Skip to main content

Differential regulation of proteins in rice (Oryza sativa L.) under iron deficiency

Plant Cell Reports volume 34, pages 83–96 (2015)Cite this article

Abstract

Key message

Sixty-three proteins were identified to be differentially accumulated due to iron deficiency in shoot and root. The importance of these proteins alterations on shoot physiology is discussed.

Abstract

Iron (Fe) is an essential micronutrient for plant growth and its accumulation affects the quality of edible plant organs. To investigate the adaptive mechanism of a Chinese rice variety grown under iron deficiency, proteins differentially accumulated in leaves and roots of Yangdao 6, an indica cultivar, under Fe deficiency growth condition, were profiled using a two-dimensional electrophoresis (2-DE) and matrix-assisted laser desorption/ionization time of flight mass spectrometry (MALDI-TOF/MS). The accumulations of seventy-three proteins were detected to be increased or decreased upon iron deficiency, and sixty-three of them were successfully identified. Among the sixty-three proteins, a total of forty proteins were identified in rice leaves, and twenty-three proteins were in roots. Most of these proteins are involved in photosynthesis, C metabolism, oxidative stress, Adenosine triphosphate synthesis, cell growth or signal transduction. The results provide a comprehensive way to understand, at the level of proteins, the adaptive mechanism used by rice shoots and roots under iron deficiency.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Article  Google Scholar 

  • Andersen GR, Nissen P, Nyborg J (2003) Elongation factors in protein biosynthesis. Trends Biochem Sci 28:434–441

    CAS  PubMed  Article  Google Scholar 

  • Cakmak I, Kirkby EA (2008) Role of magnesium in carbon partitioning and alleviating photooxidative damage. Physiol Plant 133:692–704

    CAS  PubMed  Article  Google Scholar 

  • Calvo JM, Matthews RG (1994) The leucine-responsive regulatory protein, a global regulator of metabolism in Escherichia coli. Microbiol Rev 58:466–490

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chatelain E, Hundertmark M, Leprince O, Le Gall S, Satour P, Deligny-Penninck S, Rogniaux H, Buitink J (2012) Temporal profiling of the heat-stable proteome during late maturation of Medicago truncatula seeds identifies a restricted subset of late embryogenesis abundant proteins associated with longevity. Plant Cell Environment 35:1440–1455

    CAS  Article  Google Scholar 

  • Chen Y, Barak P (1982) Iron nutrition of plants in calcareous soils. In: Brady NC (ed) Advance in agronomy. Rehovot, Israel, pp 217–240

    Google Scholar 

  • Ciereszko I, Zambrzycka A, Rychter A (1998) Sucrose hydrolysis in bean roots (Phaseolus vulgaris L.) under phosphate deficiency. Plant Sci 133:139–144

    CAS  Article  Google Scholar 

  • Colangelo EP, Guerinot ML (2004) The essential bHLH protein FIT1 is required for the iron deficiency response. Plant Cell 16:3400–3412

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Cordin O, Banroques J, Tanner NK, Linder P (2006) The DEAD-box protein family of RNA helicases. Gene 367:17–37

    CAS  PubMed  Article  Google Scholar 

  • Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409:346–349

    CAS  PubMed  Article  Google Scholar 

  • Curie C, Cassin G, Counch D, Divol F, Higuchi K, Jean ML, Misson J, Schikora A, Czernic P, Mari S (2009) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann Bot 103:1–11

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • DeLong A, Calderon-Urrea A, Dellaporta SL (1993) Sex determination gene TASSELSEED2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell 74:757–768

    CAS  PubMed  Article  Google Scholar 

  • Ding CQ, You J, Liu ZH, Rehmani MIA, Wang SH, Li GH, Wang QS, Ding YF (2011) Proteomic analysis of low nitrogen stress-responsive proteins in roots of rice. Plant Mol Biol Rep 29:618–625

    CAS  Article  Google Scholar 

  • Dinneny JR, Long TA, Wang JY, Jung JW, Mace D, Pointer S, Barron C, Brady SM, Schiefelbein J, Benfey PN (2008) Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320:942–945

