Log in

Comparative proteome analysis of high and low cadmium accumulating soybeans under cadmium stress

  • Original Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

A comparative proteomic study was performed to unravel the protein networks involved in cadmium stress response in soybean. Ten-day-old seedlings of contrasting cadmium accumulating soybean cultivars—Harosoy (high cadmium accumulator), Fukuyutaka (low cadmium accumulator), and their recombinant inbred line CDH-80 (high cadmium accumulator) were exposed to 100 μM CdCl2 treatment for 3 days. Root growth was found to be affected under cadmium stress in all. Varietal differences at root protein level were evaluated. NADP-dependent alkenal double bond reductase P1 was found to be more abundant in low cadmium accumulating Fukuyutaka. Leaf proteome analysis revealed that differentially expressed proteins were primarily involved in metabolism and energy production. The results indicate that both high and low cadmium accumulating cultivars and CDH-80 share some common defense strategies to cope with the cadmium stress. High abundance of enzymes involved in glycolysis and TCA cycle might help cadmium challenged cells to produce more energy necessary to meet the high energy demand. Moreover, enhanced expressions of photosynthesis related proteins indicate quick utilization of photoassimilates in energy generation. Increased abundance of glutamine synthetase in all might be involved in phytochelatin mediated detoxification of cadmium ions. In addition, increased abundance of antioxidant enzymes, namely superoxide dismutase, ascorbate peroxidase, catalase, ensures cellular protection from reactive oxygen species mediated damages under cadmium stress. Enhanced expression of molecular chaperones in high cadmium accumulating cultivar might be another additional defense mechanism for refolding of misfolded proteins and to stabilize protein structure and function, thus maintain cellular homeostasis.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

2-DE:

Two-dimensional polyacrylamide gel electrophoresis

CBB:

Coomassie brilliant blue

MS:

Mass spectrometry

pI :

Isoelectric point

IEF:

Isoelectric focusing

ROS:

Reactive oxygen species

LC:

Liquid chromatography

GS:

Glutamine synthetase

GSH:

Glutathione

SOD:

Superoxide dismutase

References

  • Ahsan N, Lee SH, Lee DG, Lee H, Lee SW, Bahk JD et al (2007) Physiological and protein profiles alternation of germinating rice seedlings exposed to acute cadmium toxicity. CR Biol 330:735–746

    Article  CAS  Google Scholar 

  • Ahsan N, Nakamura T, Komatsu S (2012) Differential responses of microsomal proteins and metabolites in two contrasting cadmium (Cd)-accumulating soybean cultivars under Cd stress. Amino Acids 42:317–327

    Article  PubMed  CAS  Google Scholar 

  • Aina R, Labra M, Fumagalli P, Vannini C, Marsoni M, Cucchi U et al (2007) Thiolpeptide level and proteomic changes in response to cadmium toxicity in Oryza sativa L. roots. Environ Exp Bot 59:381–392

    Article  CAS  Google Scholar 

  • Alvarez S, Berla BM, Sheffield J, Cahoon RE, Jez JM, Hicks LM (2009) Comprehensive analysis of the Brassica juncea root proteome in response to cadmium exposure by complementary proteomic approaches. Proteomics 9:2419–2431

    Article  PubMed  CAS  Google Scholar 

  • Arao T, Ae N, Sugiyama M, Takahashi M (2003) Genotypic differences in cadmium uptake and distribution in soybeans. Plant Soil 251:247–253

    Article  CAS  Google Scholar 

  • Barber DJW, Thomas JK (1978) Reactions of radicals with lecithin bilayers. Radiat Res 74:51–58

    Article  CAS  Google Scholar 

  • Barranco-Medina S, Lazaro JJ, Dietz KJ (2009) The oligomeric conformation of peroxiredoxins links redox state to function. FEBS Lett 583:1809–1816

    Article  PubMed  CAS  Google Scholar 

  • Baryla A, Carrier P, Franck F, Coulomb C, Sahut C, Havaux M (2001) Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth. Planta 212:696–709

    Article  PubMed  CAS  Google Scholar 

  • Benavides MP, Gallego SM, Tomaro M (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:21–34

    Article  CAS  Google Scholar 

  • Bevan M, Bancroft I, Bent E, Love K, Goodman H, Dean C et al (1998) Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 391:485–488

