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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
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.
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.
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.
Barron, G. L., & Thorn, R. G. (1987). Destruction of nematodes by species of Pleurotus. Canadian Journal of Botany, 65, 774–778.
Bernardini, M., Carilli, A., Pacioni, G., et al. (1975). Isolation of beauvericin from Paecilomyces fumoso-roseus. Phytochemistry, 14, 1865.
Closse, A., & Huguenin, R. (1974). Solierung und strukturaufklarung von chlamydocin (Isolation and elucidation of structure of chlamydocin). Helvetica Chimica Acta, 57, 533–545.
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.
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.
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.
Dixon, R. A., & Strack, D. (2003). Phytochemistry meets genome analysis, and beyond. Phytochemistry, 62, 815–816.
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.
Duarte, A., Maleita, C., Abrantes, I., et al. (2015). Tomato root exudates induce transcriptional changes of Meloidogyne hispanica genes. Phytopathologia Mediterranea, 54, 104–108.
Eichinger, D. (1997). Encystation of entamoeba parasites. BioEssays, 19, 633–639.
Elsworth, J. F., & Grove, J. F. (1974). Search for biologically-active cyclodepsipeptides from Beauveria bassiana. South African Journal of Science, 70, 379.
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.
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.
Fiehn, O. (2002). Metabolomics- the link between genotypes and phenotypes. Plant Molecular Biology, 48, 155–171.
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.
Gheysen, G., & Mitchum, M. G. (2011). How nematodes manipulate plant development pathways for infection. Current Opinion in Plant Biology, 14, 415–421.
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.
Griffiths, W. J. (2008). Metabolomics, metabonomics and metabolite profiling. Cambridge: RSC Publishing.
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.
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.
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.
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.
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.
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.
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.
Khambay, B. P. S., Bourne, J. M., Cameron, S., et al. (2000). A nematicidal metabolite from Verticillium chlamydosporium. Pest Management Science, 56, 1098−1099.
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.
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.
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.
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.
Lindon, J. C., Nicholson, J. K., & Holmes, E. (2011). The handbook of Metabonomics and metabolomics. Amsterdam: Elsevier Science.
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.
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.
Lutz, N. W., Sweedler, J. V., & Wevers, R. A. (2013). Methodologies for metabolomics: Experimental strategies and techniques. Cambridge: Cambridge University Press.
Madsen, R., Lundstedt, T., & Trygg, J. (2010). Chemometrics in metabolomics – A review in human disease diagnosis. Analytica Chimica Acta, 659, 23–33.
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.
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.
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.
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.
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.
Niu, X.-M., & Zhang, K.-Q. (2011). Arthrobotrys oligospora: A model organism for understanding the interaction between fungi and nematodes. Mycology, 2, 59–78.
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.
Païs, M., Das, B. C., & Ferron, P. (1981). Depsipeptides from Metarhizium anisopliae. Phytochemistry, 20, 715–723.
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.
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.
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.
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.
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.
Stähelin, H., & Trippmacher, A. (1974). Cytostatic activity of chlamydocin, a rapidly inactivated cyclic tetrapeptide. European Journal of Cancer, 10, 801–808.
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.
Suzuki, A., Kuyama, S., Kodaira, Y., et al. (1966). Structural elucidation of destruxin A. Agricultural and Biological Chemistry, 30, 517–518.
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.
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.
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.
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.
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.
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.
Vega, F. E., Goettel, M. S., Blackwell, M., et al. (2009). Fungal entomopathogens: New insights on their ecology. Fungal Ecology, 2, 149–159.
Wahlman, M., & Davidson, B. S. (1993). New destruxins from the entomopathogenic fungus Metarhizium anisopliae. Journal of Natural Products, 56, 643–647.
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.
Weckwerth, W. (2007). Metabolomics: Methods and protocols. Totowa/NJ: Humana Press.
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.
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.
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.
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.
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
Corresponding author
Editor information
Editors and Affiliations
Rights 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
DOI: https://doi.org/10.1007/978-3-319-59224-4_8
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-59222-0
Online ISBN: 978-3-319-59224-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)