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Using metabolic profiling to assess plant-pathogen interactions: an example using rice (Oryza sativa) and the blast pathogen Magnaporthe grisea

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Abstract

A metabolomics based approach has been used to study the infection of the Hwacheong rice cultivar (Oryza sativa L. cv. Hwacheong) with compatible (KJ201) and incompatible (KJ401) strains of the rice blast fungal pathogen Magnaporthe grisea. The metabolic response of the rice plants to each strain was assessed 0, 6, 12, 24, 36, and 48 h post inoculation. Nuclear Magnetic Resonance (NMR) spectroscopy and Gas and Liquid Chromatography Tandem Mass spectrometry (GC/LC-MS/MS) were used to study both aqueous and organic phase metabolites, collectively resulting in the identification of 93 compounds. Clear metabolic profiles were observed at each time point but there were no significant differences in the metabolic response elicited by each pathogen strain until 24 h post inoculation. The largest change was found to be in alanine, which was ~30% (±9%) higher in the leaves from the compatible, compared to the resistant, plants. Together with several other metabolites (malate, glutamine, proline, cinnamate and an unknown sugar) alanine exhibited a good correlation between time of fungal penetration into the leaf and the divergence of metabolite profiles in each interaction. The results indicate both that a wide range of metabolites can be identified in rice leaves and that metabolomics has potential for the study of biochemical changes in plant-pathogen interactions.

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References

  • Allan, A. C., Lapidot, M., Culver, J. N., & Fluhr, R. (2001). An early tobacco mosaic virus-induced oxidative burst in tobacco indicates extracellular perception of the virus coat protein. Plant Physiology, 126, 97–108.

    Article  PubMed  CAS  Google Scholar 

  • Allwood, J. W., Ellis, D. I., & Goodacre, R. (2008). Metabolomic technologies and their application to the study of plants and plant-host interactions. Physologia Plantarum, 132, 117–135.

    CAS  Google Scholar 

  • Allwood, J. W., Ellis, D. I., Heald, J. K., Goodacre, R., & Mur, L. A. J. (2006). Metabolomic approaches reveal that phosphatidic and phosphatidyl glycerol phospholipids are major discriminatory non-polar metabolites in responses by Brachypodium distachyon to challenge by Magnaporthe grisea. The Plant Journal, 46, 351–368.

    Article  PubMed  CAS  Google Scholar 

  • Antti, H., Bollard, M. E., Ebbels, T., Keun, H., Lindon, J. C., Nicholson, J. K., et al. (2002). Batch statistical processing of 1H NMR-derived urinary spectral data. Journal of Chemometrics, 16, 461–468.

    Article  CAS  Google Scholar 

  • Bechinger, C., Giebel, K.-F., Schnell, M., Leiderer, P., Deising, H. B., & Bastmeyer, M. (1999). Optical measurements of invasive forces exerted by appressoria of a plant pathogenic fungus. Science, 285, 1896–1899.

    Article  PubMed  CAS  Google Scholar 

  • Bölling, C., & Fiehn, O. (2005). Metabolite profiling of Chlamydomonas reinhardtii under nutrient deprivation. Plant Physiology, 139, 1995–2005.

    Article  PubMed  Google Scholar 

  • Chen, J., Hall, D. E., Murata, J., & De Luca, V. (2006). l-Alanine induces programmed cell death in V. labrusca cell suspension cultures. Plant Science, 171, 734–744.

    Article  CAS  Google Scholar 

  • Cloarec, O., Dumas, M.-E., Craig, A., Barton, R. H., Trygg, J., Hudson, J., et al. (2005). Statistical total correlation spectroscopy: An exploratory approach for latent biomarker identification from metabolic 1H NMR data sets. Analytical Chemistry, 77, 1282–1289.

    Article  PubMed  CAS  Google Scholar 

  • Dean, R. A., Talbot, N. J., Ebbole, D. J., Farman, M. L., Mitchell, T. K., Orbach, M. J., et al. (2005). The genome sequence of the rice blast fungus Magnaporthe grisea. Nature, 434, 980–986.

