Skip to main content

Advertisement

Log in

Quantitative proteomics to study the response of wheat to contrasting fertilisation regimes

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Negative environmental impacts from mineral fertilisers and pesticides used in conventional cropping have raised concern over the sustainability of arable crop production. Organic cropping uses alternatives that avoid many of these negative environmental effects; however, crop yields can be significantly reduced, possibly due to a lower proportion of plant-available nutrients. To gain insights into the molecular effects of organic compared to conventional cropping systems on plant utilisation of nutrients, we used proteomics to analyse winter wheat (Triticum aestivum). Our aim was to investigate the effects of contrasting fertility management and crop protection regimes in organic and conventional cropping systems on the wheat flag leaf proteome and the association between the proteome and physiological traits. Wheat flag leaves were flash-frozen, lyophilised and milled prior to protein extraction (TCA/acetone) and analysed using 2D gel electrophoresis and MALDI-TOF MS. The abundance of 111 protein spots varied significantly between fertilisation regimes. Flag leaf N and P composition were significant drivers of differences in protein spot abundance, including major proteins involved in nitrogen remobilisation, photosynthesis, metabolism and stress response. These results indicate that molecular-based mechanisms are involved in the effect of contrasting cropping systems on nutrient utilisation and wheat grain yield. Using a functional genomics approach, we were able to identify proteins that are linked to causal genes, enabling the potential development of functional molecular markers for crop improvement in nutrient use efficiency.

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

Access this article

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

Similar content being viewed by others

References

  • Barraclough PB, Howarth JR, Jones J, Lopez-Bellido R, Parmar S, Shepherd CE, Hawkesford MJ (2010) Nitrogen efficiency of wheat: genotypic and environmental variation and prospects for improvement. Eur J Agron 33(1):1–11. doi:10.1016/j.eja.2010.01.005

    Article  CAS  Google Scholar 

  • Bernard SM, Moller ALB, Dionisio G, Kichey T, Jahn TP, Dubois F, Baudo M, Lopes MS, Terce-Laforgue T, Foyer CH, Parry MAJ, Forde BG, Araus JL, Hirel B, Schjoerring JK, Habash DZ (2008) Gene expression, cellular localisation and function of glutamine synthetase isozymes in wheat (Triticum aestivum L.). Plant Mol Biol 67(12):89–105. doi:10.1007/s11103-008-9303-y

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Gallie DR (2008) Dehydroascorbate reductase affects non-photochemical quenching and photosynthetic performance. J Biol Chem 283(31):21347–21361. doi:10.1074/jbc.M802601200

    Article  PubMed  CAS  Google Scholar 

  • Chiba A, Ishida H, Nishizawa NK, Makino A, Mae T (2003) Exclusion of ribulose-1,5-bisphosphate carboxylase/oxygenase from chloroplasts by specific bodies in naturally senescing leaves of wheat. Plant Cell Physiol 44(9):914–921

    Article  PubMed  CAS  Google Scholar 

  • Cooper J, Sanderson R, Cakmak I, Ozturk L, Shotton P, Carmichael A, Haghighi RS, Tétard-Jones C, Volakakis N, Eyre M, Leifert C (2011) Effect of organic and conventional crop rotation, fertilization, and crop protection practices on metal contents in wheat (Triticum aestivum). J Agric Food Chem 59(9):4715–4724. doi:10.1021/jf104389m

    Article  PubMed  CAS  Google Scholar 

  • Cordell D, Dangert J-O, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Chang 19:292–305

    Article  Google Scholar 

  • Crafts-Brandner SJ, Hölzer R, Feller U (1998) Influence of nitrogen deficiency on senescence and the amounts of RNA and proteins in wheat leaves. Physiol Plant 102(2):192–200. doi:10.1034/j.1399-3054.1998.1020206.x

    Article  CAS  Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, Chichester

    Book  Google Scholar 

  • Dawson JC, Huggins DR, Jones SS (2008) Characterizing nitrogen use efficiency in natural and agricultural ecosystems to improve the performance of cereal crops in low-input and organic agricultural systems. Field Crops Res 107(2):89–101

    Article  Google Scholar 

  • Donnelly BE, Madden RD, Ayoubi P, Porter DR, Dillwith JW (2005) The wheat (Triticum aestivium L.) leaf proteome. Proteomics 5(6):1624–1633

    Article  PubMed  CAS  Google Scholar 

  • EFMA (2007) Forecast of food, farming and fertiliser use in the European Union 2007–2017

  • Eyre MD, Sanderson RA, Shotton PN, Leifert C (2009) Investigating the effects of crop type, fertility management and crop protection on the activity of beneficial invertebrates in an extensive farm management comparison trial. Ann Appl Biol 155:267–276

    Article  Google Scholar 

  • Fantel RJ, Peterson GR, Stowasser WF (1985) The worldwide availability of phosphate rock. NatResour Forum 9:5–24

    Google Scholar 

  • Ferry N, Stavroulakis S, Guan W, Davison GM, Bell HA, Weaver RJ, Down RE, Gatehouse JA, Gatehouse AMR (2011) Molecular interactions between wheat and cereal aphid (Sitobion avenae); analysis of changes to the wheat proteome. Proteomics 11:1985–2002

