Abstract
The role of glutathione (GSH) in plant defense has long been known in addition to its substantial role in stress tolerance and antioxidant signalling. In this study, molecular analysis of GSH fed Arabidopsis thaliana, exhibiting enhanced GSH content and stress tolerance potential, was performed to explore the intricate position of GSH in the plant defense signaling network. Microarray data revealed the differential regulation of 653 transcripts of which 379 were upregulated and 274 were downregulated by 2-fold or more (p < 0.05). Gene enrichment and KEGG database analysis identified glucosinolate (GLS), a plant defense compound, and tryptophan biosynthetic pathways as specifically enriched by GSH. Interestingly, upregulation of genes related to biosynthesis was also observed under enhanced GSH condition. Functional annotation noted upregulation of biotic stress related and ethylene (ET)-related genes like 1-aminocyclopropane carboxylate synthase 2 at transcript level. These data were supported by the up-accumulation of ACC oxidase at proteomics level signifying the interplay between GSH and ET in defense signaling pathway. Differential expression of salicylic acid (SA)-mediated signaling genes direct the involvement of GSH with SA. Our proteomic analysis also identified the upregulation of stress and defense related proteins. The effect of GSH on GLS biosynthetic pathways as observed here might be an important information linking GSH to GLS mediated defense. Together, this investigation reveals the association of GSH with tryptophan, lignin and GLS in addition to SA and ET, in plant defense.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- ABA:
-
Abscisic acid
- ACC 1:
-
Aminocyclopropane carboxylic acid
- ADC2 :
-
Arginine decarboxylase 2
- AIG1 :
-
AVRRPT2-induced gene 1
- APX1 :
-
Ascorbate peroxidase 1
- ASA1 :
-
Anthranilate synthase alpha subunit 1
- CYP79B2:
-
Cytochrome P450 79B2
- DAVID:
-
Database for Annotation, Visualization and Integrated Discovery
- ERD5:
-
Proline dehydrogenase
- ET:
-
Ethylene
- GLS:
-
Glucosinolate
- GPX:
-
Glutathione peroxidase
- Grxs:
-
Glutaredoxins
- GSH:
-
Glutathione
- GSSG:
-
Oxidised glutathione
- GST:
-
Glutathione-S-transferase
- GSTU3:
-
Glutathione-S-transferase TAU 3
- HPLC:
-
High performance liquid chromatography
- HSP:
-
Heat shock protein
- JA:
-
Jasmonate
- KEGG:
-
Kyoto Encyclopedia of Genes and Genomes
- MAPKKK19:
-
Mitogen-activated protein kinase kinase kinase 19
- MDHAR :
-
Monodehydroascorbate reductase
- NPR1:
-
Norexpressor of pathogenesis related genes
- ROS:
-
Reactive oxygen species
- SA:
-
Salicylic acid
- SEA:
-
Singular enrichment analysis
- TEM1:
-
Tempranillo 1
- Trxs:
-
Thioredoxins
References
Agrawal SB, Agrawal M, Lee EH, Kramer GF, Pillai P (1992) Changes in polyamine and glutathione contents of a green alga, Chlorogonium elongatum (Dang) France exposed to mercury. Environ Exp Bot 32:145–151. doi:10.1016/0098-8472(92)90039-5
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. doi:10.1146/annurev.arplant.55.031903.141701
Ball L, Accotto G-P, Bechtold U, Creissen G, Funck D, Jimenez A, Kular B, Leyland N, Mejia-Carranza J, Reynolds H, Karpinski S, Mullineaux PM (2004) Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell 16:2448–2462. doi:10.1105/tpc.104.022608
Binder BM, O’malley RC, Wang W, Moore JM, Parks BM, Spalding EP, Bleecker AB (2004) Arabidopsis seedling growth response and recovery to ethylene. A kinetic analysis. Plant Physiol 136:2913–2920. doi:10.1104/pp.104.050369
Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12:2383–2393. doi:10.1105/tpc.12.12.2383
Bossio E, Diaz Paleo A, del Vas M, Baroli I, Acevedo A, Rios RD (2013) Silencing of glutathione biosynthetic pathway inhibits somatic embryogenesis in wheat. Plant Cell Tissue Org 112:239–248. doi:10.1007/s11240-012-0228-4
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3
