Skip to main content

Advertisement

Log in

Aluminum toxicity-induced alterations in the leaf proteome of rice contrasting response towards inoculation of plant growth-promoting bacteria

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Aluminum (Al) toxicity is one of the primary factors limiting crop production on acid sulfate soils. In the present study, two-dimensional polyacrylamide gel electrophoresis approach (2D-PAGE) was applied to identify Al tolerance, plant growth promotion and separately expressed proteins were determined using mass spectrometry. Seedlings of rice were grown in an acid sulfate soil. Bio-fertilizer containing acid-tolerant and plant growth-promoting bacteria (PGPB) were given alone or in combination with ground magnesium limestone (GML) at 4 t ha−1. Leaf samples were taken at 45 days after transplanting. Results exhibited that the application of bio-fertilizer and GML increased soil pH and leaf chlorophyll content. Highest plant height, root length and tiller number were observed in the modified treatments. A total of eight different proteins have been identified to be differentially expressed in rice leaf tissues by mass spectrometry analysis that exposed the differential expression of certain vital proteins. The identified proteins were involved in tolerating abiotic stress, disease resistance, oxidation–reduction process and internal plant physiological functions. Results of analyzing multiple protein spots have shown their involvement for the promotion of plant development and reduction of Al toxicity. The study thus confirms the primary role of PGPB containing bio-fertilizer with GML on growth of rice under Al toxic conditions in acid sulfate soil.

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

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

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

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Abbreviations

2D DIGE:

Two-dimensional differential in gel electrophoresis

CHAPS:

3-[(3-Cholamidopropyl) dimethylammonio]-1-propanesulfonate

CI%:

Confidence interval percentage

DTT:

Dithiothreitol

GML:

Ground magnesium limestone

IPG:

Immobilized pH gradient

SDS-PAGE:

Sodium dodecyl sulfate polyacrylamide gel electrophoresis

TCA cycle:

Tricarboxylic acid cycle

References

  • Amin MA, Uddin MA, Hossain MA (2004) Regeneration study of some Indica rice cultivars followed by Agrobacterium-mediated transformation of highly regenerable cultivar BR-8. J Biol Sci 4:207–211

    Article  Google Scholar 

  • Barcelo J, Poschenrieder C (2002) Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminum toxicity and resistance: a review. Environ Exp Bot 48:75–79

    Article  CAS  Google Scholar 

  • Bedon F, Villari E, Vincent D (2011) Proteomic plasticity of two Eucalyptus genotypes under contrasted water regimes in the field. Plant Cell Environ 35(4):790–805

    Article  PubMed  Google Scholar 

  • Benton J Jr (2001) Laboratory guide for conducting soil tests and plant analysis”. CRC Press LLC, New York

    Book  Google Scholar 

  • Bevan M, Bancroft I, Bent E, Love K, Goodman H, Dean C, Bergkamp R, Dirske W, Van-Staveren M, Stiekema W (1998) Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 391:485–488

    Article  CAS  PubMed  Google Scholar 

  • Ciamporova M (2002) Morphological and structural responses of plant roots to aluminum at organ, tissue, and cellular levels. Biol Plant 45:161–171

    Article  CAS  Google Scholar 

  • Davey MW, Gudimella R, Harikrishna JA, Sin LW, Khalid N, Keulemans J (2013) A draft Musa balbisiana genome sequence for molecular genetics in polyploid, inter- and intra-specific Musa hybrids. BMC Genom 14:669–683

    Article  Google Scholar 

  • Douché T, San Clemente H, Burlat V, Roujol D, Valot B, Zivy M, Pont-Lezica R, Jamet E (2013) Brachypodium distachyon as a model plant toward improved biofuel crops: search for secreted proteins involved in biogenesis and disassembly of cell wall polymers. Proteomics 13(16):2438–2454

    Article  PubMed  Google Scholar 

  • Duressa D, Soliman K, Taylor R (2011) Proteomic analysis of soybean roots under aluminum stress. Int J Plant Genom 2011:282531

    Google Scholar 

  • Enio MSK, Shamshuddin J, Fauziah CI, Husni MHA (2011) Pyritization of the coastal sediments in the Kelantan Plains in the Malay Peninsula during the Holocene. Am J Agric Biol Sci 6(3):393–402

