Advertisement

Metabolomics

  • Nuria EscuderoEmail author
  • Frutos Marhuenda-Egea
  • Luis V. Lopez-Llorca
Chapter
Part of the Sustainability in Plant and Crop Protection book series (SUPP)

Abstract

Metabolomics is the study of metabolites, small biomolecules (carbohydrates, lipids, amino acids and organic acids) present in a biological sample. Metabolomics tools include chromatography for separating metabolites and spectroscopy techniques for their identification. Metabolomics tools have allowed to analyze the composition of tomato root exudates in the tritrophic system: Pochonia chlamydosporia, Meloidogyne javanica and tomato (Solanum lycopersicum) and changes in root exudates that were due to the presence of the fungus, the nematode or both. Large amounts of fluorescent compounds were detected in tomato root exudates from plants with M. javanica root galls and egg masses. Profiles of root exudates in 1H NMR included organic acids, sugars and amino acids. Acetate signal increased in root exudates with M. javanica. Using HPLC-MS metabolomic fingerprints of tomato root exudates were generated. Several m/z signals have been found and related to the presence of M. javanica and only one with the presence of P. chlamydosporia. Metabolomics data integrated with transcriptomics will help to understand rhizosphere signalling in multitrophic systems.

Notes

Acknowledgements

This research was funded by the Spanish Ministry of Economy and Competitiveness Grant AGL 2015-66833-R. Luis Vicente Lopez-Llorca was awarded a sabbatical grant (PR2015_00087) by the Spanish Ministry of Education, Culture and Sport.

