Abstract
Fusarium foetens, a pathogen of Begonia plants, has been recently described as a new fungal species. This Fusarium species causes a destructive vascular wilt disease which leads to the death of the plant. Moreover, Fusarium species are known to produce a huge variety of secondary metabolites such as mycotoxins and phytotoxins. Here, we studied the toxicogenic profile of one F. foetens strain, isolated from maize, employing two methods based on the use of ultra-performance liquid chromatography coupled to mass spectrometry-ion trap-time of flight detection. The mycotoxins beauvericin and fusaric acid were detected in a pure culture of F. foetens. In addition, four fusaric acid analogs (10,11-dihidroxyfusaric acid, hydroxyfusaric acid, dehydrofusaric acid, and a hydroxylated unsaturated fusaric acid analog) were tentatively identified on the basis of their accurate mass and fragmentation patterns. Therefore, these preliminary data indicate that F. foetens isolated from maize is able to produce Fusarium mycotoxins including beauvericin and fusaric acid.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Burmeister HR, Grove MD, Peterson RE, Weisleder D, Plattner RD (1985) Isolation and characterization of two new fusaric acid analogs from Fusarium moniliforme NRRL 13,163. Appl Environ Microbiol 50:311–314
Capasso R, Evidente A, Cutignano A, Vurro M, Zonno MC, Bottalico A (1996) Fusaric and 9,10-dehydrofusaric acids and their methyl esters from Fusarium nygamai. Phytochemistry 41:1035–1039. https://doi.org/10.1016/0031-9422(95)00716-4
Crutcher FK, Puckhaber LS, Bell AA, Liu J, Duke SE, Stipanovic RD, Nichols RL (2017) Detoxification of fusaric acid by the soil microbe Mucor rouxii. J Agric Food Chem 65:4989–4992. https://doi.org/10.1021/acs.jafc.7b01655
Curir P, Guglieri L, Dolci M, Capponi A, Aurino G (2000) Fusaric acid production by Fusarium oxysporum f sp lilii and its role in the lily basal rot disease. Eur J Plant Pathol 106:849–856. https://doi.org/10.1023/A:1008739708931
D’Mello JPF, Placinta CM, Macdonald AMC (1999) Fusarium mycotoxins: a review of global implications for animal health, welfare and productivity. Anim Feed Sci Technol 80:183–205. https://doi.org/10.1016/S0377-8401(99)00059-0
EPPO (2013) PM 7/111 (1) Fusarium foetens. EPPO Bulletin 43:68–80. https://doi.org/10.1111/epp.12021
Ferrer I, Thurman EM (2003) Liquid chromatography/time-of-flight/mass spectrometry (LC/TOF/MS) for the analysis of emerging contaminants. TrAC Trends Anal Chem 22:750–756. https://doi.org/10.1016/S0165-9936(03)01013-6
Frisvad JC, Andersen B, Thrane U (2008) The use of secondary metabolite profiling in chemotaxonomy of filamentous fungi. Mycol Res 112:231–240. https://doi.org/10.1016/j.mycres.2007.08.018
Gonzalez JM, Alfonso A, Sainz MJ, Botana LM (2016) Production and detection of the natural ionophore beauvericin. Planta Med 82:S1–S381. https://doi.org/10.1055/s-0036-1596691
Gonzalez-Jartin JM, Alfonso A, Sainz MJ, Vieytes MR, Botana LM (2017) UPLC-MS-IT-TOF identification of circumdatins produced by Aspergillus ochraceus. J Agric Food Chem 65:4843–4852. https://doi.org/10.1021/acs.jafc.7b01845
Gonzalez-Jartin JM, Alfonso A, Sainz MJ, Vieytes MR, Botana LM (2018) Detection of new emerging type-A trichothecenes by untargeted mass spectrometry. Talanta 178:37–42. https://doi.org/10.1016/j.talanta.2017.09.009
Gruber-Dorninger C, Novak B, Nagl V, Berthiller F (2017) Emerging mycotoxins: beyond traditionally determined food contaminants. J Agric Food Chem 65:7052–7070. https://doi.org/10.1021/acs.jafc.6b03413
