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Antioxidant response and proteomic modulations in Indian mustard grown under salt stress

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Abstract

Productivity of Indian mustard (Brassica juncea L. Czern. and Coss.) is markedly reduced by salt stress. To develop salt tolerance in this important oilseed crop is a need of the hour. This study, based on analysis of growth parameters and antioxidant profile of fourteen Indian mustard genotypes treated with 50, 100, 150 and 200 mM of sodium chloride, was performed to identify the salt-sensitive and salt-tolerant genotypes. Salinity stress inhibited biomass accumulation and reduced the protein and chlorophyll contents in a dose-dependent manner. The reduction was the highest in genotype Pusa Agrani and lowest in CS-54, depicting their contrasting sensitivity to salt stress. Salt treatments triggered a concentration-dependent overproduction of reactive-oxygen species and a concurrent upregulation of the expression of different antioxidants. Genotype CS-54 showed the least damage and maintained a high antioxidant level with almost each salt treatment, exhibiting its competence to withstand the damage provoked by salinity stress. Genotype Pusa Agrani, on the contrary, depicted a salt-sensitive nature by way of its very high lipid peroxidation and low intensity of antioxidants. These two genotypes were further investigated through gel-based proteomic approach, which resulted in the identification and quantification of 42 salinity-responsive proteins related to different metabolic modifications. Molecular processes, including photosynthesis, redox homeostasis, nitrogen metabolism, ATP synthesis, protein synthesis and degradation, signal transduction and respiratory pathways, have exhibited significant changes. The identified stress-responsive proteins could pave the way to develop salt tolerance in Indian mustard plant, thus sustaining its productivity under salinity.

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References

  • Abogadallah GM (2010) Antioxidative defense under salt stress. Plant Signal Behav 5:369–374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aebi H (1984) Catalase in vitro. Meth Enzymol 105:121–126

    Article  CAS  PubMed  Google Scholar 

  • Ahmad P, Hakeem KR, Kumar A, Ashraf M, Akram NA (2012) Salt-induced changes in photosynthetic activity and oxidative defense system of three cultivars of mustard (Brassica juncea L.). Afr J Biotechnol 11(11):2694–2703

    CAS  Google Scholar 

  • Anderson ME (1985) Determination of glutathione and glutathione disulfide in biological samples. Meth Enzymol 113:548–555

    Article  CAS  PubMed  Google Scholar 

  • Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E, Umar S, Ahmad A, Khan NA, Iqbal M, Prasad MNV (2012) Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids: a review. Environ Exp Bot 75:307–324

    CAS  Google Scholar 

  • Anjum NA, Sofo A, Scopam A, Roychoudhury A, Gill SS, Iqbal M, Lukatkin AS, Pereira E, Duarte AC, Ahmad I (2014) Lipids and proteins—major targets of oxidative modifications in abiotic stressed plants. Environ Sci Pollut Res 22(6):4099–4121. doi:10.1007/s11356-014-3917-1

    Article  Google Scholar 

  • Aref IM, Khan PR, Khan S, El-Atta H, Ahmed AI, Iqbal M (2016) Modulation of antioxidant enzymes in Juniperus procera needles in relation to habitat environment and dieback incidence. Trees Struct Funct. doi:10.1007/s00468-016-1399-0

    Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arshi A, Abdin MZ, Iqbal M (2004) Changes in biochemical status and growth performance of Senna (Cassia angustifolia Vahl.) grown under salt stress. Phytomorphology 54:109–124

    Google Scholar 

  • Arshi A, Ahmad A, Are IM, Iqbal M (2012) Comparative studies on antioxidant enzyme action and ion accumulation in soybean cultivars under salinity stress. J Environ Biol 33:9–20

    CAS  PubMed  Google Scholar 

  • Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16

    Article  CAS  Google Scholar 

  • Bandehagh A, Salekdeh GH, Toorchi M, Mohammadi A, Komatsu S (2011) Comparative proteomic analysis of canola leaves under salinity stress. Proteomics 11:1965–1975

    Article  CAS  PubMed  Google Scholar 

  • Bashir H, Qureshi MI, Ibrahim AM, Iqbal M (2015) Chloroplast and photosystems: impact of cadmium and iron deficiency. Photosynthetica 53:321–335

  • Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    Article  CAS  PubMed  Google Scholar 