    Article  Google Scholar 

  • Garcia-Canas V, Simo C, Leon C, Ibanez E, Cifuentes A (2011) Ms-based analytical methodologies to characterize genetically modified crops. Mass Spec Rev 30:396–416

    Article  CAS  Google Scholar 

  • Ghosh JS, Chaudhuri S, Dey N, Pal A (2013) Functional characterization of a serine-threonine protein kinase from Bambusa balcooa that implicates in cellulose overproduction and superior quality fiber formation. BMC Plant Biol 13:1–17

    Article  Google Scholar 

  • Glick BR, Patten CL, Holguin G, Penrose DM (1999) Biochemical and genetic mechanisms used by plant growth promoting bacteria. Imperial College Press, London, pp 125–140

    Book  Google Scholar 

  • Gong CY, Wang T (2013) Proteomic evaluation of genetically modified crops: current status and challenges. Front Plant Sci 4:37–41

    Article  Google Scholar 

  • Hakeem KR, Chandna R, Ahmad A, Iqbal M (2012a) Proteomic analysis for low and high nitrogen-responsive proteins in the leaves of rice genotypes grown at three nitrogen levels. Appl Biochem Biotechnol 168:834–850

    Article  CAS  PubMed  Google Scholar 

  • Hakeem KR, Chandna R, Ahmad P, Ozturk M, Iqbal M (2012b) Relevance of proteomic investigations in plant stress physiology. OMICS: A J Integr Biol 16(11):621–635

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hakeem KR, Qureshi MI, Iqbal M, Mir BA (2013) Physiological studies and proteomic analysis for differentially expressed proteins and their possible role in the root of N-efficient rice (Oryza sativa L.). Mol Breed. doi:10.1007/s11032-013-9906-0

    Google Scholar 

  • Handakumbura PP, Matos DA, Osmont KS, Harrington MJ, Heo K, Kafle K, Kim SH, Baskin TI, Hazen SP (2013) Perturbation of Brachypodium distachyon CELLULOSE SYNTHASE A4 or 7 results in abnormal cell walls. BMC Plant Biol 13:122–131

    Article  Google Scholar 

  • Huang CF, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF (2009) A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 21:655–667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim ST, Kim SG, Hwang DH, Kang SY, Kim HJ, Lee BH, Lee JJ, Kang KY (2004) Proteomic analysis of pathogen-responsive proteins from rice leaves induced by rice blast fungus, Magna porthe grisea. Proteomics 4:3569–3578

    Article  CAS  PubMed  Google Scholar 

  • Kim SR, Yang JI, Moon S (2009) Anrice OGR1 encodes a pentatricopeptide repeat—DYW protein and is essential for RNA editing in mitochondria. Plant J 59:738–749

    Article  CAS  PubMed  Google Scholar 

  • Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Ann Rev Plant Physiol Plant Mol Biol 46:237–260

    Article  CAS  Google Scholar 

  • Kochian LV, Pinsferos MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195

    Article  CAS  Google Scholar 

  • Li JY, Liu J, Dong D, Jia X, McCouch SR, Kochian LV (2014) Natural variation underlies alterations in Nramp aluminum transporter (NRAT1) expression and function that play a key role in rice aluminum tolerance. Proc Natl Acad Sci 111(17):6503–6508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu HY, Dai JR, Feng DR, Liu B, Wang HB, Wang JF (2010) Characterization of a novel plantain Asr gene, MpAsr, that is regulated in response to infection of Fusarium oxysporum sp. cubense and abiotic stresses. J Integr Plant Biol 152:315–323

    Article  Google Scholar 

  • Lucy M, Reed E, Glick BR (2004) Applications of free living plant growth-promoting rhizobacterial. Antonie Van Leeuwenhoek 86(1):1–25

    Article  CAS  PubMed  Google Scholar 

  • Mahmoud A, Sukumar S, Krishnan HB (2007) Interspecific rice hybrid of Oryza sativa × Oryza nivara reveals a significant increase in seed protein content. J Agric Food Chem 56(2):476–482