    CAS  PubMed  Article  Google Scholar 

  • Fu HY, Doelling JH, Rubin DM, Vierstra RD (1999) Structural and functional analysis of the six regulatory particle triple-A ATPase subunits from the Arabidopsis 26S proteasome. Plant J 18:529–539

    CAS  PubMed  Article  Google Scholar 

  • Guo D, Chen F, Inoue K, Blount JW, Dixon RA (2001) Downregulation of caffeic acid 3-O-methyltransferase and caffeoyl CoA 3-O-methyltransferase in transgenic alfalfa. impacts on lignin structure and implications for the biosynthesis of G and S lignin. Plant Cell 13:73–88

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Haydon MJ, Cobbett CS (2007) Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506

    CAS  PubMed  Article  Google Scholar 

  • Hopff D, Wienkoop S, Lüthje S (2013) The plasma membrane proteome of maize roots grown under low and high iron conditions. J Proteomics. doi:10.1016/j.jprot.2013.01.006

    PubMed  Google Scholar 

  • Hubbard MJ, Cohen P (1993) On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem Sci 18:172–177

    CAS  PubMed  Article  Google Scholar 

  • Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y, Suzuki K, Nakazono M, Nakanishi H, Mori S, Nishizawa NK (2009) Rice OsYSL15 is an Fe-regulated Fe(III)-deoxymugineic acid transporter expressed in the roots and is essential for Fe uptake in early growth of the seedlings. J Biol Chem 284:3470–3479

    CAS  PubMed  Article  Google Scholar 

  • Ishimaru Y, Suzuki M, Tsukamoto T, Suzuki K, Nakazono M, Kobayashi T, Wada Y, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2006) Rice plants take up Fe as an Fe3+-phytosiderophore and as Fe2+. Plant J 45:335–346

    CAS  PubMed  Article  Google Scholar 

  • Itai R, Suzuki K, Yamaguchi H, Nakanishi H, Nishizawa NK, Yoshimura E, Mori S (2000) Induced activity of adenine phosphoribosyltransferase (APRT) in iron-deficient barley roots: a possible role for phytosiderophore production. J Exp Bot 51:1179–1188

    CAS  PubMed  Article  Google Scholar 

  • Kiddle G, Pastori GM, Bernard S, Pignocchi C, Antoniw J, Verrier PJ, Foyer CH (2003) Effects of leaf ascorbate content on defense and photosynthesis gene expression in Arabidopsis thaliana. Antioxid Redox Signal 5:23–32

    CAS  PubMed  Article  Google Scholar 

  • Kohlhaw GB (2003) Leucine biosynthesis in fungi: entering metabolism through the back door. Microbiol Mol Biol Rev 67:1–15

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Kruger C, Berkowitz O, Stephan UW, Hell R (2002) A metal-binding member of the late embryogenesis abundant protein family transports iron in the phloem of Ricinus communis L. J Biol Chem 227:25062–25069

    Article  Google Scholar 

  • Li L, Kaplan J (2004) A mitochondrial vacuolar signaling pathway in yeast that affects iron and copper metabolism. J Biol Chem 279:33653–33661

    CAS  PubMed  Article  Google Scholar 

  • Li J, Wu XD, Hao ST, Wang XJ, Ling HQ (2008) Proteomic response to iron deficiency in tomato root. Proteomics 8:2299–2311

    CAS  PubMed  Article  Google Scholar 

  • Ling HQ, Pich A, Scholz G, Ganal MW (1996) Genetic analysis of two tomato mutants affected in the regulation of iron metabolism. Mol Gen Genet 252:87–92

    CAS  PubMed  Article  Google Scholar 

  • Ling HQ, Koch G, Baumlein H, Ganal MW (1999) Map-based cloning of chloronerva, a gene involved in iron uptake of higher plants encoding nicotianamine synthase. Proc Natl Acad Sci 96:7098–7103

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Ling HQ, Bauer P, Bereczky Z, Keller B, Ganal M (2002) The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots. Proc Natl Acad Sci 99:13938–13943

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • López-Millán AF, Morales F, Andaluz S, Gogorcena Y, Abadía A, De Rivas Las J, Abadía J (2000) Responses of sugar beet roots to iron deficiency. Changes in carbon assimilation and oxygen use. Plant Physiol 124:885–897