  • Boex-Fontvieille E, Daventure M, Jossier M, Hodges M, Zivy M, Tcherkez G (2014) Phosphorylation pattern of Rubisco activase in Arabidopsis leaves. Plant Biol 16:550–557

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Busheva M, Tzonova I, Stoitchkova K, Andreeva A (2012) Heat-induced reorganization of the structure of photosystem II membranes: role of oxygen evolving complex. J Photochem Photobiol, B 117:214–221

    Article  CAS  Google Scholar 

  • Caruso G, Cavaliere C, Guarino C, Gubbiotti R, Foglia P, Lagana A (2008) Identification of changes in Triticum durum L. leaf proteome in response to salt stress by two-dimensional electrophoresis and MALDI-TOF mass spectrometry. Anal Bioanal Chem 391:381–390

    Article  CAS  PubMed  Google Scholar 

  • Du CX, Fan HF, Guo SR, Tezuka T, Li J (2010) Proteomic analysis of cucumber seedling roots subjected to salt stress. Phytochemistry 71:1450–1459

    Article  CAS  PubMed  Google Scholar 

  • Feller U, Anders I, Demirevska K (2008) Degradation of rubisco and other chloroplast proteins under abiotic stress. Gen Appl Plant Physiol 34:5–18

    CAS  Google Scholar 

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts, A proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antiox Redox Sign 11:861–905

    Article  CAS  Google Scholar 

  • Galmes J, Aranjuelo I, Medrano H et al (2013) Variation in Rubisco content and activity under variable climatic factors. Photosynth Res 117:73–90

    Article  CAS  PubMed  Google Scholar 

  • Gapinska M, Skodowska M, Gabara B (2008) Effect of short- and long-term salinity on the activities of antioxidative enzymes and lipid peroxidation in tomato roots. Acta Physiol Plant 30:11–18

    Article  CAS  Google Scholar 

  • Gengmao Z, Yu Z, Xing S et al (2015) Salinity stress increases secondary metabolites and enzyme activity in safflower. Indust Crops Prod 64(1):175–181. doi:10.1016/j.indcrop.2014.10.058

    Article  Google Scholar 

  • Ghaffari A, Gharechahi J, Nakhoda B et al (2014) Physiology and proteome responses of two contrasting rice mutants and their wild type parent under salt stress conditions at the vegetative stage. J Plant Physiol 171:31–44

    Article  CAS  PubMed  Google Scholar 

  • Guan Z, Chai T, Zhang Y et al (2009) Enhancement of Cd tolerance in transgenic tobacco plants overexpressing a Cd-induced catalase cDNA. Chemosphere 76(5):623–630

    Article  CAS  PubMed  Google Scholar 

  • Hakeem KR, Chandana R, Ahmad P, Iqbal M, Ozturk M (2012a) Relevance of proteomic investigations in plant abiotic stress physiology. OMICS 16(11):621–635

    Article  CAS  PubMed  Google Scholar 

  • Hakeem KR, Khan F, Chandna R, Siddiqui TO, Iqbal M (2012b) Genotypic variability among soybean genotypes under NaCl stress and proteome analysis of salt-tolerant genotype. Appl Biochem Biotechnol 168(8):2309–2329

    Article  CAS  PubMed  Google Scholar 

  • Harinasut P, Poonsopa D, Roengmongkol K et al (2003) Salinity effects on antioxidant enzymes in mulberry cultivar. Sci Asia 29:109–113

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophy 125:189–198

    Article  CAS  Google Scholar 

  • Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334

    Article  CAS  Google Scholar 

  • Hsieh TH, Li CH, Su RC et al (2010) A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 231:1459–1473

    Article  CAS  PubMed  Google Scholar 

  • Huergo LF, Chandra G, Merrick M (2013) PII signal transduction proteins: nitrogen regulation and beyond. FEMS Microbiol Rev 37:251–283

  • Iqbal M, Ahmad A, Ansari MKA et al (2015) Improving the phytoextraction capacity of plants to scavenge metal(loid)-contaminated sites. Environ Rev 23:44–65

  • Isaacson T, Damasceno CM, Saravanan RS et al (2006) Sample extraction techniques for enhanced proteomic analysis of plant tissues. Nat Protoc 1(2):769–774

