Skip to main content
SpringerLink
Log in

Salt stress-induced modulations in the shoot proteome of Brassica juncea genotypes

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Indian mustard [Brassica juncea (L.) Czern and Coss] is cultivated mainly in the northwestern agroclimatic region of India and suffers huge losses in productivity due to salinization. In an effort to figure out adaptation strategies of Indian mustard to salt stress, we conducted a comparative proteome analysis of shoots of its two genotypes, with contrasting sensitivity to salt stress. Differential expression of 21 proteins was observed during the two-dimensional electrophoresis (2DE). The identified salt-stress-responsive proteins were associated with different functional processes including osmoregulation, photosynthesis, carbohydrate metabolism, ion homeostasis, protein synthesis and stabilization, energy metabolism, and antioxidant defense system. Salt-tolerant genotype (CS-52) showed a relatively higher expression of proteins involved in turgor regulation, stabilization of photosystems and proteins, and salt compartmentalization, as compared to salt-sensitive genotype (Pusa Varuna). Our results suggest that modulating the expression of salt-responsive proteins can pave the way for developing salt tolerance in the Indian mustard plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agoston BS, Kovacs D, Tompa P, Perczel A (2011) Full backbone assignment and dynamics of the intrinsically disordered dehydrin ERD14. J Biomol NMR 5:189–193

    Article  CAS  Google Scholar 

  • Amira MS, Qados A (2011) Effect of salt stress on plant growth and metabolism of bean plant, Vicia faba L. J Saudi Society Agric Sci 10(1):7–12

    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 (2015) 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

    Article  CAS  Google Scholar 

  • Aref MI, Ahmed AI, Khan PR, El-Atta H, Iqbal M (2013) Drought-induced adaptive changes in the seedling anatomy of Acacia ehrenbergiana and Acacia tortilis subsp raddiana. Trees Struct Func 27:959–971. doi:10.1007/s00468-013-0848-2

    Article  Google Scholar 

  • Bashir H, Qureshi MI, Ibrahim MM, Iqbal M (2015) Chloroplast and photosystems: Impact of cadmium and iron deficiency. Photosynthetica 53(3):321–335. doi:10.1007/s11099-015-0152-z

    Article  CAS  Google Scholar 

  • Budak H, Akpinar BA, Unver T, Turktas M (2013) Proteome changes in wild and modern wheat leaves upon drought stress by two-dimensional electrophoresis and nanoLC-ESI–MS/MS. Plant Mol Biol 83:89–103

    Article  CAS  Google Scholar 

  • Carillo P, Annunziata MG, Pontecorvo G, Fuggi A, Woodrow P (2011) Salinity stress and salt tolerance. In: Shanker AK, Venkateswarlu B (eds) Abiotic stress in plants—mechanisms and adaptations. InTech, Croatia - European Union. ISBN: 978-953-307-394-1, pp 21–38

  • Carmo-Silvaa AE, Gorea MA, Andrade-Sanchez P, Frencha AN, Hunsaker DJ, Salvucci ME (2012) Decreased CO2 availability and inactivation of Rubisco limit photosynthesis in cotton plants under heat and drought stress in the field. Environ Exp Bot 83:1–11

    Article  CAS  Google Scholar 

  • Chomczynski  P, Sacchi N (1987)  Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159

  • Cramer GR, Ergül A, Grimplet J, Tillett RL et al (2007) Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct Integr Genomics 7:111–134

    Article  CAS  Google Scholar 

  • Fatehi F, Hosseinzadeh A, Alizadeh H, Brimavandi T, Struik PC (2012) The proteome response of salt-resistant and salt-sensitive barley genotypes to long-term salinity stress. Mol Biol Rep 39:6387–6397

    Article  CAS  Google Scholar 

  • Feller U, Anders I, Demirevska K (2008) Degradation of rubisco and other chloroplast proteins under abiotic stress. Gen Appl Plant Physiol 34(1–2):5–18

    CAS  Google Scholar 

  • Fu J, Momcilovic I, Prasad PVV (2012) Roles of protein synthesis elongation factor EF-Tu in heat tolerance in plants. J.Bot. doi10.1155/2012/835836