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Dietz KJ (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54:93–107

    Article  PubMed  CAS  Google Scholar 

  • Dixit V, Pandey V, Shyam R (2001) Differential oxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). J Exp Bot 52:1101–1109

    Article  PubMed  CAS  Google Scholar 

  • Durand TC, Sergeant K, Planchon S, Carpin S, Label P, Morabito D, Hausman JF, Renaut J, Durand TC, Sergeant K, Planchon S, Carpin S, Label P, Morabito D, Hausman JF, Renaut J (2010) Acute metal stress in Populus tremula x P. alba (717-1B4 genotype): leaf and cambial proteome changes induced by cadmium2+. Proteomics 10:349–368

    Article  PubMed  CAS  Google Scholar 

  • Grill E, Löffler S, Winnacker EL, Zenk MH (1989) Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific gamma-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc Natl Acad Sci USA 86:6838–6842

    Article  PubMed  CAS  Google Scholar 

  • Hajduch M, Rakwal R, Agrawal GK, Yonekura M, Pretova A (2001) High-resolution two-dimensional electrophoresis separation of proteins from metal-stressed rice (Oryza sativa L.) leaves: drastic reductions/fragmentation of ribulose-1,5-bisphosphate carboxylase/oxygenase and induction of stress-related proteins. Electrophoresis 22:2824–2831

    Article  PubMed  CAS  Google Scholar 

  • Hart JJ, Welch RM, Norvell WA, Sullivan LA, Kochian LV (1998) Characterization of cadmium binding, uptake, and translocation in intact seedlings of bread and durum wheat cultivars. Plant Physiol 116:1413–1420

    Article  PubMed  CAS  Google Scholar 

  • Hernández LE, Cárpena-Ruiz R, Garate A (1996) Alterations in the mineral nutrition of pea seedlings exposed to cadmium. J Plant Nutr 19:1581–1598

    Article  Google Scholar 

  • Hradilová J, Rehulka P, Rehulková H, Vrbová M, Griga M, Brzobohatý B (2010) Comparative analysis of proteomic changes in contrasting flax cultivars upon cadmium exposure. Electrophoresis 31:421–431

    Article  PubMed  Google Scholar 

  • Kieffer P, Dommes J, Hoffmann L, Hausman JF, Renaut J (2008) Quantitative changes in protein expression of cadmium-exposed poplar plants. Proteomics 8:2514–2530

    Article  PubMed  CAS  Google Scholar 

  • Kieffer P, Planchon S, Oufir M, Ziebel J, Dommes J, Hoffmann L, Hausman JF, Renaut J (2009a) Combining proteomics and metabolite analyses to unravel cadmium stress-response in poplar leaves. J Proteome Res 8:400–417

    Article  PubMed  CAS  Google Scholar 

  • Kieffer P, Schroder P, Dommes J, Hoffmann L et al (2009b) Proteomic and enzymatic response of poplar to cadmium stress. J Proteomics 72:379–396

    Article  PubMed  CAS  Google Scholar 

  • Lee K, Bae DW, Kim SH, Han HJ et al (2010) Comparative proteomic analysis of the short-term responses of rice roots and leaves to cadmium. J Plant Physiol 167:161–168

    Article  PubMed  CAS  Google Scholar 

  • Lu LL, Tian SK, Yang XE, Wang XC, Brown P, Li TQ, He ZL (2008) Enhanced root-to-shoot translocation of cadmium in the hyperaccumulating ecotype of Sedum alfredii. J Exp Bot 59:3203–3213

    Article  PubMed  CAS  Google Scholar 

  • Mano J, Belles-Boix E, Babiychuk E, Inzé D, Torii Y, Hiraoka E et al (2005) Protection against photooxidative injury of tobacco leaves by 2-alkenal reductase. Detoxication of lipid peroxide-derived reactive carbonyls. Plant Physiol 139:1773–1783

    Article  PubMed  CAS  Google Scholar 

  • Mishra S, Srivastava S, Tripathi RD, Govindarajan R, Kuriakose SV, Prasad MN (2006) Phytochelatin synthesis and response of antioxidants during cadmium stress in Bacopa monnieri L. Plant Physiol Biochem 44:25–37