    Article  PubMed  CAS  Google Scholar 

  • Fontaine JX, Ravel C, Pageau K, Heumez E, Dubois F, Hirel B, Le Gouis J (2009) A quantitative genetic study for elucidating the contribution of glutamine synthetase, glutamate dehydrogenase and other nitrogen-related physiological traits to the agronomic performance of common wheat. Theor Appl Genet 119(4):645–662. doi:10.1007/s00122-009-1076-4

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Ferris C, Moreno J (1994) Oxidative modification and breakdown of ribulose-1,5-bisphosphate carboxylase induced in Euglena gracilis by nitrogen starvation. Planta 193(2):208–215

    Article  CAS  Google Scholar 

  • Hepperly P, Lotter D, Ziegler C, Seidel R, Reider C (2009) Compost, manure and synthetic fertilizer influences crop yields, soil properties, nitrate leaching and crop nutrient content. Compost Sci Util 17:117–126

    CAS  Google Scholar 

  • Herencia JF, Ruiz-Porras JC, Melero S, Garcia-Galavis PA, Morillo E, Maqueda C (2007) Comparison between organic and mineral fertilization for soil fertility levels, crop macronutrient concentrations, and yield. Agron J 99:973–983

    Article  CAS  Google Scholar 

  • Howarth JR, Parmar S, Jones J, Shepherd CE, Corol DI, Galster AM, Hawkins ND, Miller SJ, Baker JM, Verrier PJ, Ward JL, Beale MH, Barraclough PB, Hawkesford MJ (2008) Co-ordinated expression of amino acid metabolism in response to N and S deficiency during wheat grain filling. J Exp Bot 59(13):3675–3689. doi:10.1093/jxb/ern218

    Article  PubMed  CAS  Google Scholar 

  • Irving LJ, Robinson D (2006) A dynamic model of Rubisco turnover in cereal leaves. New Phytol 169(3):493–504

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kant S, Bi Y-M, Rothstein SJ (2011) Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. J Exp Bot 62(4):1499–1509. doi:10.1093/jxb/erq297

    Article  PubMed  CAS  Google Scholar 

  • Le Gouis J, Béghin D, Heumez E, Pluchard P (2000) Genetic differences for nitrogen uptake and nitrogen utilisation efficiencies in winter wheat. Eur J Agron 12:163–173

    Article  Google Scholar 

  • Lehesranta SJ, Koistinen KM, Massat N, Davies HV, Shepherd LVT, McNicol JW, Cakmak I, Cooper J, Luck L, Karenlampi SO, Leifert C (2007) Effects of agricultural production systems and their components on protein profiles of potato tubers. Proteomics 7(4):597–604. doi:10.1002/pmic.200600889

    Article  PubMed  CAS  Google Scholar 

  • Lombard K, O’Neill M, Mexal J, Ulery A, Onken B, Bettmann G, Heyduck R (2010) Can soil plant analysis development values predict chlorophyll and total Fe in hybrid poplar? Agrofor Syst 78:1–11

    Article  Google Scholar 

  • Lu C, Hawkesford MJ, Barraclough PB, Poulton PR, Wilson ID, Barker GL, Edwards KJ (2005) Markedly different gene expression in wheat grown with organic or inorganic fertilizer. Proc R Soc B Biol Sci 272(1575):1901–1908. doi:10.1098/rspb.2005.3161

    Article  CAS  Google Scholar 

  • Mäder P, Fliessbach A, Dubois D, Gunst L, Fried P, Niggli U (2002) Soil fertility and biodiversity in organic farming. Science 296(5573):1694–1697

    Article  PubMed  Google Scholar 

  • Mae T (2004) Leaf senescence and nitrogen metabolism. In: Nooden LD (ed) Plant cell death processes. Academic Press, San Diego, pp 157–168

    Chapter  Google Scholar 

  • Mae T, Makino A, Ohira K (1983) Changes in the amounts of ribulose bisphosphate carboxylase synthesized and degraded during the life span of rice leaf (Oryza sativa L.). Plant Cell Physiol 24(6):1079–1086

    CAS  Google Scholar 

  • Martínez DE, Costa ML, Guiamet JJ (2008) Senescence-associated degradation of chloroplast proteins inside and outside the organelle. Plant Biol 10(Suppl s1):15–22

    Article  PubMed  Google Scholar 

  • Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L, Suzuki A (2010) Nitogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Ann Bot 105:1141–1157

    Article  PubMed  Google Scholar 

  • Moreno JI, Martin R, Castresana C (2005) Arabidopsis SHMT1, a serine hydroxymethyltransferase that functions in the photorespiratory pathway influences resistance to biotic and abiotic stress. Plant J 41(3):451–463. doi:10.1111/j.1365-313X.2004.02311.x

    Article  PubMed  CAS  Google Scholar 

  • Nawrocki A, Thorup-Kristensen K, Jensen ON (2011) Quantitative proteomics by 2DE and MALDI MS/MS uncover the effects of organic and conventional cropping methods on vegetable products. J Proteomics 74(12):2810–2825. doi:10.1016/j.jprot.2011.06.021