    Article  CAS  PubMed  Google Scholar 

  • Jeong MJ, Park SC, Byun MO (2001) Improvement of salt tolerance in transgenic potato plants by glyceraldehyde-3 phosphate dehydrogenase gene transfer. Mol Cells 12:185–189

    CAS  PubMed  Google Scholar 

  • Ji H, Pardo JM, Batelli G et al (2013) The salt overly sensitive (SOS) pathway: established and emerging roles. Mol Plant 6(2):275–286

    Article  CAS  PubMed  Google Scholar 

  • Jiang Y, Yang B, Harris NS et al (2007) Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J Exp Bot 58:3591–3607

    Article  CAS  PubMed  Google Scholar 

  • Kim Y, Arihara J, Nakayama T, Nakayama N (2004) Antioxidative responses and their relation to salt tolerance in Echinochloa oryzicola Vasing and Steraia virdis (L.) Beauv. Plant Growth Regul 44:87–92

    Article  CAS  Google Scholar 

  • Kim DW, Rakwal R, Agrawal GK et al (2005) A hydroponic rice seedling culture model system for investigating proteome of salt stress in rice leaf. Electrophor 26:4521–4539

    Article  CAS  Google Scholar 

  • Kong-Ngern K, Daduang S, Wongkham CH et al (2005) Protein profiles in response to salt stress in leaf sheaths of rice seedlings. Sci Asia 31:403–408

    Article  CAS  Google Scholar 

  • Kukreja S, Nandval AS, Kumar N et al (2005) Plant water status, H2O2 scavenging enzymes, ethylene evolution and membrane integrity of Cicer arietinum roots as affected by salinity. Biol Plant 49:305–308

    Article  CAS  Google Scholar 

  • Kulik A, Mazur AA, Bucholc M et al (2004) Antioxidant responses of shoots and roots of lentil to NaCl salinity stress. Plant Growth Regul 42:69–77

    Article  Google Scholar 

  • Kulik A, Wawer I, Krzywinska E et al (2011) SnRK2 protein kinases-key regulators of plant response to abiotic stresses. OMICS 15:859–872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid in spinach chloroplasts. Biol Biochem J 210:899–903

    CAS  Google Scholar 

  • Lei P, Xu Z, Liang J, Luo X, Zhang Y, Feng X, Xu H (2016) Poly (γ-glutamic acid) enhanced tolerance to salt stress by promoting proline accumulation in Brassica napus L. Plant Growth Regul 78(2):233–241

    Article  CAS  Google Scholar 

  • Li C, Lv J, Zhao X et al (2010) TaCHP: a wheat zinc finger protein gene down-regulated by abscisic acid and salinity stress plays a positive role in stress tolerance. Plant Physiol 154:211–221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu S, Li T, Jiang J (2010) Effects of salinity on sucrose metabolism during tomato fruit development. Afr J Biotech 9(6):842–849

    Article  CAS  Google Scholar 

  • Lyzenga WJ, Stone SL (2012) Abiotic stress tolerance mediated by protein ubiquitination. J Exp Bot 63(2):599–616

    Article  CAS  PubMed  Google Scholar 

  • Manaa A, Mimouni H, Wasti S, Gharbi E, Aschi-Smiti S, Faurobert M, Ahmed HB (2013) Comparative proteomic analysis of tomato (Solanum lycopersicum) leaves under salinity stress. Plant Omics J 6(4):268–277

    CAS  Google Scholar 

  • Medeiros CD, Oliveira MT, Rivas R et al (2012) Gas exchange, growth, and antioxidant activity in sugarcane under biological nitrogen fixation. Photosynthetica 50:519–528

    Article  CAS  Google Scholar 

  • Meskiene I, Baudouin E, Schweighofer A et al (2003) Stress-induced protein phosphatase 2C Is a negative regulator of a mitogen-activated protein kinase. J Biol Chem 278(21):18945–18952

    Article  CAS  PubMed  Google Scholar 

  • Miranda RS, Gomes-Filho E, Prisco JT, Alvariz-Pizzaro JC (2016) Ammonium improves tolerance to salinity stress in Sorghum bicolor plants. Plant Growth Regul 78(1):121–131

    Article  CAS  Google Scholar 

  • Munns R, James RA (2003) Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant Soil 253:201–218

    Article  CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681

    Article  CAS  Google Scholar 

  • Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nazar R, Iqbal N, Syeed S et al (2011) Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. J Plant Physiol 168:807–815