    Article  PubMed  CAS  Google Scholar 

  • Nocito FF, Lancilli C, Giacomini B, Gian AS (2007) Sulfur metabolism and cadmium stress in higher plants. Plant Stress 1:142–156

    Google Scholar 

  • Rodriguez-Celma J, Rellan-Alvarez R, Abadia A, Abadia J, Lopez-Millan AF (2010) Changes induced by two levels of cadmium toxicity in the 2-DE protein profile of tomato roots. J Proteomics 73:1694–1706

    Article  PubMed  CAS  Google Scholar 

  • Roth U, von Roepenack-Lahaye E, Clemens S (2006) Proteome changes in Arabidopsis thaliana roots upon exposure to Cd2+. J Exp Bot 57:4003–4013

    Article  PubMed  CAS  Google Scholar 

  • Sanita di Toppi L, Gabrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130

    Article  Google Scholar 

  • Sarry JE, Kuhn L, Ducruix C, Lafaye A, Junot C, Hugouvieux V et al (2006) The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 6:2180–2198

    Article  PubMed  CAS  Google Scholar 

  • Semane B, Dupae J, Cuypers A, Noben JP, Tuomainen M, Tervahauta A, Kärenlampi S, Van Belleghem F, Smeets K, Vangronsveld J (2010) Leaf proteome responses of Arabidopsis thaliana exposed to mild cadmium stress. J Plant Physiol 167:247–254

    Article  PubMed  CAS  Google Scholar 

  • Sobkowiak R, Deckert J (2006) Proteins induced by cadmium in soybean cells. J Plant Physiol 163:1203–1206

    Article  PubMed  CAS  Google Scholar 

  • Tran LS, Mochida K (2010) Functional genomics of soybean for improvement of productivity in adverse conditions. Funct Integr Genomics 10:447–462

    Article  PubMed  CAS  Google Scholar 

  • Tuomainen MH, Nunan N, Lehesranta SJ, Tervahauta AI, Hassinen VH, Schat H et al (2006) Multivariate analysis of protein profiles of metal hyperaccumulator Thlaspi caerulescens accessions. Proteomics 6:3696–3706

    Article  PubMed  CAS  Google Scholar 

  • Uraguchi S, Kamiya T, Sakamoto T, Kasai K, Sato Y, Nagamura Y et al (2011) Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. Proc Natl Acad Sci USA 108:20959–20964

    Article  PubMed  CAS  Google Scholar 

  • Vassilev A, Iordanov I, Chakalova E, Kerin V (1995) Effect of cadmium stress on growth and photosynthesis of young barley (H. vulgare L.) plants. 2. Structural and functional changes in the photosynthetic apparatus. Bulg J Plant Physiol 1:12–21

    Google Scholar 

  • Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 2:364–372

    Article  Google Scholar 

  • Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42:579–620

    Article  CAS  Google Scholar 

  • Villiers F, Ducruix C, Hugouvieux V, Jarno N, Ezan E, Garin J et al (2011) Investigating the plant response to cadmium exposure by proteomic and metabolomic approaches. Proteomics 1:1650–1663

    Article  Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    Article  PubMed  CAS  Google Scholar 

  • Welch RM, Norvell WA (1999) Mechanisms of cadmium uptake, translocation and deposition in plants. In: McLaughlin MJ, Singh BR (eds) Cadmium in soils and plants. Kluwer Academic Publishers, Dordrecht, pp 125–150

    Chapter  Google Scholar 

  • Zhao FJ, Hamon RE, Lombi E, McLaughlin MJ, McGrath SP (2002) Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. J Exp Bot 53:535–543

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The author Z.H. thankfully acknowledges the financial support provided through the DST-BOYSCAST fellowship programme, Govt. of India. We thank the National Institute of Crop Science, Tsukuba, Japan for providing all the necessary facilities. The authors also thank Dr. Yohei Nanjo and Dr. Keito Nishazawa for their valuable suggestions.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Setsuko Komatsu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hossain, Z., Hajika, M. & Komatsu, S. Comparative proteome analysis of high and low cadmium accumulating soybeans under cadmium stress. Amino Acids 43, 2393–2416 (2012). https://doi.org/10.1007/s00726-012-1319-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-012-1319-6

Keywords

Navigation