References

  1. Allwood, J. W., Ellis, D. I., & Goodacre, R. (2007). Metabolomic technologies and their application to the study of plants and plant–host interactions. Physiologia Plantarum, 132, 117–135.Google Scholar
  2. Azumi, M., Ishidoh, K., Kinoshita, H., et al. (2008). Aurovertins F−H from the entomopathogenic fungus Metarhizium anisopliae. Journal of Natural Products, 71, 278–280.CrossRefPubMedGoogle Scholar
  3. Baldacci-Cresp, F., Chan, C., Maucourt, M., et al. (2012). (homo)glutathione deficiency impairs root-knot nematode development in Medicago truncatula. PLoS Pathogens, 8(1), e1002471.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Barron, G. L., & Thorn, R. G. (1987). Destruction of nematodes by species of Pleurotus. Canadian Journal of Botany, 65, 774–778.CrossRefGoogle Scholar
  5. Bernardini, M., Carilli, A., Pacioni, G., et al. (1975). Isolation of beauvericin from Paecilomyces fumoso-roseus. Phytochemistry, 14, 1865.CrossRefGoogle Scholar
  6. Closse, A., & Huguenin, R. (1974). Solierung und strukturaufklarung von chlamydocin (Isolation and elucidation of structure of chlamydocin). Helvetica Chimica Acta, 57, 533–545.CrossRefPubMedGoogle Scholar
  7. de Bekker, C., Smith, P. B., Patterson, A. D., et al. (2013). Metabolomics reveals the heterogeneous secretome of two entomopathogenic fungi to ex vivo cultured insect tissues. PloS One, 8(8), e70609.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Degenkolb, T., & Vilcinskas, A. (2016a). Metabolites from nematophagous fungi and nematicidal natural products from fungi as an alternative for biological control. Part I: Metabolites from nematophagous ascomycetes. Applied Microbiology and Biotechnology, 100, 3799–3812.CrossRefPubMedGoogle Scholar
  9. Degenkolb, T., & Vilcinskas, A. (2016b). Metabolites from nematophagous fungi and nematicidal natural products from fungi as alternatives for biological control. Part II: Metabolites from nematophagous basidiomycetes and non-nematophagous fungi. Applied Microbiology and Biotechnology, 100, 3813–3824.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Dixon, R. A., & Strack, D. (2003). Phytochemistry meets genome analysis, and beyond. Phytochemistry, 62, 815–816.CrossRefPubMedGoogle Scholar
  11. Donzelli, B. G. G., Krasnoff, S. B., Sun-Moon, Y., et al. (2012). Genetic basis of destruxin production in the entomopathogen Metarhizium robertsii. Current Genetics, 58, 105–116.CrossRefGoogle Scholar
  12. Duarte, A., Maleita, C., Abrantes, I., et al. (2015). Tomato root exudates induce transcriptional changes of Meloidogyne hispanica genes. Phytopathologia Mediterranea, 54, 104–108.Google Scholar
  13. Eichinger, D. (1997). Encystation of entamoeba parasites. BioEssays, 19, 633–639.CrossRefPubMedGoogle Scholar
  14. Elsworth, J. F., & Grove, J. F. (1974). Search for biologically-active cyclodepsipeptides from Beauveria bassiana. South African Journal of Science, 70, 379.Google Scholar
  15. Elsworth, J. F., & Grove, J. F. (1977). Cyclodepsipeptides from Beauveria bassiana Bals. Part 1. Beauverolides H and I. Journal of the Chemical Society, Perkin Transactions, 1, 270–273.CrossRefGoogle Scholar
  16. Escudero, N., Marhuenda-Egea, F. C., Ibanco-Cañete, R., et al. (2014). A metabolomic approach to study the rhizodeposition in the tritrophic interaction: Tomato, Pochonia chlamydosporia and Meloidogyne javanica. Metabolomics, 10, 788–804.CrossRefGoogle Scholar
  17. Fiehn, O. (2002). Metabolomics- the link between genotypes and phenotypes. Plant Molecular Biology, 48, 155–171.CrossRefPubMedGoogle Scholar
  18. García-Alcalde, F., García-López, F., Dopazo, J., et al. (2011). Paintomics: A web based tool for the joint visualization of transcriptomics and metabolomics data. Bioinformatics, 27(1.), btq594), 137–139.CrossRefPubMedGoogle Scholar
  19. Gheysen, G., & Mitchum, M. G. (2011). How nematodes manipulate plant development pathways for infection. Current Opinion in Plant Biology, 14, 415–421.CrossRefPubMedGoogle Scholar
  20. Gómez-Vidal, S., Salinas, J., Tena, M., et al. (2009). Proteomic analysis of date palm (Phoenix dactylifera L.) responses to endophytic colonization by entomopathogenic fungi. Electrophoresis, 30, 2996–3005.CrossRefPubMedGoogle Scholar