  • Ghaffari A, Gharechahi J, Nakhodaa B, Salekdehc GH (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  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hakeem KR, Mir BA, Qureshi MI, Ahmad A, Iqbal M (2013) Proteomic analysis of differentially expressed proteins and their role in the roots of N-efficient rice (Oryza sativa L.). Mol Breeding 32(4):785–798

    Article  CAS  Google Scholar 

  • Iqbal M, Ahmad A, Ansari MKA, Qureshi MI, Aref MI, Khan PR, Hegazy SS, El-Atta H, Husen A, Hakeem KR (2015) Improving the phytoextraction capacity of plants to scavenge metal(loid)-contaminated sites. Environ Rev 23(1):44–65. doi:10.1139/er-2014-0043

    Article  CAS  Google Scholar 

  • Isaacson T, Damasceno CM, Saravanan RS, He Y, Catala C, Saladie M, Rose JK (2006) Sample extraction techniques for enhanced proteomic analysis of plant tissues. Nat Protoc 1(2):769–774

    Article  CAS  Google Scholar 

  • Jabeen R, Ahmad A, Iqbal M (2009) Phytoremediation of heavy metals: Physiological and molecular aspects. Bot Rev 75:339–364

    Article  Google Scholar 

  • Khan S, Andralojc PJ, Lea PJ, Parry MAJ (1999) 2-Carboxy-d-arabitinol 1-phosphate protects ribulose 1,5-bisphosphate carboxylase/oxygenase against proteolytic breakdown. Eur J Biochem 266:840–847

    Article  CAS  Google Scholar 

  • Khare T, Kumar V, Kishor PBK (2014) Na+ and Cl− ions show additive effects under NaCl stress on induction of oxidative stress and the responsive antioxidative defense in rice. Protoplasma. doi10.1007/s00709-014-0749-2

  • Li XP, Gilmore AM, Caffarri S, Bassi R, Golan T, Kramer D, Niyogi KK (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem 279(22):22866–22874

    Article  CAS  Google Scholar 

  • Liu XD, Shen YG (2004) NaCl-induced phosphorylation of light harvesting chlorophyll a/b proteins in thylakoid membranes from the halotolerant green alga, Dunaliella salina. FEBS Lett 569(1–3):337–340

    Article  CAS  Google Scholar 

  • Lokesh U, Kiranmai K, Pandurangaiah M, Sudhakarbabu O, Nareshkumar A, Sudhakar C (2013) Role of plant fatty acid elongase (3 keto acyl-CoA synthase) gene in cuticular wax biosynthesis. J Agric Allied Sci 2(4):35–42

    Google Scholar 

  • Madan S, Nainawatee HS, Jain RK, Chowdhury JB (1995) Proline and proline metabolizing enzymes in in-vitro selected NaCl-tolerant Brassica juncea L. under salt stress. Annals Bot 76:51–57

    Article  CAS  Google Scholar 

  • Majoul T, Bancel E, Triboi E, Ben Hamida J, Branlard G (2004) Proteomic analysis of the effect of heat stress on hexaploid wheat grain: characterization of heat-responsive proteins from non-prolamins fraction. Proteomics 4:505–13

    Article  CAS  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 

  • Nayyar H, Walia DP (2003) Water stress induced proline accumulation in contrasting wheat genotypes as affected by calcium and abscisic acid. Biol Plant 46:275–279

    Article  CAS  Google Scholar 

  • Nazar R, Iqbal N, Syeed S, Khan NA (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  Google Scholar 

  • Nounjana N, Nghia PT, Theerakulpisut P (2012) Exogenous proline and trehalose promote recovery of rice seedlings from salt-stress and differentially modulate antioxidant enzymes and expression of related genes. J Plant Physiol 169:596–604

    Article  CAS  Google Scholar 

  • Nunes-Nesi A, Carrari F, Lytovchenko A, Smith AM, Loureiro ME, Ratcliffe RG, Sweetlove LJ, Fernie AR (2005) Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiol 137:611–622