Harvey RB, Edrington TS, Kubena LF, Elissalde MH, Casper HH, Rottinghaus GE, Turk JR (1996) Effects of dietary fumonisin B1-containing culture material, deoxynivalenol-contaminated wheat, or their combination on growing barrows. Am J Vet Res 57:1790–1794
Huvenne H, Debode J, Maes M, Heungens K (2011) Real-time PCR mediated monitoring of Fusarium foetens in symptomatic and non-symptomatic hosts. Eur J Plant Pathol 131:705–717. https://doi.org/10.1007/s10658-011-9844-9
Klitgaard A, Iversen A, Andersen MR, Larsen TO, Frisvad JC, Nielsen KF (2014) Aggressive dereplication using UHPLC-DAD-QTOF: screening extracts for up to 3000 fungal secondary metabolites. Anal Bioanal Chem 406:1933–1943. https://doi.org/10.1007/s00216-013-7582-x
Komada H (1975) Development of a selective medium for quantitative isolation of Fusarium oxysporum from natural soil. Rev Plant Prot Res 8:114–125
Leslie JF, Summerell BA (2006) The Fusarium laboratory manual. Blackwell Publishing, New Jersey. https://doi.org/10.1002/9780470278376
Li-Jun M, van der Does HC, Borkovich KA et al (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367–373. https://doi.org/10.1038/nature08850
Löffler H, Mouris J (1992) Fusaric acid: phytotoxicity and in vitro production by Fusarium oxysporum f. sp. lilii, the causal agent of basal rot in lilies Netherlands. J Plant Pathol 98:107–115. https://doi.org/10.1007/BF01996323
Lopez-Diaz C, Rahjoo V, Sulyok M, Ghionna V, Martín-Vicente A, Capilla J, Di Pietro A, López- Berges MS (2018) Fusaric acid contributes to virulence of Fusarium oxysporum on plant and mammalian hosts. Mol Plant Pathol 19:440–453. https://doi.org/10.1111/mpp.12536
Munkvold GP (2017) Fusarium species and their associated mycotoxins. In: Moretti A, Susca A (eds) Mycotoxigenic fungi. Methods in molecular biology, vol 1542. Humana Press, New York, pp 51–106. https://doi.org/10.1007/978-1-4939-6707-0_4
Nazari F, Sulyok M, Kobarfard F, Yazdanpanah H, Krska R (2015) Evaluation of emerging Fusarium mycotoxins beauvericin, enniatins, fusaproliferin and moniliformin in domestic rice in Iran. Iran J Pharm Res 14:505–512
Niehaus EM, von Bargen KW, Espino JJ, Pfannmuller A, Humpf HU, Tudzynski B (2014) Characterization of the fusaric acid gene cluster in Fusarium fujikuroi. Appl Microbiol Biotechnol 98:1749–1762. https://doi.org/10.1007/s00253-013-5453-1
O'Donnell K, Kistler HC, Tacke BK, Casper HH (2000) Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proc Natl Acad Sci U S A 97:7905–7910. https://doi.org/10.1073/pnas.130193297
Rabie CJ, Marasas WFO, Thiel PG, Lübben A, Vleggaar R (1982) Moniliformin production and toxicity of different Fusarium species from Southern Africa. Appl Environ Microbiol 43:517–521
Sainz MJ, Alfonso A, Botana LM (2015) Considerations about international mycotoxin legislation, food security, an climate change. In: Botana LM, Sainz MJ (eds) Climate change and mycotoxins. De Gruyter, Berlin, pp 153–173. https://doi.org/10.1515/9783110333619-010
Sainz MJ, Gonzalez-Jartin JM, Aguin O, Mansilla JP, Botana LM (2018) Isolation, characterization, and identification of mycotoxin-producing fungi. In: Botana LM (ed) Environmental toxicology. De Gruyter, Berlin, pp 203–245. https://doi.org/10.1515/9783110442045-008
Schroers HJ, Baayen RP, Meffert JP, de Gruyter J, Hooftman M, O'Donnell K (2004) Fusarium foetens, a new species pathogenic to begonia elatior hybrids (Begonia x hiemalis) and the sister taxon of the Fusarium oxysporum species complex. Mycologia 96:393–406. https://doi.org/10.2307/3762070