  21. Griffiths, W. J. (2008). Metabolomics, metabonomics and metabolite profiling. Cambridge: RSC Publishing.Google Scholar
  22. Gupta, S., Roberts, D. W., & Renwick, J. A. A. (1989). Insecticidal cyclodepsipeptides from Metarhizium anisopliae. Journal of the Chemical Society, Perkin Transactions 1, 12, 2347–2358.CrossRefGoogle Scholar
  23. Hamill, R. L., Higgens, C. E., Boaz, H. E., et al. (1969). The structure of Beauvericin, a new depsipeptide antibiotic toxic to Artemia salina. Tetrahedron Letters, 10, 4255–4258.CrossRefGoogle Scholar
  24. Hellwig, V., Mayer-Bartschmid, A., Müller, H., et al. (2003). Pochonins A-F, new antiviral and antiparasitic resorcylic acid lactones from Pochonia chlamydosporia var. catenulata. Journal of Natural Products, 66, 829–837.CrossRefPubMedGoogle Scholar
  25. Hofmann, J., Ashry El, A. E. N., Anwar, S., et al. (2010). Metabolic profiling reveals local and systemic responses of host plants to nematode parasitism. The Plant Journal, 62, 1058–1071.PubMedPubMedCentralGoogle Scholar
  26. Huang, T. C., Chang, H. Y., Hsu, C. H., et al. (2008). Targeting therapy for breast carcinoma by ATP synthase inhibitor aurovertin B. Journal of Proteome Research, 7, 1433–1444.CrossRefPubMedGoogle Scholar
  27. Ikeda, A., Shinonaga, H., Fujimoto, N., Kasai, Y. (2003). PCT Gazette – Section I. Published international applications. WO 03/086334, 23 Oct 2003, p 62. http://www.wipo.int/edocs/pctdocs/en/2003/pct_2003_43-section1.pdf
  28. Jammes, F., Lecomte, P., Almeida-Engler, J., et al. (2005). Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. The Plant Journal, 44, 447–458.CrossRefPubMedGoogle Scholar
  29. Kanaoka, M., Isogai, A., & Murakoshi, S. (1978). Bassianolide, a new insecticidal cyclodepsipeptide from Beauveria bassiana and Verticillium lecanii. Agricultural and Biological Chemistry, 42, 629–635.Google Scholar
  30. Khambay, B. P. S., Bourne, J. M., Cameron, S., et al. (2000). A nematicidal metabolite from Verticillium chlamydosporium. Pest Management Science, 56, 1098−1099.CrossRefGoogle Scholar
  31. Kershaw, M. J., Moorhouse, E. R., Bateman, R., et al. (1999). The role of destruxins in the pathogenicity of Metarhizium anisopliae for three species of insect. Journal of Invertebrate Pathology, 74, 213–223.CrossRefPubMedGoogle Scholar
  32. Kitamura, Y., Koshino, H., Nakamura, T., et al. (2013). Total synthesis of the proposed structure for pochonicine and determination of its absolute configuration. Tetrahedron Letters, 54, 1456.CrossRefGoogle Scholar
  33. Kodaira, Y. (1961). Biochemical studies on the muscardine fungi in the silkworms Bombyx mori. Journal of the Faculty of Textile Science and Technology, Shinshu University Series A, Biology, 29, 1–68.Google Scholar
  34. Larriba, E., Jaime, M. D. L. A., Carbonell-Caballero, J., et al. (2014). Sequencing and functional analysis of the genome of a nematode egg-parasitic fungus, Pochonia chlamydosporia. Fungal Genetics and Biology, 65(C), 69–80.CrossRefPubMedGoogle Scholar
  35. Lindon, J. C., Nicholson, J. K., & Holmes, E. (2011). The handbook of Metabonomics and metabolomics. Amsterdam: Elsevier Science.Google Scholar
  36. Liu, C. M., Huang, S. S., & Tzeng, Y. M. (2004). Analysis of destruxins produced from Metarhizium anisopliae by capillary electrophoresis. Journal of Chromatographic Science, 42, 140–144.CrossRefPubMedGoogle Scholar
  37. Luo, F., Wang, Q., Yin, C., et al. (2015). Differential metabolic responses of Beauveria bassiana cultured in pupae extracts, root exudates and its interactions with insect and plant. Journal of Invertebrate Pathology, 130, 1–11.CrossRefGoogle Scholar
  38. Lutz, N. W., Sweedler, J. V., & Wevers, R. A. (2013). Methodologies for metabolomics: Experimental strategies and techniques. Cambridge: Cambridge University Press.Google Scholar
  39. Madsen, R., Lundstedt, T., & Trygg, J. (2010). Chemometrics in metabolomics – A review in human disease diagnosis. Analytica Chimica Acta, 659, 23–33.CrossRefPubMedGoogle Scholar