    Article  PubMed  CAS  Google Scholar 

  • Del Pozo, O., Pedley, K. F., & Martin, G. B. (2004). MAPKKK alpha is a positive regulator of cell death associated with both plant immunity and disease. EMBO Journal, 23, 3072–3082.

    Article  PubMed  Google Scholar 

  • Eriksson, L., Johansson, E., Kettaneh-Wold, N., & Wold, S. (2001). Multi- and megavariate data analysis: principles and applications. Umeå, Sweden: Umetrics.

    Google Scholar 

  • Fiehn, O. (2002). Metabolomics -- the link between genotypes and phenotypes. Plant Molecular Biology, 48(1), 155–171.

    Google Scholar 

  • Goff, S. A., Ricke, D., Lan, T.-H., Presting, G., Wang, R., Dunn, M., et al. (2002). A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science, 92, 100.

    Google Scholar 

  • Govrin, E. M., & Levine, A. (2000). The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Current Biology, 10, 751–757.

    Article  PubMed  CAS  Google Scholar 

  • Griffin, J. L., & Shore, R. F. (2007). Applications of metabonomics within environmental toxicology. In J. C. Lindon, J. K. Nicholson, & E. Holmes (Eds.), The Handbook of Metabonomics and Metabolomics (pp. 517–532). Kidlington: Elsevier Press.

    Chapter  Google Scholar 

  • Gullberg, J., Jonsson, P., Nordstrom, A., Sjostrom, M., & Moritz, T. (2004). Design of experiments: an efficient strategy to identify factors influencing extraction and derivatization of Arabidopsis thaliana samples in metabolomic studies with gas chromatography/mass spectrometry. Analytical Biochemistry, 331, 283–295.

    Article  PubMed  CAS  Google Scholar 

  • Le Belle, J., Harris, N., Williams, S., & Bhakoo, K. (2002). A comparison of cell and tissue extraction techniques using high-resolution 1H-NMR spectroscopy. NMR in Biomedicine, 15, 37–44.

    Article  PubMed  Google Scholar 

  • Lin, C. U., Wu, H., Tjeerdema, R. S., & Viant, M. R. (2007). Evaluation of metabolite extraction strategies from tissue samples using NMR metabolomics. Metabolomics, 3, 55–67.

    Article  CAS  Google Scholar 

  • Morrison, W. R., & Smith, L. M. (1964). Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoride-methanol. Journal of Lipid Research, 5, 600–608.

    PubMed  CAS  Google Scholar 

  • Park, J.-Y., Jin, J., Lee, Y.-W., Kang, S., & Lee, Y.-H. (2009). Rice blast fungus (Magnaporthe oryzae) infects Arabidopsis via a mechanism distinct from that required for the infection of rice. Plant Physiology, 149, 474–486.

    Article  PubMed  CAS  Google Scholar 

  • Pedley, K. F., & Martin, G. B. (2004). Identification of MAPKs and their possible MAPK kinase activatiors involved in the Pto-mediated defence response of tomato. Journal of Biological Chemistry, 279, 49229–49235.

    Article  PubMed  CAS  Google Scholar 

  • Sato, S., Soga, T., Nishioka, T., & Tomita, M. (2004). Simultaneous determination of the main metabolites in rice leaves using capillary electrophoresis mass spectrometry and capillary electrophoresis diode array detection. The Plant Journal, 40, 151–163.

    Article  PubMed  CAS  Google Scholar 

  • Schauer, N., & Fernie, A. R. (2006). Plant metabolomics: towards biological function and mechanism. Trends in Plant Science, 11, 508–516.

    Article  PubMed  CAS  Google Scholar 

  • Sobolev, A. P., Brosio, E., Gianferri, R., & Segre, A. L. (2005). Metabolic profile of lettuce leaves by high-field NMR spectra. Magnetic Resonance in Chemistry, 43, 625–638.

    Article  PubMed  CAS  Google Scholar 

  • Talbot, N. J. (1995). Having a blast: exploring the pathogenicity of Magnaporthe grisea. Trends in Microbiology, 3, 9–16.