    Article  PubMed  Google Scholar 

  • Muhrizal S, Shamshuddin J, Husni MHA, Fauziah I (2003) Alleviation of aluminum toxicity in acid sulfate soils in Malaysia using organic materials. Commun Soil Sci Plant Anal 34:2993–3012

    Article  CAS  Google Scholar 

  • Naher UA, Radziah O, Shamsuddin Zh, Halimi S (2009) Isolation of diazotrophs from different soils of TanjongKarang rice growing area in Malaysia. Int J Agric Biol 11(5):547–552

    CAS  Google Scholar 

  • Naher UA, Radziah O, Shamsuddin ZH, Halimi S (2011) Effect of root exuded specific sugars on biological nitrogen fixation and growth promotion in rice (Oryza sativa). Aust J Crop Sci 5(10):1210–1217

    CAS  Google Scholar 

  • Naher UA, Radziah O, Latif MA, Panhwar QA, Puteri AMA, Shamshuddin ZH (2013) Biomolecular characterization of diazotrophs isolated from the tropical soil in Malaysia. Int J Mol Sci 14:17812–17829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakkeeran S, Dilantha WG, Fernando WG (2005) Plant growth promoting Rhizobacteria formulations and its scope in commercialization for the management of pest and diseases. In: Siddiqui ZA (ed) PGPR: biocontrol and biofertilization. Springer, Dordrecht, pp 257–296

    Google Scholar 

  • Ngoc Son T, Diep CN, Giang TTM (2003) Effect of bradyrhizobia and phosphate solubilizing bacteria application on soybean in rotational system in the mekong delta. Omonrice 14:48–57

    Google Scholar 

  • Panda SK, Balusk F, Matsumoto H (2009) Aluminum stress signaling in plants. Plant Signal Behav 4(7):592–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Panhwar QA, Radziah O, Zaharah AR, Sariah M, Mohd Razi I, Naher UA (2011) Contribution of phosphate-solubilizing bacteria in phosphorus bioavailability and growth enhancement of aerobic rice. Span J Agric Res 9(3):810–820

    Article  Google Scholar 

  • Panhwar QA, Radziah O, Zaharah AR, Sariah M, Mohd Razi I (2012) Isolation and characterization of phosphorus solubilizing bacteria from aerobic rice. Afr J Biotechnol 11(11):2711–2719

    CAS  Google Scholar 

  • Panhwar QA, Shamshuddin J, Naher UA, Radziah O, Mohd Razi I (2014) Changes in the chemical properties of an acid sulfate soil and the growth of rice as affected by bio-fertilizer, ground magnesium limestone and basalt application. Pedosphere 24(6):827–835

    Article  Google Scholar 

  • Panhwar QA, Shamshuddin J, Naher UA, Radziah O, Mohd Razi I (2015) Eliminating aluminum toxicity in an acid sulfate soil for rice cultivation using plant growth promoting bacteria. Molecules 20:3628–3646

    Article  CAS  PubMed  Google Scholar 

  • Pappin DJ (1993) Rapid identification of proteins by peptide-mass finger printing. Curr Biol 3(6):327–332

    Article  CAS  PubMed  Google Scholar 

  • Peterson TA, Blackmer TM, Francis DD (1993) Using a chlorophyll meter to improve N management. Nebguide G93-1171A.Coop. Ext. Ser. University of Nebraska, Lincoln

    Google Scholar 

  • Plomion C, Lalanne C, Claverol S (2006) Mapping the proteome of poplar and application to the discovery of drought-stress responsive proteins. Proteomics 6:6509–6527

    Article  CAS  PubMed  Google Scholar 

  • Rengel Z (2006) Disturbance of cell Ca2+ homeostasis as a primary trigger of Al toxicity syndrome. Plant Cell Environ 15:931–938

    Article  Google Scholar 

  • Rengel Z, Elliott DC (1992) Mechanism of Al inhibition of net 43Ca2+ uptake by Amaranthus protoplasts. Plant Physiol 198:632–638

    Article  Google Scholar 

  • Rossignol M, Peltier JB, Mock HP, Matros A, Maldonado AM, Jorrin J (2006) Plant proteome analysis. Proteomics 6:5529–5548