    Article  PubMed  CAS  Google Scholar 

  • Orr CH, James A, Leifert C, Cooper JM, Cummings SP (2011) Diversity and activity of free-living nitrogen-fixing bacteria and total bacteria in organic and conventionally managed soils. Appl Environ Microbiol 77:911–919

    Article  PubMed  CAS  Google Scholar 

  • Osaki M, Shinano T, Tadano T (1993) Effect of nitrogen, phosphorus, or potassium deficiency on the accumulation of ribulose-1,5-bisphosphate carboxylase/oxygenase and chlorophyll in several field crops. Soil Sci Plant Nutr 39:417–425

    Article  CAS  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York

    Book  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • QLIF (2009) www.QLIF.org

  • RDC Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Robertson GP, Vitousek PM (2009) Nitrogen in agriculture: balancing the cost of an essential resource. Annu Rev Environ Resour 34:97–125

    Article  Google Scholar 

  • Schneider G, Lindqvist Y, Branden CI (1992) Rubisco: structure and mechanism. Annu Rev Biophys Biomol Struct 21(1):119–143. doi:10.1146/annurev.bb.21.060192.001003

    Article  PubMed  CAS  Google Scholar 

  • Siedow JN (1991) Plant lipoxygenase: structure and function. Annu Rev Plant Physiol Plant Mol Biol 42:145–188

    Article  CAS  Google Scholar 

  • Suzuki Y, Makino A, Mae T (2001) Changes in the turnover of Rubisco and levels of mRNAs of rbcL and rbcS in rice leaves from emergence to senescence. Plant, Cell Environ 24(12):1353–1360

    Article  CAS  Google Scholar 

  • Ter Braak CJF, Šmilauer P (1998) CANOCO reference manual and user’s guide to Canoco for Windows: Software for Canonical Community Ordination. Version 4 edn. Centre for Biometry, Wageningen

    Google Scholar 

  • The Council of the European Communities (1991) Council Directive 91/676/EEC of 12 December 1991 concerning the protection of waters against pollution caused by nitrates from agricultural sources. vol 91/676/EEC 375 edn. Official Journal of the European Union L 375

  • Thoenen M, Herrmann B, Feller U (2007) Senescence in wheat leaves: is a cysteine endopeptidase involved in the degradation of the large subunit of Rubisco? Acta Physiologiae Plant 29(4):339–350. doi:10.1007/s11738-007-0043-4

    Article  CAS  Google Scholar 

  • Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677

    Article  PubMed  CAS  Google Scholar 

  • Trehan SP, Sharma RC (2005) Differences in phosphorus use efficiency in potato genotypes. Adv Hort Sci 19:13–20

    Google Scholar 

  • Uddling J, Gelang-Alfredsson J, Piikki K, Pleijel H (2007) Evaluating the relationship between leaf chlorophyll concentration and SPAD-502 chlorophyll meter readings. Photosynth Res 91(1):37–46. doi:10.1007/s11120-006-9077-5

    Article  PubMed  CAS  Google Scholar 

  • Varshney RK, Graner A, Sorrells ME (2005) Genomics-assisted breeding for crop improvement. Trends Plant Sci 10(12):621–630. doi:10.1016/j.tplants.2005.10.004

    Article  PubMed  CAS  Google Scholar 

  • Warman PR, Burnham JC, Eaton LJ (2009) Effects of repeated applications of municipal solid waste compost and fertilizers to three lowbush blueberry fields. Sci Hort 122:393–398

    Article  CAS  Google Scholar 

  • Warren CR, Adams MA (2002) Phosphorus affects growth and partitioning of nitrogen to Rubisco in Pinus pinaster. Tree Physiol 22(1):11–19

    Article  PubMed  CAS  Google Scholar 

  • Zadoks JC, Chang TT, Konzak CF (1974) Decimal code for growth stages of cereals. Weed Res 14(6):415–421

    Article  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge funding from the European Community financial participation under the Seventh Framework Program for Research, Technological Development and Demonstration Activities, for the Integrated Project NUE-CROPS FP7-CP-IP 222645.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Angharad M. R. Gatehouse.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 104 kb)

11032_2012_9796_MOESM2_ESM.tif

Online Resource 4: Values for ANOVA for grain yield across contrasting fertilisation and crop management regimes. Letters above the columns refer to Tukey test for significant differences between means (p < 0.05). (TIFF 995 kb)

11032_2012_9796_MOESM3_ESM.tif

Online Resource 8: Image of the DIGE reference gel (pH3–10 non-linear). The red arrows point to RuBisCo and glutamine synthetase protein spots that were up-regulated in flag leaves of compost- and mineral- (bold) fertilised wheat. The numbers on the right indicate the molecular mass. (TIFF 6616 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tétard-Jones, C., Shotton, P.N., Rempelos, L. et al. Quantitative proteomics to study the response of wheat to contrasting fertilisation regimes. Mol Breeding 31, 379–393 (2013). https://doi.org/10.1007/s11032-012-9796-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11032-012-9796-6

Keywords

Navigation