    Article  PubMed  CAS  Google Scholar 

  • Talbot, N. J. (2003). On the trail of a cereal killer: Exploring the biology of Magnaporthe grisea. Annual Review of Microbiology, 57, 177–202.

    Article  PubMed  CAS  Google Scholar 

  • Tamogami, S., Rakwal, R., & Agrawal, G. K. (2008). Interplant communication: Airborne methyl jasmonate is essentially converted into JA and JA-Ile activating jasmonate signaling pathway and VOCs emission. Biochemical and Biophysical Research Communications, 376, 723–727.

    Article  PubMed  CAS  Google Scholar 

  • Weljie, A. M., Dowlatabadi, R., Miller, B. J., Vogel, H. J., & Jirik, F. R. (2007). An inflammatory arthritis-associated metabolite biomarker pattern revealed by 1H NMR spectroscopy. Journal of Proteome Research, 6, 3456–3464.

    Article  PubMed  CAS  Google Scholar 

  • Wiklund, S., Karlsson, M., Antti, H., Johnels, D., Sjöström, M., Wingsle, G., et al. (2005). A new metabonomic strategy for analysing the growth process of the poplar tree. Plant Biotechnology Journal, 3, 353–362.

    Article  PubMed  CAS  Google Scholar 

  • Yu, J., Hu, S., Wang, J., Wong, G. K.-S., Li, S., Liu, B., et al. (2002). A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science, 296, 79–92.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Oliver A.H. Jones was financially supported by the European Union (European Commission, FP6 Contract No. 003956. The study was in part funded by a grant from the Plant Signalling Network Research Centre from the Korean Science and Engineering Foundation. The authors also thank Dr. Young Hae Choi, Professor Robert Verpoorte and Professor George Ratcliffe for help with the NMR analysis and Drs. Aalim Welji and Denis Rubtsov for help with the Matlab code. The authors also thank the three anonymous reviewers whose thoughtful comments greatly improved the final manuscript.

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  1. Oliver A. H. Jones

    Present address: The Christopherson Building, School of Engineering & Computing Sciences, University of Durham, South Road, Durham, DH1 3LE, UK

Authors and Affiliations

  1. The Hopkins Building, Department of Biochemistry, University of Cambridge, Tennis Court Road, Cambridge, CB2 1QW, UK

    Oliver A. H. Jones & Julian L. Griffin

  2. BHF Magnetic Resonance Unit, Wellcome Trust Centre for Human Genetics, University of Oxford, Roosevelt Drive, Oxford, OX3 7BN, UK

    Mahon L. Maguire

  3. Department of Molecular Biology, College of Life Sciences, Sejong University, Seoul, 143-747, South Korea

    Young-Ho Jung & Nam-Soo Jwa

  4. Analysis Department, General Analysis Division, Biotoxtech Co., Ltd., Ochang Scientific Industrial Complex, 686-2 Yangcheong-ri, Ochang-eup, Chungcheongbuk-do, 363-883, South Korea

    Young-Ho Jung

  5. Health Technology Research Centre (HTRC), National Institute of Advanced Industrial Science and Technology (AIST), 16-1 Onogawa, Tsukuba, 305-8569, Ibaraki, Japan

    Junko Shibato & Randeep Rakwal

  6. Research Laboratory for Biotechnology and Biochemistry (RLABB), GPO Box 8207, Kathmandu, Nepal

    Randeep Rakwal & Ganesh K. Agrawal

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  1. Oliver A. H. Jones
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Correspondence to Oliver A. H. Jones.

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Jones, O.A.H., Maguire, M.L., Griffin, J.L. et al. Using metabolic profiling to assess plant-pathogen interactions: an example using rice (Oryza sativa) and the blast pathogen Magnaporthe grisea . Eur J Plant Pathol 129, 539–554 (2011). https://doi.org/10.1007/s10658-010-9718-6

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  • DOI: https://doi.org/10.1007/s10658-010-9718-6

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