    PubMed Central  PubMed  Article  Google Scholar 

  • López-Millán AF, Morales F, Gogorcena Y, Abadía A, Abadía J (2009) Metabolic responses in iron deficient tomato plants. J Plant Physiol 166:375–384

    PubMed  Article  Google Scholar 

  • López-Millán AF, Grusak MA, Abadía A, Abadía J (2013) Iron deficiency in plants: an insight from proteomic approaches. Front Plant Sci 4:254

    PubMed Central  PubMed  Article  Google Scholar 

  • Mochizuki N, Tanaka R, Grimm B, Moulin M, Masuda T, Smith AG, Tanaka A, Terry MJ (2010) The cell biology of tetrapyrroles: a life and death struggle. Trends Plant Sci 15:488–498

    CAS  PubMed  Article  Google Scholar 

  • Mol PC, Park HM, Mullins JT, Cabib E (1994) A GTP-binding protein regulates the activity of (1→3)-beta-glucan synthase, an enzyme directly involved in yeast cell wall morphogenesis. J Biol Chem 269:31267–31274

    CAS  PubMed  Google Scholar 

  • Mowla SB, Cuypers A, Driscoll SP, Kiddle G, Thomson J, Foyer CH, Theodoulou FL (2006) Yeast complementation reveals a role for an Arabidopsis thaliana late embryogenesis abundant (LEA)-like protein in oxidative stress tolerance. Plant J 48:743–756

    CAS  PubMed  Article  Google Scholar 

  • Mumby MC, Walter G (1993) Protein serine/threonine phosphatases: structure, regulation, and functions in cell growth. Physiol Rev 73:673–699

    CAS  PubMed  Google Scholar 

  • Nelson DL, Cox MM (2000) Lehninger. Principles of Biochemistry, New York

    Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    CAS  PubMed  Article  Google Scholar 

  • Ouyang JP, Guo WB, Li B, Gu L, Zhang HJ, Chen XH (2013) Proteomic analysis of differential protein expression in Acidithiobacillus ferrooxidans cultivated in high potassium concentration. Microbiol Res 168:455–460

    CAS  PubMed  Article  Google Scholar 

  • Santi S, Schmidt W (2008) Laser microdissection-assisted analysis of the functional fate of iron deficiency-induced root hairs in cucumber. J Exp Bot 59:697–704

    CAS  PubMed  Article  Google Scholar 

  • Schmidt W (2003) Fe solutions: acquisition strategies and signaling pathway in plants. Trends Plant Sci 8:188–193

    CAS  PubMed  Article  Google Scholar 

  • Schönthal AH (1998) Role of PP2A in intracellular signal transduction pathways. Front Biosci 3:1262–1273

    Google Scholar 

  • Severance S, Hamza I (2009) Trafficking of heme and porphyrins in metazoa. Chem Rev 109:4596–4616

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozak K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    CAS  PubMed  Article  Google Scholar 

  • Suyal DC, Yadav A, Shouche Y, Goel R (2014) Differential proteomics in response to low temperature diazotrophy of Himalayan psychrophilic nitrogen fixing Pseudomonas migulae S10724 strain. Curr Microbiol 68:543–550

    CAS  PubMed  Article  Google Scholar 

  • Takahashi M, Terada Y, Nakai I, Nakanishi H, Yoshimura E, Mori S, Nishizawa NK (2003) Role of nicotianamine in the intracellular delivery of metals and plant reproductive development. Plant Cell 15:1263–1280

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Thimm O, Essigmann B, Kloska S, Altmann T, Buckhout TJ (2001) Response of Arabidopsis to iron deficiency stress as revealed by microarray analysis. Plant Physiol 127:1030–1043

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Virshup DM, Cegielska A, Russo A, Kelly TJ, Shaffer S (1993) The initiation of SV40 DNA replication is controlled by a phosphorylation-dephosphorylation cycle. Adv Protein Phosphatases 7:271–293