Burow M, Zhang Z-Y, Ober JA, Lambrix VM, Wittstock U, Gershenzon J, Kliebenstein DJ (2008) ESP and ESM1 mediate indol-3-acetonitrile production from indol-3-ylmethyl glucosinolate in Arabidopsis. Phytochemistry 69:663–671. doi:10.1016/j.phytochem.2007.08.027
Bushey DF, Law DM, Davies PJ (1987) High-performance liquid chromatography analysis of 1-aminocyclopropane-1-carboxylic acid using o-phthaldialdehyde precolumn derivatization. Anal Biochem 167:31–36. doi:10.1016/0003-2697(87)90130-8
Datta R, Sinha R, Chattopadhyay S (2013) Changes in leaf proteome profile of Arabidopsis thaliana in response to salicylic acid. J Biosci 38:317–328. doi:10.1007/s12038-013-9308-9
De Grauwe L, Dugardeyn J, Van Der Straeten D (2008) Novel mechanisms of ethylene-gibberellin crosstalk revealed by the gai eto2-1 double mutant. Plant Signal Behav 3:1113–1115. doi:10.4161/psb.3.12.7037
De Vos M, Denekamp M, Dicke M, Vuylsteke M, Van Loon L, Smeekens SC, Pieterse CMJ (2006) The Arabidopsis thaliana transcription factor AtMYB102 functions in defense against the insect herbivore Pieris rapae. Plant Signal Behav 1:305–311. doi:10.4161/psb.1.6.3512
Dence CW (1992) Lignin determination. In: Lin SY, Dence CW (eds) Methods in lignin chemistry: springer series in wood science. Springer-Verlag, Berlin, pp 33–61
Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143:1789–1801. doi:10.1104/pp.106.093971
Dong X, Mindrinos M, Davis KR, Ausubel FM (1991) Induction of Arabídopsís defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell 3:61–72. doi:10.1105/tpc.3.1.61
Dron M, Clouse SD, Dixon RA, Lawton MA, Lamb CJ (1988) Glutathione and fungal elicitor regulation of a plant defense gene promoter in electroporated protoplasts. Proc Natl Acad Sci USA 85:6738–6742. doi:10.1073/pnas.85.18.6738
Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70. doi:10.1093/nar/gkq310
Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581. doi:10.1016/j.tplants.2010.06.005
Dubreuil-Maurizi C, Poinssot B (2012) Role of glutathione in plant signaling under biotic stress. Plant Signal Behav 7:210–212. doi:10.4161/psb.18831
Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875. doi:10.1105/tpc.105.033589
Frendo P, Baldacci-Cresp F, Benyamina SM, Puppo A (2013) Glutathione and plant response to the biotic environment. Free Radic Biol Med 65:724–730. doi:10.1016/j.freeradbiomed.2013.07.035
Ghanta S, Bhattacharyya D, Chattopadhyay S (2011a) Glutathione signaling acts through NPR1-dependent SA-mediated pathway to mitigate biotic stress. Plant Signal Behav 6:607–609. doi:10.4161/psb.6.4.15402
Ghanta S, Bhattacharyya D, Sinha R, Banerjee A, Chattopadhyay S (2011b) Nicotiana tabacum overexpressing γ-ECS exhibits biotic stress tolerance likely through NPR1-dependent salicylic acid-mediated pathway. Planta 233:895–910. doi:10.1007/s00425-011-1349-4
Ghanta S, Datta R, Bhattacharyya D, Sinha R, Kumar D, Hazra S, Mazumder AB, Chattopadhyay S (2014) Multistep involvement of glutathione with salicylic acid and ethylene to combat environmental stress. J Plant Physiol. doi:10.1016/j.jplph.2014.03.002
Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis—2001 status. Curr Opin Plant Biol 4:301–308. doi:10.1016/S1369-5266(00)00177-1
Gomez LD, Noctor G, Knight MR, Foyer CH (2004) Regulation of calcium signalling and gene expression by glutathione. J Exp Bot 55:1851–1859. doi:10.1093/jxb/erh202
Grene R (2002) Oxidative stress and acclimation mechanisms in plants. Arab Book Am Soc Plant Biol. doi:10.1199/tab.0036.1
Grubb CD, Abel S (2006) Glucosinolate metabolism and its control. Trends Plant Sci 11:89–100. doi:10.1016/j.tplants.2005.12.006
Hahn A, Harter K (2009) Mitogen-activated protein kinase cascades and ethylene: signaling, biosynthesis, or both? Plant Physiol 149:1207–1210. doi:10.1104/pp.108.132241
Han Y, Chaouch S, Mhamdi A, Queval G, Zechmann B, Noctor G (2013a) Functional analysis of Arabidopsis mutants points to novel roles for glutathione in coupling H2O2 to activation of salicylic acid accumulation and signaling. Antioxid Redox Signal 18:2106–2121. doi:10.1089/ars.2012.5052