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Petrusa LM, Winicov I (1997) Proline status in salt tolerant and salt sensitive alfalfa cell lines and plants in response to NaCl. Plant Physiol Biochem 35:303–310

    CAS  Google Scholar 

  • Portis AR (2003) Rubisco activase—Rubisco’s catalytic chaperone. Photosynthesis Res 75:11–27

    Article  CAS  Google Scholar 

  • Qureshi MI, Abdin MZ, Ahmad J, Iqbal M (2013) Effect of long-term salinity on cellular antioxidants, compatible solute and fatty acid profile of Sweet annie (Artemisia annua L.). Phytochem 95:215–223

    Article  CAS  Google Scholar 

  • Rai S, Agrawal C, Shrivastava AK, Singh PK, Rai LC (2014) Comparative proteomics unveils cross species variations in Anabaena under salt stress. J Proteomics 98:254–270

    Article  CAS  Google Scholar 

  • Rasool S, Ahmad A, Siddiqi TO, Ahmad P (2013) Changes in growth, lipid peroxidation and some key antioxidant enzymes in chickpea genotypes under salt stress. Acta Physiol Plant 35:1039–1050

    Article  CAS  Google Scholar 

  • Salvucci ME (2008) Association of Rubisco activase with chaperonin-60b: a possible mechanism for protecting photosynthesis during heat stress. J Exp Bot 59(7):1923–1933

    Article  CAS  Google Scholar 

  • Sharada P, Naik GR (2011) Δ1-Pyrroline-5-carboxylate synthetase(P5CS) - Isolation, partial purification, and its characterization. Recent Res Sci Tech 3(12):29–32

    CAS  Google Scholar 

  • Sumithra K, Reddy AR (2004) Changes in proline metabolism of cowpea seedlings under water deficit. J Plant Biol 31:201–204

    CAS  Google Scholar 

  • Ueda A, Kathiresan A, Bennett J, Takabe T (2006) Comparative transcriptome analyses of barley and rice under salt stress. Theor Appl Genet 112:1286–1294

    Article  CAS  Google Scholar 

  • Vaseva I, Sabotic J, Sustar-Vozlic J, Meglic V, Kidric M, Demirevska K, Simova-Stoilova L (2011) The response of plants to drought stress – the role of dehydrins, chaperones, proteases and protease inhibitors in maintaining cellular protein function. In: Neves DF, Sanz JD (eds) Droughts: New Research. Nova Science Publishers, New York, pp 1–46

    Google Scholar 

  • Xu Y, Liu R, Yan L, Li Z, Jiang S, Shen Y, Wang X, Zhang D (2011) Light-harvesting chlorophyll a/b-binding proteins are required for stomatal response to abscisic acid in Arabidopsis. J Exp Bot 63:1095–106

    Article  CAS  Google Scholar 

  • Zhu JK (2003) Regulation of homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The first author is grateful to Hamdard National Foundation New Delhi (India) for granting a Research Fellowship.

Author information

Authors and Affiliations

  1. Molecular Ecology Laboratory, Department of Botany, Jamia Hamdard, New Delhi, 110062, India

    Peerzada Yasir Yousuf, Altaf Ahmad, Arshid Hussain Ganie & Muhammad Iqbal

Authors
  1. Peerzada Yasir Yousuf
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Altaf Ahmad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Arshid Hussain Ganie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Muhammad Iqbal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Muhammad Iqbal.

Additional information

Responsible editor: Philippe Garrigues

Additional file

Below is the link to the electronic supplementary material.

Additional file 1: Table S1

Spot intensity of salt stress-responsive shoot proteins of Indian mustard genotypes (Pusa Varuna and CS-52) under the control and salt-stress conditions. (DOCX 19 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yousuf, P.Y., Ahmad, A., Ganie, A.H. et al. Salt stress-induced modulations in the shoot proteome of Brassica juncea genotypes. Environ Sci Pollut Res 23, 2391–2401 (2016). https://doi.org/10.1007/s11356-015-5441-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-5441-3

Keywords

Search

Navigation