    Article  CAS  PubMed  Google Scholar 

  • O’Farrel PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021

    Google Scholar 

  • Parihar R, Singh S, Singh R et al (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Environ Sci Pollut Res 22:4056–4075

    Article  CAS  Google Scholar 

  • Parker R, Flowers TJ, Moore AL et al (2006) An accurate and reproducible method for proteome profiling of the effects of salt stress in the rice leaf. J Exp Bot 57:1109–1118

    Article  CAS  PubMed  Google Scholar 

  • Paszkowski U, Kroken S, Roux C, Briggs S (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 99:13324–13329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Puig J, Meynard D, Khong GN et al (2013) Analysis of the expression of the AGL17-like clade of MADS-box transcription factors in rice. Gene Express Patter 13:160–170

    Article  CAS  Google Scholar 

  • Qadir M, Schubert S (2002) Degradation processes and nutrient constraints in sodic soils. Land Degrad Develop 13(4):275–294

    Article  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org/

  • Rais L, Masood A, Inam A, Khan N (2013) Sulfur and nitrogen co-ordinately improve photosynthetic efficiency, growth and proline accumulation in two cultivars of mustard under salt stress. J Plant Biochem Physiol 1:101

    Article  Google Scholar 

  • Rao MV (1992) Cellular detoxifying mechanisms determine age dependent injury in tropical plants exposed to SO2. J Plant Physiol 140:733–740

    Article  CAS  Google Scholar 

  • Rowley ER, Mockler TC (2011) Plant abiotic stress: insights from the genomics era. In: Shankar A, Venkateswarlu B (eds) Abiotic stress response in plants—physiological, biochemical and genetic perspectives. InTech Open, Rijeka, Croatia, pp 221–268

  • Sahi C, Singh A, Blumwald E, Grover A (2006) Beyond osmolytes and transporters: novel plant salt stress tolerance-related genes from transcriptional profiling data. Physiol Plant 127:1–9

    Article  CAS  Google Scholar 

  • Santos CV (2004) Regulation of chlorophyll biosynthesis and degradation by salt stress in sunflower leaves. Sci Hort 103:93–99

    Article  CAS  Google Scholar 

  • Shah SH (2007) Effects of salt stress on mustard as affected by gibberellic acid application. Gen App Plant Physiol 33(1–2):9–106

    Google Scholar 

  • Sharma P, Jha AB, Dubey RS et al (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:1–26

    Article  Google Scholar 

  • Sharma P, Sardana V, Banga SS (2013) Salt tolerance of Indian mustard (Brassica juncea) at germination and early seedling growth. Environ Exp Biol 11:39–46

    Google Scholar 

  • Shekhawat GS, Verma K (2010) Heme oxygenase (HO): an overlooked enzyme of plant metabolism and defence. J Exp Bot 61(9):2255–2270

    Article  CAS  PubMed  Google Scholar 

  • Sumithra K, Jutur PP, Carmel BD, Reddy AR (2006) Salinity-induced changes in two cultivars of Vigna radiata: responses of antioxidative and proline metabolism. Plant Growth Regul 50:11–22

    Article  CAS  Google Scholar 

  • Suorsa M, Aro EM (2007) Expression, assembly and auxiliary functions of photosystem II oxygen-evolving proteins in higher plants. Photosynth Res 93:89–100

    Article  CAS  PubMed  Google Scholar 

  • Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16(1):53–60

    Article  CAS  PubMed  Google Scholar 

  • Uhrig GR, Kenneth KS, Greg BG et al (2009) PII in higher plants: a modern role for an ancient protein. Trend Plant Sci 14(9):505–511

    Article  CAS  Google Scholar 

  • Umezawa T, Yoshida R, Maruyama K et al (2004) SRK2C a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana. PNAS 101(49):17306–17311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Venkatesh J, Upadhyaya CP, Yu JW, Hemavathi A, Kim DH, Strasser RJ, Park SW (2012) Chlorophyll a fluorescence transient analysis of transgenic potato overexpressing d-galacturonic acid reductase gene for salinity stress tolerance. Hort Environ Biotechnol 53:320–328

    Article  CAS  Google Scholar 

  • Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Wei Z, Liu D et al (2011) Effects of NaCl and silicon on activities of antioxidative enzymes in roots, shoots and leaves of alfalfa. Afr J Biotechnol 10(4):545–549