Han Y, Mhamdi A, Chaouch S, Noctor G (2013b) Regulation of basal and oxidative stress-triggered jasmonic acid-related gene expression by glutathione. Plant, Cell Environ 36:1135–1146. doi:10.1111/pce.12048
Hirai MY, Sugiyama K, Sawada Y, Tohge T, Obayashi T, Suzuki A, Araki R, Sakurai N, Suzuki H, Aoki K, Goda H, Nishizawa OI, Shibata D, Saito K (2007) Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc Natl Acad Sci USA 104:6478–6483. doi:10.1073/pnas.0611629104
Hiruma K, Fukunaga S, Bednarek P, Pislewska-Bednarek M, Watanabe S, Narusaka Y, Shirasu K, Takano Y (2013) Glutathione and tryptophan metabolism are required for Arabidopsis immunity during the hypersensitive response to hemibiotrophs. Proc Natl Acad Sci USA 110:9589–9594. doi:10.1073/pnas.1305745110
Huang Z, Zhao L, Chen D, Liang M, Liu Z, Shao H, Long X (2013) Salt stress encourages proline accumulation by regulating proline biosynthesis and degradation in Jerusalem Artichoke plantlets. PLoS One 8:e62085. doi:10.1371/journal.pone.0062085
Huffaker A, Pearce G, Ryan CA (2006) An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc Natl Acad Sci USA 103:10098–10103. doi:10.1073/pnas.0603727103
Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31:e15. doi:10.1093/nar/gng015
Isaacson T, Damasceno CMB, Saravanan RS, He Y, Catalá C, Saladié M, Rose JKC (2006) Sample extraction techniques for enhanced proteomic analysis of plant tissues. Nat Protoc 1:769–774. doi:10.1038/nprot.2006.102
Jiang Y, Yang B, Harris NS, Deyholos MK (2007) Comparative proteomic analysis of NaCl stress responsive proteins in Arabidopsis roots. J Exp Bot 58:3591–3607. doi:10.1093/jxb/erm207
Kreps JA, Wu Y, Chang H-S, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141. doi:10.1104/pp.008532
Lappartient AG, Touraine B (1997) Glutathione-mediated regulation of ATP sulfurylase activity, SO4 2− uptake, and oxidative stress response in intact canola roots. Plant Physiol 114:177–183. doi:10.1104/pp.114.1.177
Leon-Reyes A, Spoel SH, Lange ESD, Abe H, Kobayashi M, Tsuda S, Millenaar FF, Welschen RAM, Ritsema T, Pieterse CMJ (2009) Ethylene modulates the role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 in cross talk between salicylate and jasmonate signaling. Plant Physiol 149:1797–1809. doi:10.1104/pp.108.133926
Leon-Reyes A, Du Y, Koornneef A, Proietti S, Körbes AP, Memelink J, Pieterse CMJ, Ritsema T (2010) Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid. Mol Plant Microbe Interact 23:187–197. doi:10.1094/MPMI-23-2-0187
Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593. doi:10.1016/0092-8674(94)90544-4
Lim B, Pasternak M, Meyer AJ, Cobbett CS (2013) Restricting glutamylcysteine synthetase activity to the cytosol or glutathione biosynthesis to the plastid is sufficient for normal plant development and stress tolerance. Plant Biol (Stuttg). doi:10.1111/plb.12033
Lin RC, Park HJ, Wang HY (2008) Role of Arabidopsis RAP2.4 in regulating light- and ethylene-mediated developmental processes and drought stress tolerance. Mol Plant 1:42–57. doi:10.1093/mp/ssm004
Mandaokar A, Browse J (2009) MYB108 acts together with MYB24 to regulate jasmonate-mediated stamen maturation in Arabidopsis. Plant Physiol 149:851–862. doi:10.1104/pp.108.132597
May MJ, Vernoux T, Leaver C, Montagu MV, Inzé D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49:649–667. doi:10.1093/jxb/49.321.649
Meister A (1988) Glutathione metabolism and its selective modification. J Biol Chem 263:17205–17208
Mhamdi A, Hager J, Chaouch S, Queval G, Han Y, Taconnat L, Saindrenan P, Gouia H, Issakidis-Bourguet E, Renou JP, Noctor G (2010) Arabidopsis GLUTATHIONE REDUCTASE1 plays a crucial role in leaf responses to intracellular hydrogen peroxide and in ensuring appropriate gene expression through both salicylic acid and jasmonic acid signaling pathways. Plant Physiol 153:1144–1160. doi:10.1104/pp.110.153767
