Skip to main content

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.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barron, G. L., & Thorn, R. G. (1987). Destruction of nematodes by species of Pleurotus. Canadian Journal of Botany, 65, 774–778.

    Article  Google Scholar 

  • Bernardini, M., Carilli, A., Pacioni, G., et al. (1975). Isolation of beauvericin from Paecilomyces fumoso-roseus. Phytochemistry, 14, 1865.

    Article  CAS  Google Scholar 

  • Closse, A., & Huguenin, R. (1974). Solierung und strukturaufklarung von chlamydocin (Isolation and elucidation of structure of chlamydocin). Helvetica Chimica Acta, 57, 533–545.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon, R. A., & Strack, D. (2003). Phytochemistry meets genome analysis, and beyond. Phytochemistry, 62, 815–816.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Duarte, A., Maleita, C., Abrantes, I., et al. (2015). Tomato root exudates induce transcriptional changes of Meloidogyne hispanica genes. Phytopathologia Mediterranea, 54, 104–108.

    CAS  Google Scholar 

  • Eichinger, D. (1997). Encystation of entamoeba parasites. BioEssays, 19, 633–639.

    Article  CAS  PubMed  Google Scholar 

  • Elsworth, J. F., & Grove, J. F. (1974). Search for biologically-active cyclodepsipeptides from Beauveria bassiana. South African Journal of Science, 70, 379.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Gheysen, G., & Mitchum, M. G. (2011). How nematodes manipulate plant development pathways for infection. Current Opinion in Plant Biology, 14, 415–421.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Griffiths, W. J. (2008). Metabolomics, metabonomics and metabolite profiling. Cambridge: RSC Publishing.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Khambay, B. P. S., Bourne, J. M., Cameron, S., et al. (2000). A nematicidal metabolite from Verticillium chlamydosporium. Pest Management Science, 56, 1098−1099.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Lindon, J. C., Nicholson, J. K., & Holmes, E. (2011). The handbook of Metabonomics and metabolomics. Amsterdam: Elsevier Science.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Lutz, N. W., Sweedler, J. V., & Wevers, R. A. (2013). Methodologies for metabolomics: Experimental strategies and techniques. Cambridge: Cambridge University Press.

    Google Scholar 

  • Madsen, R., Lundstedt, T., & Trygg, J. (2010). Chemometrics in metabolomics – A review in human disease diagnosis. Analytica Chimica Acta, 659, 23–33.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Nordbring-Hertz, B., Jansson, H.B., Tunlid, A. (2006) Nematophagous fungi. eLS Citable reviews in the life sciences doi: 10.1002/9780470015902.a0000374.pub3.

  • Olthof, T. H. A., & Estey, R. H. A. (1963). A nematotoxin produced by the nematophagous fungus Arthrobotrys oligospora Fresenius. Nature, 197, 514–515.

    Article  Google Scholar 

  • Païs, M., Das, B. C., & Ferron, P. (1981). Depsipeptides from Metarhizium anisopliae. Phytochemistry, 20, 715–723.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

  • 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.

    Article  CAS  Google Scholar 

  • Stähelin, H., & Trippmacher, A. (1974). Cytostatic activity of chlamydocin, a rapidly inactivated cyclic tetrapeptide. European Journal of Cancer, 10, 801–808.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Suzuki, A., Kuyama, S., Kodaira, Y., et al. (1966). Structural elucidation of destruxin A. Agricultural and Biological Chemistry, 30, 517–518.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Vega, F. E., Goettel, M. S., Blackwell, M., et al. (2009). Fungal entomopathogens: New insights on their ecology. Fungal Ecology, 2, 149–159.

    Article  Google Scholar 

  • Wahlman, M., & Davidson, B. S. (1993). New destruxins from the entomopathogenic fungus Metarhizium anisopliae. Journal of Natural Products, 56, 643–647.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Weckwerth, W. (2007). Metabolomics: Methods and protocols. Totowa/NJ: Humana Press.

    Book  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nuria Escudero .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Escudero, N., Marhuenda-Egea, F., Lopez-Llorca, L.V. (2017). Metabolomics. In: Manzanilla-López, R., Lopez-Llorca, L. (eds) Perspectives in Sustainable Nematode Management Through Pochonia chlamydosporia Applications for Root and Rhizosphere Health. Sustainability in Plant and Crop Protection. Springer, Cham. https://doi.org/10.1007/978-3-319-59224-4_8

Download citation

Publish with us

Policies and ethics