Smedsgaard J (1997) Micro-scale extraction procedure for standardized screening of fungal metabolite production in cultures. J Chromatogr A 760:264–270. https://doi.org/10.1016/S0021-9673(96)00803-5
Smith JE, Solomons GL, Lewis CW, Anderson JG (1994) Mycotoxins in human nutrition and health. European Commission Directorate-General XII, Bruxelles
Smith TK, McMillan EG, Castillo JB (1997) Effect of feeding blends of Fusarium mycotoxin-contaminated grains containing deoxynivalenol and fusaric acid on growth and feed consumption of immature swine. J Anim Sci 75:2184–2191. https://doi.org/10.2527/1997.7582184x
Streit E, Schatzmayr G, Tassis P, Tzika E, Marin D, Taranu I, Tabuc C, Nicolau A, Aprodu I, Puel O, Oswald IP (2012) Current situation of mycotoxin contamination and co-occurrence in animal feed-focus on Europe. Toxins 4:788–809. https://doi.org/10.3390/toxins4100788
Sulyok M, Berthiller F, Krska R, Schuhmacher R (2006) Development and validation of a liquid chromatography/tandem mass spectrometric method for the determination of 39 mycotoxins in wheat and maize. Rapid Commun Mass Spectrom 20:2649–2659. https://doi.org/10.1002/rcm.2640
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
van der Gaag D, Raak M (2010) Pest risk assessment Fusarium foetens. Plant Protection Service, Ministry of Agriculture, Nature and Food Quality, The Hague
Wu H-S, BW LD-Y, Ling N, Ying R-R, Raza W, Shen Q-R (2008) Effect of fusaric acid on biomass and photosynthesis of watermelon seedlings leaves. Caryologia 61:258–268. https://doi.org/10.1080/00087114.2008.10589638
Zhu Q, Zhang H, Duan Y, Chang S, Wei L, Li C, Miao H (2016) Identification of the toxin of sesame Fusarium wilt pathogen and its toxic effect on sesame seedlings. Plant Prot 42:27–33. https://doi.org/10.3969/j.issn.0529-1542.2016.04.004
Zonno MC, Vurro M, Capasso R, Evidente A, Cutignano A, Sauerborn J, Thomas H (1996) Phytotoxic metabolites produced by Fusarium nygamai from Striga hermonthica. In: Moran VC, Hoffmann (eds) Proceedings of the IX International Symposium on Biological Control of Weeds, University of Cape Town, South Africa, pp 223–226
Acknowledgments
The research leading to these results has received funding from the following FEDER cofunded grants: from Conselleria de Cultura, Educacion e Ordenación Universitaria, Xunta de Galicia, 2017 GRC GI-1682 (ED431C 2017/01); from CDTI and Technological Funds, supported by Ministerio de Economía, Industria y Competitividad, AGL2014-58210-R, AGL2016-78728-R (AEI/FEDER, UE), ISCIII/PI16/01830, RTC-2016-5507-2, and ITC-20161072; from European Union POCTEP 0161-Nanoeaters-1-E-1, Interreg AlertoxNet EAPA-317-2016, Interreg Agritox EAPA-998-2018, and H2020 778069-EMERTOX. Jesús M. González-Jartín was supported by a fellowship from Programa de Formación de Profesorado Universitario (FPU14/00166), Ministerio de Educación, Cultura y Deporte, Spain.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest. The authors have full control of all primary data and allow the journal to review the data if requested.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 49 kb)
Rights and permissions
About this article
Cite this article
González-Jartín, J.M., Alfonso, A., Sainz, M.J. et al. First report of Fusarium foetens as a mycotoxin producer. Mycotoxin Res 35, 177–186 (2019). https://doi.org/10.1007/s12550-019-00341-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12550-019-00341-3