    Article  CAS  PubMed  Google Scholar 

  • Ryan PR, Kochian LV (1993) Interaction between aluminum toxicity and calcium uptake at the root apex in near-isogenic lines of wheat (Triticum aestivum L.) differing in aluminum tolerance. Plant Physiol 102:975–982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salekdeh GH, Siopongco J, Wade LJ (2002) A proteomic approach to analyzing drought-and salt-responsive in rice. Field Crop Res 76:1999–2199

    Article  Google Scholar 

  • Sanchez PL, Wing RA, Brar DS (2013) The wild relative of rice: genomes and genomics. In: Zhang Q, Wing RA (eds) Genetics and genomics of rice. Plant genetics and genomics: crops and models, vol 5. Springer, New York, pp 9–25

  • Saveetha K (2009) Interactive genomics and proteomics of Plant Growth Promoting Rhizobacteria (PGPR) for the management of major pests and diseases in rice, Ph.D. Thesis. TNAU, Coimbatore, p 238

  • Shamshuddin J, Muhrizal S, Fauziah I, Husni MHA (2004) Effects of adding organic materials to an acid sulfate soil on growth of cocoa (Theobroma cacao L). Sci Total Environ 323(1–3):33–45

    Article  CAS  PubMed  Google Scholar 

  • Shamshuddin J, Elisa AA, Shazana MARS, Fauziah CI (2013) Rice defence mechanism system against excess amount of Al3+ and Fe2+ in the water. Aust J Crop Sci 7(3):314–320

    Google Scholar 

  • Shamshuddin J, Elisa Azura A, Shazana MARS, Fauziah CI, Panhwar QA, Naher UA (2014) Properties and management of acid sulfate soils in Southeast Asia for sustainable cultivation of rice, oil palm and cocoa. Adv Agron 124:91–142

    Article  CAS  Google Scholar 

  • Shazana MARS, Shamshuddin J, Fauziah CI, Syed Omar SR (2013) Alleviating the infertility of an acid sulphate soil using ground basalt with or without lime and organic fertilizer under submerged condition. Land Degrad Dev 24:129–140

    Article  Google Scholar 

  • Shoresh M, Harman GE (2008) Genome-wide identification, expression and chromosomal location of the genes encoding chitinolytic enzymes in Zea mays. Mol Genet Genom 147:2147–2163

    CAS  Google Scholar 

  • Silva S (2013) Aluminium toxicity targets in plants. J Bot. doi:10.1155/2012/219462

    Google Scholar 

  • Suswanto T, Shamshuddin J, Syed Omar SR, Mat Peli, Teh CBS (2007) Alleviating an acid sulfate soil cultivated to rice (Oryza sativa) using ground magnesium limestone and organic fertilizer. J Tanah Lingkungan 9(1):1–9

    Google Scholar 

  • Vaugha DA, Lu BR, Tomooka N (2008) The evolving story of rice evolution. Plant Sci 174:394–408

    Article  Google Scholar 

  • Xiong E, Wu X, Shi J (2013) Proteomic identification of differentially expressed proteins between male and female plants in Pistacia chinensis. PLoS One 8(5):e64276. doi:10.1371/journal.pone.0064276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Q, Wang Y, Zhang J, Shi W, Qian C, Peng X (2007) Identification of aluminum-responsive proteins in rice roots by a proteomic approach: cysteine synthase as a key player in Al response. Proteomics 7:737–749

    Article  CAS  PubMed  Google Scholar 

  • Yeh SH, Lin CS, Wu FH, Wang W (2013) Analysis of the expression of BohLOL1, which encodes an LSD1-like zinc finger protein in Bambusa oldhamii. Planta 234(6):1179–1189

    Article  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the technical support provided by Universiti Putra Malaysia and the Long Term Research Grant Scheme (LRGS) fund for Food Security by the Ministry of Higher Education Malaysia for providing the financial support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Radziah Othman.

Additional information

Communicated by Z.-L. Zhang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Panhwar, Q.A., Naher, U.A., Othman, R. et al. Aluminum toxicity-induced alterations in the leaf proteome of rice contrasting response towards inoculation of plant growth-promoting bacteria. Acta Physiol Plant 39, 214 (2017). https://doi.org/10.1007/s11738-017-2498-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-017-2498-2

Keywords