    CAS  Google Scholar 

  • Warren CR, Livingston NJ, Turpin DH (2004) Photosynthetic responses and N allocation in Douglas-fir needles following a brief pulse of nutrients. Tree Physiol 24:601–608

    CAS  PubMed  Article  Google Scholar 

  • Wasaki J, Yonetani R, Kuroda S, Shinano T, Yazaki J et al (2003) Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant Cell Environ 26:1515–1523

    CAS  Article  Google Scholar 

  • Watson GMF, Tabita FR (1997) Microbial ribulose 1, 5-bisphosphate carboxylase/oxygenase: a molecule for phylogenetic and enzymological investigation. FEMS Microbiol Lett 146:13–22

    CAS  PubMed  Article  Google Scholar 

  • Whiteheart SW, Rossnagel K, Buhrow SA, Brunner M, Jaenicke R, Rothman JE (1994) N-ethylmaleimide-sensitive fusion protein: a trimeric ATPase whose hydrolysis of ATP is required for membrane fusion. J Cell Biol 126:945–954

    CAS  PubMed  Article  Google Scholar 

  • Winder TL, Nishio JN (1995) Early iron deficiency stress response in leaves of sugar beet. Plant Physiol 108:1487–1494

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Witmer X, Nonogaki H, Beers EP, Bradford KJ, Welbaum GE (2003) Characterization of chitinase activity and gene expression in muskmelon seeds. Seed Science Research 13:167–178

    CAS  Article  Google Scholar 

  • Xu CP, Huang BR (2008) Root proteomic responses to heat stress in two Agrostis grass species contrasting in heat tolerance. J Exp Bot 59:4183–4194

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Xu WF, Shi WM (2006) Expression Profiling of the 14-3-3 gene family in response to salt stress and potassium and iron Deficiencies in young tomato (Solanum lycopersicum) roots: analysis by real-time RT-PCR. Ann Bot 98:965–974

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Yan JX, Wait R, Berkelman T, Harry RA, Westbrook JA, Wheeler CH, Dunn MJ (2000) A modified silver staining protocol for visualization of proteins compatible with matrix-assisted laser desorption/ionization and electrospray ionization-mass spectrometry. Electrophoresis 21:3666–3672

    CAS  PubMed  Article  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice. Los Baños

  • Zaharieva TB, Abadia J (2003) Iron deficiency enhances the levels of ascorbate, glutathione, and related enzymes in sugar beet roots. Protoplasma 221:269–275

    CAS  PubMed  Google Scholar 

  • Zhao XF, Ding CQ, Chen L, Wang SH, Wang QS, Ding YF (2012) Comparative proteomic analysis of the effects of nitric oxide on alleviating Cd-induced toxicity in rice (Oryza sativa L.). Plant Omics J 5:604–614

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Ministry of National Science and Technology of China (Project No. 2012BAD04B00) and the Science and Technology Department of Henan Province (Project No. 2013BAD07B00). We thank Professor Andre Jagendorf for the language editing.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Affiliations

  1. Key Laboratory of Crop Physiology and Ecology in Southern China, College of Agriculture, Ministry of Agricultural University, Nanjing Agricultural University, Nanjing, China

    Lin Chen, Chengqiang Ding, Junxu Xu, Shaohua Wang & Yanfeng Ding

  2. Institute of Agricultural Environment and Resource, Shanxi Academy of Agricultural Science, Taiyuan, China

    Xiufeng Zhao

  3. Department of Agronomy and Agricultural Extension, University of Rajshahi, Rajshahi, Bangladesh

    Alim Abdul Mohammad

Authors
  1. Lin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chengqiang Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiufeng Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Junxu Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alim Abdul Mohammad
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shaohua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yanfeng Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yanfeng Ding.

Additional information

Communicated by Wendy Harwood.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Chen, L., Ding, C., Zhao, X. et al. Differential regulation of proteins in rice (Oryza sativa L.) under iron deficiency. Plant Cell Rep 34, 83–96 (2015). https://doi.org/10.1007/s00299-014-1689-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-014-1689-1

Keywords

  • Iron deficiency
  • Proteomics
  • Rice (Oryza sativa L.)
  • Leaf
  • Root
  • Two-dimensional gel electrophoresis