach1 , 2005, Plant Physiology.

[92]  M. Skłodowska,et al.  Compartment-specific role of the ascorbate-glutathione cycle in the response of tomato leaf cells to Botrytis cinerea infection. , 2005, Journal of experimental botany.

[93]  M. Skłodowska,et al.  Differential Implication of Glutathione, Glutathione-Metabolizing Enzymes and Ascorbate in Tomato Resistance to Pseudomonas syringae , 2004 .

[94]  Ulrich Wagner,et al.  Probing the Diversity of the Arabidopsis glutathione S-Transferase Gene Family , 2002, Plant Molecular Biology.

[95]  A. Millar,et al.  Proteomic Analysis of Glutathione S-Transferases of Arabidopsis thaliana Reveals Differential Salicylic Acid-Induced Expression of the Plant-Specific Phi and Tau Classes , 2004, Plant Molecular Biology.

[96]  D. Burritt,et al.  The influence of Cocksfoot mottle virus on antioxidant metabolism in the leaves of Dactylis glomerata L. , 2003 .

[97]  J. A. Navas‐Cortés,et al.  Induction of an antioxidant enzyme system and other oxidative stress markers associated with compatible and incompatible interactions between chickpea (Cicer arietinum L.) and Fusarium oxysporum f. sp.ciceris , 2002 .

[98]  C. Jenner,et al.  Turnip mosaic virus and the quest for durable resistance. , 2002, Molecular plant pathology.

[99]  D. Burritt,et al.  Changes in the activities of antioxidant enzymes in response to virus infection and hormone treatment. , 2002, Physiologia plantarum.

[100]  Z. Kiraly,et al.  Down-regulation of Antioxidative Capacity in a Transgenic Tobacco which Fails to Develop Acquired Resistance to Necrotization Caused by TMV , 2002, Free radical research.

[101]  E. Kuzniak,et al.  Ascorbate, glutathione and related enzymes in chloroplasts of tomato leaves infected by Botrytis cinerea. , 2001, Plant science : an international journal of experimental plant biology.

[102]  C. Foyer,et al.  Early H(2)O(2) accumulation in mesophyll cells leads to induction of glutathione during the hyper-sensitive response in the barley-powdery mildew interaction. , 2000, Plant physiology.

[103]  G. Gullner,et al.  Elevation of glutathione level and activation of glutathione-related enzymes affect virus infection in tobacco. , 1999, Free radical research.

[104]  Walsh,et al.  Serotypic variation in turnip mosaic virus , 1999 .

[105]  I. Kranner Determination of Glutathione, Glutathione Disulphide and Two Related Enzymes, Glutathione Reductase and Glucose-6-Phosphate Dehydrogenase, in Fungal and Plant Cells , 1998 .

[106]  Z. Kiraly,et al.  Local and Systemic Responses of Antioxidants to Tobacco Mosaic Virus Infection and to Salicylic Acid in Tobacco (Role in Systemic Acquired Resistance) , 1997, Plant physiology.

[107]  R. Gáborjányi,et al.  Notes: Differential Alterations of Glutathione S-Transferase Enzyme Activities in Three Sorghum Varieties Following Viral Infection , 1995 .

[108]  G J Brakenhoff,et al.  Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. , 1992, Journal of cell science.