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Rapid Macroconidia Production in Fusarium Graminearum 3- and 15-Acetyldeoxynivalenol (ADON) Chemotypes Using Sucrose-Water Medium

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Rapid Macroconidia Production in Fusarium Graminearum 3- and 15-Acetyldeoxynivalenol (ADON) Chemotypes Using Sucrose-Water Medium Ann Microbiol (2012) 62:965–971 DOI 10.1007/s13213-011-0335-1 ORIGINAL PAPERS Rapid macroconidia production in Fusarium graminearum 3- and 15-acetyldeoxynivalenol (ADON) chemotypes using sucrose-water medium Manel Ben Mansour & Yit Kheng Goh & Vladimir Vujanovic Received: 23 May 2011 /Accepted: 25 July 2011 /Published online: 11 August 2011 # Springer-Verlag and the University of Milan 2011 Abstract Sucrose-water medium induced a high rate of Petch] is the most common and devastating fungal disease macroconidia formation in Fusarium graminearum 3- and of small grain cereals in North America (Bai and Shaner 15-acetyldeoxynivalenol (ADON) chemotypes. The F. grami- 1994, 2004). Moreover, mycotoxins produced by F. grami- nearum isolates tested produced uniform macroconidia in nearum 3- and 15-ADON chemotypes are major sources of large quantities and within a shorter incubation period in food contamination (Desjardins and Proctor 2007, 2011). sucrose-water medium compared to other assessed media. At The primary mycotoxins present in grain include zearale- the same time, high rates of mycotoxin accumulation none and trichothecene derivatives, such as deoxynivalenol (trichothecenes: DON, 3-ADON, 15-ADON, and zearalenone: (DON), 3-acetyldeoxynivalenol (3-ADON) and 15- ZEA) in macroconidia were detected using high performance acetyldeoxynivalenol (15-ADON) (Foroud and Eudes liquid chromatography. The proposed “saccharose-water” 2009; Gale et al. 2011; Von der Ohe et al. 2010; Ward method represents a valuable alternative for conidia produc- et al. 2002). tion in mycotoxigenic F. graminearum isolates, having In fungal plant pathogens, including food molds, asexual advantages over the potentially mutagenic UV light, and spore formation (sporulation or conidiation) is a regular potato-dextrose agar, which can degenerate macroconidia, and secondary reproductive cycle for massive generation of over expensive chemical compounds or natural substances for conidia or infective inocula (Ohara et al. 2004; Sutton which the preparation protocols and handling procedures are 1982). Macroconidia are used frequently in artificially relatively complex or time-consuming. inoculated field trials to test the level of isolate pathoge- nicity by measuring mycotoxin accumulation in cereal grain Keywords Fusarium graminearum . Chemotype . (Harris et al. 1999; Miedaner et al. 2010). The latter is an Macroconidia formation . HPLC . Mycotoxin important parameter in the assessment of food quality and safety. Fusarium graminearum 3-ADON isolates have higher Introduction macroconidia production and growth rates compared to 15- ADON strains (Ward et al. 2008). This feature might Fusarium head blight (FHB) caused by Fusarium grami- partially explain the rapid spread of 3-ADON over 15- nearum Schwabe [teleomorph: Gibberella zeae (Schw.) ADON populations in North America (Gilbert et al. 2001; Ward et al. 2008). Under in vitro conditions, F. graminearum is unable to : : * M. B. Mansour Y. K. Goh V. Vujanovic ( ) generate macroconidia on commercially available, Department of Food and Bioproduct Sciences, University of Saskatchewan, carbohydrate-rich media such as potato dextrose agar Saskatoon SK S7N 5A8, Canada (PDA). Physical (near UV light), chemical [CMC: 1- e-mail: [email protected] cyclohexyl-3-(2-morpholinoethyl) carbodiimide metho-p- toluenesulfonate] and natural (carnation leaf and wheat M. B. Mansour Department of Plant Biotechnology, University of Tunis El Manar, bran) elements have been proposed to induce large-scale F. 1060 Tunis, Tunisia graminearum macroconidia production in the laboratory 966 Ann Microbiol (2012) 62:965–971 (Eudes et al. 2001;Fisheretal.1982; Hassan and Oakville, ON); (2) BM with 7 g/L CMC; (3) BM with Bullerman 2009). UV light and PDA medium are poten- 15 g/L CMC; (4) BM with 7 g/L CMC and without yeast tially mutagenic and degenerative, respectively (Leslie and powder; (5) 1% sucrose (saccharose) in sterile distilled Summerell 2006; Seifert 2006; Wing et al. 1995). In water(SDW);and(6)SDWonly.BMwasMgSO4·7H2O, particular, PDA medium has been shown to induce the 0.5 g/L; NH4NO3 1g/L;KH2PO4, 1 g/L; yeast powder, formation of irregularly sized and shaped conidia. More- 1 g/L (Eudes et al. 2001). Liquid media inoculated with F. over, CMC based-medium is relatively costly, while natural graminearum mycelial plugs were incubated at 23°C on a products require complex steps in media preparation and shaker (230 rpm) for up to 2 weeks. The number of have only a slight effect on conidia production (Leslie and macroconidia per milliliter produced in the different media Summerell 2006). The objectives of this study were (1) to was assessed with a hemocytometer under Carl Zeiss use a sucrose-water suspension as an environmentally Axioscop2 with a Carl Zeiss AxioCAm IcC1 camera 3, 7, friendly and inexpensive method of stimulating rapid 10 and 14 days after inoculation (Zeiss, Jena, Germany). macroconidia formation in both