    CAS  Google Scholar 

  • Yamamoto M, Nasrallah JB (2009) In planta assessment of the role of thioredoxin h proteins in the regulation of S-locus receptor kinase signaling in transgenic Arabidopsis. Plant Physiol 163:1387–1395

    Article  Google Scholar 

  • Yasar F, Ellialtioglu S, Yildiz K (2008) Effect of salt stress on antioxidant defense systems, lipid peroxidation and chlorophyll content in green bean. Russ J Plant Physiol 55(6):782–786

    Article  CAS  Google Scholar 

  • Yousuf PY, Hakeem KR, Chandna R, Ahmad P (2012) Role of glutathione reductase in plant abiotic stress. In: Ahmad P, Prasad MNV (eds) Abiotic stress responses in plants. Springer, New York, pp 149–158

    Chapter  Google Scholar 

  • Yousuf PY, Ahmad A, Ganie AH, Iqbal M (2016a) Salt stress-induced modulations in the shoot proteome of Brassica juncea genotypes. Environ Sci Pollut Res 23(3):2391–2401. doi:10.1007/s11356-015-5441-3

    Article  CAS  Google Scholar 

  • Yousuf PY, Ahmad A, Aref IM, Ozturk M, Hemant Ganie AH, Iqbal M (2016b) Salt-stress-responsive chloroplast proteins in Brassica juncea genotypes with contrasting salt tolerance and their quantitative PCR analysis. Protoplasma. doi:10.1007/s00709-015-0917-z

    PubMed  Google Scholar 

  • Zhang C, Liu J, Zhang Y, Cai X, Gong P, Zhang J, Wang T, Li H, Ye Z (2011) Overexpression of SlGMEs leads to ascorbate accumulation with enhanced oxidative stress, cold, and salt tolerance in tomato. Plant Cell Rep 30:389–398

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The first author is grateful to Hamdard National Foundation (HNF) New Delhi, India for granting a fellowship. The second author (A Ahmad) is now working at the Department of Botany, Aligarh Muslim University, Aligarh 202002, India.

Author contributions

P. Y. Yousuf conducted experimental research with the help of A. Ahmad and A. H. Ganie. Statistical analysis was done by O Sareer and V Krishnapriya. Data interpretation and MS preparation were done by M. Iqbal, A. Ahmad and I. M. Aref.

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10725_2016_182_MOESM1_ESM.jpg

Fig. S1: Plants of salt-tolerant genotype (CS-54) grown under (a) control and (b) 200 mM NaCl treatment and salt-sensitive genotype Pusa Agrani grown under (c) control and (d) 200 mM NaCl treatment, at the time of sampling (JPEG 244 kb)

10725_2016_182_MOESM2_ESM.jpg

Fig. S2: (a) Clustering and (b) PCA analysis based on biomass of 14 different genotypes of Indian mustard grown under salt stress. Correlation matrix was used for PCA. Clustering was done using the Ward’s method of Squared Euclidean distance matrix. PCA and clustering of biomass clearly differentiate V2 and V5. Arrows for all traits are directed towards V5 indicating that it is indeed a tolerant variety, whereas V2 presents an opposite case indicating its salt-sensitive nature. Cluster dendrogram also reflects similar results (JPEG 1077 kb)

10725_2016_182_MOESM3_ESM.jpg

Fig. S3: PCA analysis of 14 different genotypes of Indian mustard under different salt treatments (a) T0 (b) T1 (c) T2 (d) T3 (e) T4, based on physiological and biochemical parameters. Percentage values given in brackets in the axis labels denote R2 values (JPEG 1586 kb)

10725_2016_182_MOESM4_ESM.jpg

Fig. S4: Spot images of five representative proteins differentially-expressed during different salt treatments in salt-sensitive (Pusa Agrani) and salt-tolerant (CS-54) genotypes of Indian mustard (JPEG 189 kb)

Table S1: Description of Brassica juncea genotypes used in the study (DOC 47 kb)

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Yousuf, P.Y., Ahmad, A., Ganie, A.H. et al. Antioxidant response and proteomic modulations in Indian mustard grown under salt stress. Plant Growth Regul 81, 31–50 (2017). https://doi.org/10.1007/s10725-016-0182-y

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