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. doi:10.1016/j.tplants.2004.08.009
Mittova V, Theodoulou FL, Kiddle G, Gómez L, Volokita M, Tal M, Foyer CH, Guy M (2003) Coordinate induction of glutathione biosynthesis and glutathione-metabolizing enzymes is correlated with salt tolerance in tomato. FEBS Lett 554:417–421. doi:10.1016/S0014-5793(03)01214-6
Morita S, Kaminaka H, Masumura T, Tanaka K (1999) Induction of rice cytosolic ascorbate peroxidase mRNA by oxidative stress; involvement of hydrogen peroxide in oxidative stress signaling. Plant Cell Physiol 40:417–422
Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944. doi:10.1016/S0092-8674(03)00429-X
Moura JCMS, Bonine CAV, de Oliveira Fernandes Viana J, Dornelas MC, Mazzafera P (2010) Abiotic and biotic stresses and changes in the lignin content and composition in plants. J Integr Plant Biol 52:360–376. doi:10.1111/j.1744-7909.2010.00892.x
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. doi:10.1111/j.1399-3054.1962.tb08052.x
Narusaka Y, Narusaka M, Seki M, Umezawa T, Ishida J, Nakajima M, Enju A, Shinozaki K (2004) Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant Mol Biol 55:327–342
Nawrath C, Heck S, Parinthawong N, Métraux J-P (2002) EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell 14:275–286. doi:10.1105/tpc.010376
Neuhoff V, Arold N, Taube D, Ehrhardt W (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9:255–262. doi:10.1002/elps.1150090603
Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant, Cell Environ 35:454–484. doi:10.1111/j.1365-3040.2011.02400.x
Nour-Eldin HH, Andersen TG, Burow M, Madsen SR, Jørgensen ME, Olsen CE, Dreyer I, Hedrich R, Geiger D, Halkier BA (2012) NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds. Nature. doi:10.1038/nature11285
Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182. doi:10.1105/tpc.7.2.173
Parisy V, Poinssot B, Owsianowski L, Buchala A, Glazebrook J, Mauch F (2007) Identification of PAD2 as a gamma-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J 49:159–172. doi:10.1111/j.1365-313X.2006.02938.x
Perez-Amador MA, Leon J, Green PJ, Carbonell J (2002) Induction of the arginine decarboxylase ADC2 gene provides evidence for the involvement of polyamines in the wound response in Arabidopsis. Plant Physiol 130:1454–1463. doi:10.1104/pp.009951
Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009. doi:10.1006/bbrc.2001.6299
Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655–11660. doi:10.1073/pnas.97.21.11655
Schlaeppi K, Bodenhausen N, Buchala A, Mauch F, Reymond P (2008) The glutathione-deficient mutant pad2-1 accumulates lower amounts of glucosinolates and is more susceptible to the insect herbivore Spodoptera littoralis. Plant J 55:774–786. doi:10.1111/j.1365-313X.2008.03545.x
Schlaeppi K, Abou-Mansour E, Buchala A, Mauch F (2010) Disease resistance of Arabidopsis to Phytophthora brassicae is established by the sequential action of indole glucosinolates and camalexin. Plant J 62:840–851. doi:10.1111/j.1365-313X.2010.04197.x
Sinha R, Chattopadhyay S (2011) Changes in the leaf proteome profile of Mentha arvensis in response to Alternaria alternata infection. J Proteomics 74:327–336. doi:10.1016/j.jprot.2010.11.009
Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3:Article 3. doi: 10.2202/1544-6115.1027
Spies JR, Chambers DC (1949) Chemical determination of tryptophan in proteins. Anal Chem 21:1249. doi:10.1021/ac60034a033
Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B (2007) Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J 50:660–677. doi:10.1111/j.1365-313X.2007.03078.x
Sung DY, Vierling E, Guy CL (2001) Comprehensive expression profile analysis of the Arabidopsis hsp70 gene family. Plant Physiol 126:789–800. doi:10.1104/pp.126.2.789
Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956. doi:10.1126/science.1156970