F. graminearum chemo- Each treatment had three replicates and the experiment types; (2) to assess the germination rate, a good indicator of was repeated twice. macroconidia viability or infection capacity (Harris 2005); and (3) to investigate the effect of liquid media on the Macroconidia germination profile of mycotoxins. Germination assays on F. graminearum macroconidia were performed in U-bottom microplates (96-well) using potato Materials and methods dextrose broth (PDB) (Difco, Becton Dickinson). On day 7, macroconidia suspensions from BM amended with 1 g/L Fungal isolates and growth CMC and 1% sucrose medium for all six F. graminearum isolates were mixed with PDB in microplates at a ratio of Selected F. graminearum 3 and 15 (3- and 15-ADON) 1:1 (1 part macroconidia suspension: 1 part PDB). isolates were obtained from various sources as summarized Inoculated microplates were incubated at 23°C in darkness in Table 1. Two chemotypes were identified according to for an additional day prior to examination of spore the procedure outlined in Von der Ohe et al. (2010). F. germination. The percentage of germinated Fusarium graminearum isolates were grown and maintained on PDA macroconidia was obtained by scoring the spores in the (Difco, Becton Dickinson, Sparks, MD) at 4°C in darkness macroconidia suspension from microplates using 200× and for 1 week prior to the study. 400× objectives of Carl Zeiss Axioskop2 microscope and systematically choosing 50 macroconidia, starting at the top Macroconidia production right corner and continuing to count until 50. There were three replicates per treatment, and experiments were Mycelial plugs (~0.5 cm2) from the actively growing repeated twice. A macroconidium was considered germi- zone were cut and transferred into six different liquid nated only when the germ tubes exceeded half the length of media: (1) basal medium (BM) with 1 g/L CMC (Sigma, the macroconidium (approximately 10 μm). Germinated macroconidia were counted and recorded as a percentage of the total macroconidia number. Table 1 Fusarium graminearum 3- and 15-ADON (acetyldeoxynivalenol- producer) isolates used in this study Trichothecene mycotoxin extraction F. graminearum isolate Accession no. Sourcea For mycotoxin analyses, only treatments with macroconidia 3-ADON chemotypes SMCD 2243 SMCD Saskatoon were selected for further studies. DON, ZEA, 3-ADON and wrs 2070 AAFC Winnipeg 15-ADON mycotoxins from treatments with macroconidia SIA-06-3 CCFC Guelph were extracted from the different liquid media on day 14 15-ADON chemotypes wrs 2085 AAFC Winnipeg using three 10 mL volumes of ethyl acetate (Vasavada and wrs 2073 AAFC Winnipeg Hsieh 1987). Samples were shaken vigorously, sonicated on M2-06-2 CCFC Guelph ice, and allowed to stand for 5 min for separation of phases. The organic phase was siphoned off and passed through a AAFC Agriculture and Agri-Food Canada, Winnipeg, MN, Canada sodium sulfate to remove water. The solvent was allowed to (Dr. A. Tekauz). CCFC University of Guelph Collection, Guelph, ON, evaporate at room temperature (23°C) for 3 days. The Canada (Dr. Lily Tamburic-Ilincic); SMCD Saskatchewan Microbial Collection and Database, University of Saskatchewan, Saskatoon, SK, residue was then re-dissolved in 2 mL acetonitrile for Canada (Dr. V. Vujanovic). HPLC analyses. Ann Microbiol (2012) 62:965–971 967 HPLC analyses and 10, with the exception of the strain wrs 2085 on day 3 (Table 2). Basal media supplemented with CMC triggered Standard trichothecene mycotoxins of DON, ZEA, 3- macroconidia production in some but not all F. graminea- ADON and 15-ADON were purchased from Sigma (HPLC rum isolates (Table 2). A high variation in abundance of grade; Oakville, ON). Mycotoxins extracted from different macroconidia was observed in all isolates tested and at all treatments were analyzed with a Water’s 2695 HPLC CMC concentrations. In contrast, 1% sucrose-water medi- system with: 250×4.60 mm, Luna 5 μ C18 (2) 100A um induced a relatively stable frequency, whereas the column (Phenomenex, Torrance, CA) and a photodiode- number of macroconidia (105/mL) ranged from 74 to 92 array (PDA) detector was used with an isocratic solvent in 3-ADON, and 41 to 64 in 15-ADON isolates by day 7 system [methanol: water-methanol containing 5% (v/v) (Table 2). After 7 days of incubation, macroconidia (90:10) ratio]. The PDA detector measured the UV produced by most F. graminearum isolates in 1% sucrose spectrum (190–500 nm). Samples were dissolved in medium began to germinate (Fig. 1). A subsequent macro- acetonitrile and 10 μL loaded onto the column using an conidia formation, statistically insignificant in terms of automatic injector. Mycotoxins were eluted with solvent or macroconidia abundance (P<0.05), was found on day 7 and mobile phase at a rate of 0.75 mL min−1 for 25 min. 14. No germination of macroconidia was detected in other Standard curves for respective mycotoxins were generated media at the incubation times tested in this study. based on five different concentrations of pure toxins, and Solid sucrose medium containing 15% agar allowed a absorbances obtained from HPLC analyses. reduced, but stable, macroconidia production in comparison with 1% sucrose-water broth, which was retained for Statistical analyses further assays.
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