  40. Martin-Mata, J., Marhuenda-Egea, F. C., Moral, R., et al. (2015). Characterization of dissolved organic matter from sewage sludge using 3D-fluorescence spectroscopy and chemometric tools. Communications in Soil Science and Plant Analysis, 46, 188–196.CrossRefGoogle Scholar
  41. Masuoka, Y., Shin-Ya, K., Kim, J. B., et al. (2000a). Diheteropeptin, a new substance with TGF-ß-like activity, produced by a fungus, Diheterospora chlamydosporia. I. Production, Isolation and biological activities. The Journal of Antibiotics, 53, 788–792.CrossRefPubMedGoogle Scholar
  42. Masuoka, Y., Shin-Ya, K., Kim, J. B., et al. (2000b). Diheteropeptin, a new substance with TGF-ß-like activity, produced by a fungus, Diheterospora chlamydosporia. II. Physico-chemical properties and structure elucidation. The Journal of Antibiotics, 53, 793–798.CrossRefPubMedGoogle Scholar
  43. Murphy, K. R., Bro, R., & Stedmon, C. A. (2014). Chemometric analysis of organic matter fluorescence. In P. G. Coble, J. Lead, A. Baker, D. M. Reynolds, & R. G. M. Spencer (Eds.), Aquatic organic matter fluorescence (pp. 339–375). New York: Cambridge University Press.CrossRefGoogle Scholar
  44. Niu, X. M., Wang, Y. L., Chu, Y. S., et al. (2010). Nematodetoxic aurovertin-type metabolites from a root-knot nematode parasitic fungus Pochonia chlamydosporia. Journal of Agricultural and Food Chemistry, 58, 828–834.CrossRefPubMedGoogle Scholar
  45. Niu, X.-M., & Zhang, K.-Q. (2011). Arthrobotrys oligospora: A model organism for understanding the interaction between fungi and nematodes. Mycology, 2, 59–78.Google Scholar
  46. Nordbring-Hertz, B., Jansson, H.B., Tunlid, A. (2006) Nematophagous fungi. eLS Citable reviews in the life sciences doi:  10.1002/9780470015902.a0000374.pub3.
  47. Olthof, T. H. A., & Estey, R. H. A. (1963). A nematotoxin produced by the nematophagous fungus Arthrobotrys oligospora Fresenius. Nature, 197, 514–515.CrossRefGoogle Scholar
  48. Païs, M., Das, B. C., & Ferron, P. (1981). Depsipeptides from Metarhizium anisopliae. Phytochemistry, 20, 715–723.CrossRefGoogle Scholar
  49. Rudd, J. J., Kanyuka, K., Hassani-Pak, K., et al. (2015). Transcriptome and metabolite profiling of the infection cycle of Zymoseptoria tritici on wheat reveals a biphasic interaction with plant immunity involving differential pathogen chromosomal contributions and a variation on the hemibiotrophic lifestyle definition. Plant Physiology, 167, 1158–1185.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Samuels, R. I., Charnley, A. K., & Reynolds, S. E. (1988). Application of reversed-phase HPLC in separation and detection of the cyclodepsipeptide toxins produced by the entomopathogenic fungus Metarhizium anisopliae. Journal of Chromatographic Science, 26, 15–19.CrossRefGoogle Scholar
  51. Shinonaga, H., Kawamura, Y., Ikeda, A., et al. (2009a). The search for a hair-growth stimulant: New radicicol analogues as WNT-5A expression inhibitors from Pochonia chlamydosporia var. chlamydosporia. Tetrahedron Letters, 50, 108–110.CrossRefGoogle Scholar
  52. Shinonaga, H., Kawamura, Y., Ikeda, A., et al. (2009b). Pochonins K-P: New radicicol analogues from Pochonia chlamydosporia var. chlamydosporia and their WNT-5A expression inhibitory activities. Tetrahedron, 65, 3446–3453.CrossRefGoogle Scholar
  53. Shinonaga, H., Sakai, N., Nozawa, Y., et al. (2009c). 13-Bomomonocillin I: A New WNT-5A expression inhibitor produced by Pochonia chlamydosporia var. chlamydosporia. Heterocycles, 78(11). doi: 10.3987/COM-09-11809.
  54. Stadler, M., Anke, H., & Sterner, O. (1993). Linoleic acid – The nematicidal principle of several nematophagous fungi and its production in trap-forming submerged cultures. Archives of Microbiology, 160, 401–405.CrossRefGoogle Scholar
  55. Stähelin, H., & Trippmacher, A. (1974). Cytostatic activity of chlamydocin, a rapidly inactivated cyclic tetrapeptide. European Journal of Cancer, 10, 801–808.CrossRefPubMedGoogle Scholar
  56. Steinkellner, S., Mammerler, R., & Vierheilig, H. (2008). Germination of Fusarium oxysporum in root exudates from tomato plants challenged with different Fusarium oxysporum strains. European Journal of Plant Pathology, 122, 395–401.CrossRefGoogle Scholar