Tsakraklides G, Martin M, Chalam R, Tarczynski MC, Schmidt A, Leustek T (2002) Sulfate reduction is increased in transgenic Arabidopsis thaliana expressing 5′-adenylylsulfate reductase from Pseudomonas aeruginosa. Plant J 32:879–889. doi:10.1046/j.1365-313X.2002.01477.x
Vadassery J, Tripathi S, Prasad R, Varma A, Oelmüller R (2009) Monodehydroascorbate reductase 2 and dehydroascorbate reductase 5 are crucial for a mutualistic interaction between Piriformospora indica and Arabidopsis. J Plant Physiol 166:1263–1274. doi:10.1016/j.jplph.2008.12.016
Wang KL-C, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14(Suppl):S131–S151. doi:10.1105/tpc.001768
Wang X, Fang G, Li Y, Ding M, Gong H, Li Y (2013) Differential antioxidant responses to cold stress in cell suspension cultures of two subspecies of rice. Plant Cell Tissue Org 113:353–361. doi:10.1007/s11240-012-0273-z
Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565. doi:10.1038/35107108
Wingate VPM, Lawton MA, Lamb CJ (1988) Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol 87:206–210. doi:10.1104/pp.87.1.206
Witt SN, Flower TR (2006) alpha-Synuclein, oxidative stress and apoptosis from the perspective of a yeast model of Parkinson’s disease. FEMS Yeast Res 6:1107–1116. doi:10.1111/j.1567-1364.2006.00135.x
Woo HJ, Sohn SI, Shin KS, Kim JK, Kim BG, Lim MH (2014) Expression of tobacco tocopherol cyclase in rice regulates antioxidative defense and drought tolerance. Plant Cell Tiss Org. doi:10.1007/s11240-014-0530-4
Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35:155–189. doi:10.1146/annurev.pp.35.060184.001103
Yang Y, Shi R, Wei X, Fan Q, An L (2010) Effect of salinity on antioxidant enzymes in calli of the halophyte Nitraria tangutorum Bobr. Plant Cell Tiss Organ Cult 102:387–395. doi:10.1007/s11240-010-9745-1
Yang G, Wang Y, Xia D, Gao C, Wang C, Yang C (2014) Overexpression of a GST gene (ThGSTZ1) from Tamarix hispida improves drought and salinity tolerance by enhancing the ability to scavenge reactive oxygen species. Plant Cell Tiss Org 117:99–112. doi:10.1007/s11240-014-0424-5
Yanhui C, Xiaoyuan Y, Kun H, Meihua L, Jigang L, Zhaofeng G, Zhiqiang L, Yunfei Z, Xiaoxiao W, Xiaoming Q, Yunping S, Li Z, Xiaohui D, Jingchu L, Xing-Wang D, Zhangliang C, Hongya G, Li-Jia Q (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60:107–124. doi:10.1007/s11103-005-2910-y
Yoshida S, Tamaoki M, Ioki M, Ogawa D, Sato Y, Aono M, Kubo A, Saji S, Saji H, Satoh S, Nakajima N (2009) Ethylene and salicylic acid control glutathione biosynthesis in ozone-exposed Arabidopsis thaliana. Physiol Plant 136:284–298. doi:10.1111/j.1399-3054.2009.01220.x
Zhu Q, Zhang J, Gao X, Tong J, Xiao L, Li W, Zhang H (2010) The Arabidopsis AP2/ERF transcription factor RAP2.6 participates in ABA, salt and osmotic stress responses. Gene 457:1–12. doi:10.1016/j.gene.2010.02.011
Acknowledgments
We acknowledge the Department of Science and Technology (DST), and Council of Scientific and Industrial Research (CSIR), New Delhi, India, for necessary funding. Research activities have been supported by fellowships to RS, DK and DB from CSIR, and RD, ABM, RM, AS and SH from Indian Council of Medical Research (ICMR), DST-INSPIRE, DST and University Grant Commission (UGC), New Delhi, India, respectively. Central proteomics facility of CSIR-IICB, Kolkata and iLife Discoveries, New Delhi is acknowledged herewith.
Conflict of interest
The authors have no conflict in interest to disclose.
Author information
Authors and Affiliations
Corresponding author
Additional information
Ragini Sinha and Deepak Kumar have contributed equally to this article.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sinha, R., Kumar, D., Datta, R. et al. Integrated transcriptomic and proteomic analysis of Arabidopsis thaliana exposed to glutathione unravels its role in plant defense. Plant Cell Tiss Organ Cult 120, 975–988 (2015). https://doi.org/10.1007/s11240-014-0651-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-014-0651-9