  57. Suzuki, A., Kuyama, S., Kodaira, Y., et al. (1966). Structural elucidation of destruxin A. Agricultural and Biological Chemistry, 30, 517–518.CrossRefGoogle Scholar
  58. Suzuki, A., Taguchi, H., & Tamura, S. (1970). Isolation and structure elucidation of three new insecticidal cyclodepsipeptides, destruxins C and D and desmethyldestruxin B, produced by Metarrhizium anisopliae. Agricultural and Biological Chemistry, 34, 813–816.CrossRefGoogle Scholar
  59. Suzuki, A., Kanaoka, M., Isogai, A., et al. (1977). Bassianolide, a new insecticidal cyclodepsipeptide from Beauveria bassiana and Verticillium lecanii. Tetrahedron Letters, 18, 2167–2170.CrossRefGoogle Scholar
  60. Tamura, S., Kuyama, S., Kodaira, Y., et al. (1964). Studies on destruxin B, an insecticidal depsipeptide produced by Oospora destructor. Institute of Applied Microbiology (University of Tokyo) Symposium Microbiology, 6, 127–140.Google Scholar
  61. Tan, K.-C., Ipcho, S. V. S., Trengove, R. D., et al. (2009). Assessing the impact of transcriptomics, proteomics and metabolomics on fungal phytopathology. Molecular Plant Pathology, 10, 703–715.CrossRefPubMedGoogle Scholar
  62. Usuki, H., Toyo-oka, M., Kanzaki, H., et al. (2009). Pochonicine, a polyhydroxylated pyrrolizidine alkaloid from fungus Pochonia suchlasporia var. suchlasporia TAMA 87 as a potent ß-N-acetylglucosaminidase inhibitor. Bioorganic & Medicinal Chemistry, 17, 7248–7253.CrossRefGoogle Scholar
  63. van Dam, N. M., & Bouwmeester, H. J. (2016). Metabolomics in the Rhizosphere: Tapping into belowground chemical communication. Trends in Plant Science, 21, 256–265.  dx.doi.org/10.1016/j.tplants.2016.01.008. Accessed 18 Oct 2016.CrossRefPubMedGoogle Scholar
  64. Vega, F. E., Goettel, M. S., Blackwell, M., et al. (2009). Fungal entomopathogens: New insights on their ecology. Fungal Ecology, 2, 149–159.CrossRefGoogle Scholar
  65. Wahlman, M., & Davidson, B. S. (1993). New destruxins from the entomopathogenic fungus Metarhizium anisopliae. Journal of Natural Products, 56, 643–647.CrossRefGoogle Scholar
  66. Wang, Y. L., Li, L. F., Li, D. X., et al. (2015). Yellow pigment aurovertins mediate interactions between the pathogenic fungus Pochonia chlamydosporia and its nematode host. Journal of Agricultural and Food Chemistry, 63, 6577–6587.CrossRefPubMedGoogle Scholar
  67. Weckwerth, W. (2007). Metabolomics: Methods and protocols. Totowa/NJ: Humana Press.CrossRefGoogle Scholar
  68. Xu, Y., Orozco, R., Wijeratne, E. M. K., et al. (2008). Biosynthesis of the cyclooligomer depsipeptide beauvericin, a virulence factor of the entomopathogenic fungus Beauveria bassiana. Chemistry & Biology, 15, 898–907.CrossRefGoogle Scholar
  69. Xu, Y., Orozco, R., Wijeratne, E. M. K., et al. (2009). Biosynthesis of the cyclooligomer depsipeptide bassianolide, an insecticidal virulence factor of Beauveria bassiana. Fungal Genetics and Biology, 46, 353–364.CrossRefPubMedGoogle Scholar
  70. Xu, Y. J., Luo, F., Gao, Q., et al. (2015). Metabolomics reveals insect metabolic responses associated with fungal infection. Analytical and Bioanalytical Chemistry. doi: 10.1007/s00216-015-8648–8.
  71. Zhang, H.-X., Tan, J.-L., Wei, L.-X., et al. (2012). Morphology regulatory metabolites from Arthrobotrys oligospora. Journal of Natural Products, 75, 1419–1423.CrossRefPubMedGoogle Scholar
  72. Zhu, J. S., Nakagawa, C. W., Adachi, I., et al. (2013). Synthesis of eight stereoisomers of Pochonicine: Nanomolar inhibition of β-N-Acetylhexosaminidases. The Journal of Organic Chemistry, 78, 10298–10309.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Nuria Escudero
    • 1
    • 2
    • 3
    Email author
  • Frutos Marhuenda-Egea
    • 4
    • 1
    • 2
  • Luis V. Lopez-Llorca
    • 1
    • 2
  1. 1.Laboratory of Plant Pathology, Department of Marine Sciences and Applied BiologyUniversity of AlicanteAlicanteSpain
  2. 2.Department of Marine Sciences and Applied Biology, Multidisciplinary Institute for Environmental Studies (MIES) Ramón MargalefUniversity of AlicanteAlicanteSpain
  3. 3.Department of Agri-Food Engineering and BiotechnologyUniversitat Politècnica de CatalunyaCatalunyaSpain
  4. 4.Department of Agrochemistry and BiochemistryUniversity of AlicanteAlicanteSpain

Personalised recommendations