Abstract
Fusarium species are common fungal pathogens of maize. Fusarium graminearum and Fusarium verticillioides, among others, can cause maize ear rot, and they are also mycotoxin producers. The aims of this work were to determine the frequency and diversity of Fusarium species in Uruguayan maize kernels, evaluate the toxigenic potential of the isolates, determine toxin contamination levels on freshly harvested grain, and assess the sensitivity of main Fusarium species against fungicides. Fusarium verticillioides was the most frequent species isolated, followed by Fusarium graminearum sensu stricto. Of F. verticillioides isolates studied for fumonisin production, 72% produced fumonisin B1 and 32% fumonisin B2. Considering in vitro toxin production by F. graminearum sensu stricto isolates, deoxynivalenol was the main toxin produced, followed by zearalenone and nivalenol. Fumonisins were the most frequently found toxins on freshly harvested maize samples (98% in 2018 and 86% in 2019), and also, fumonisin B1 was the toxin with highest concentration in both years studied (4860 µg/kg in 2018 and 1453 µg/kg in 2019). Deoxynivalenol and zearalenone were also found as contaminants. Metconazole and epoxiconazole were the most effective fungicides tested on F. verticillioides isolates. Fusarium graminearum sensu stricto isolates also were more sensitive to metconazole compared to other fungicides; nevertheless, epoxiconazole was less efficient in controlling this species. This is the first study that reports Fusarium species and mycotoxin contamination levels associated with maize grain in Uruguay. Its detection is the main step to develop management strategies in order to minimize fungal infection in maize crops.
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References
Aguín O, Cao A, Pintos C, Santiago R, Mansilla P, Butrón A (2014) Occurrence of Fusarium species in maize kernels grown in northwestern Spain. Plant Pathol 63:946–951
Alexander NJ, Proctor RH, McCormick SP (2009) Genes, gene clusters, and biosynthesis of trichothecenes and fumonisins in Fusarium. Toxin Rev 28:198–215
Almeida AP, Fonseca H, Fancelli AL, Direito GM, Ortega EM, Corrêa B (2002) Mycoflora and fumonisin contamination in Brazilian corn from sowing to harvest. J Agric Food Chem 50:3877–3882
Alvarez CL, Azcarate MP, Pinto VF (2009) Toxigenic potential of Fusarium graminearum sensu stricto isolates from wheat in Argentina. Int J Food Microbiol 135:131–135
Amarasinghe C, Tamburic-Ilincic L, Gilbert J, Brûlé-Babel AL, Fernando WG (2013) Evaluation of different fungicides for control of Fusarium head blight in wheat inoculated with 3ADON and 15ADON chemotypes of Fusarium graminearum in Canada. Can J Plant Pathol 35:200–208
AOAC International Official Methods of Analysis of AOAC International (2019)
Astolfi P, Reynoso MM, Ramirez ML, Chulze SN, Alves TCA, Tessmann DJ, Del Ponte EM (2012) Genetic population structure and trichothecene genotypes of Fusarium graminearum isolated from wheat in southern Braz. J Plant Physiol 61:289–295
Baldwin TT, Zitomer NC, Mitchell TR, Zimeri AM, Bacon CW, Riley RT, Glenn AE (2014) Maize seedling blight induced by Fusarium verticillioides: accumulation of fumonisin B1 in leaves without colonization of the leaves. J Agric Food Chem 62:2118–2125
Bankole S, Mabekoje O (2004) Occurrence of aflatoxins and fumonisins in pre-harvest maize from South-Western Nigeria. Food Addit Contam 21:251–255
Udovicki B, Audenaert K, De Saeger S, Rajkovic A (2018) Overview on the mycotoxins incidence in Serbia in the period 2004–2016. Toxins (basel) 10:279
Barros G, Alaniz Zanon M, Abod A, Oviedo M, Ramirez ML, Reynoso MM, Torres A, Chulze S (2012) Natural deoxynivalenol occurrence and genotype and chemotype determination of a field population of the Fusarium graminearum complex associated with soybean in Argentina. Food Add Cont 29:293–303
Barroso V, Rocha L, Reis T, Reis G, Duarte A, Michelotto M, Correa B (2017) Fusarium verticillioides and fumonisin contamination in Bt and non-Bt maize cultivated in Brazil. Mycotoxin Res 33:121–127
Becher R, Hettwer U, Karlovsky P, Deising HB, Wirsel SG (2010) Adaptation of Fusarium graminearum to tebuconazole yielded descendants diverging for levels of fitness, fungicide resistance, virulence, and mycotoxin production. Phytopathology 100:444–453
Boutigny AL, Ward TJ, Ballois N, Iancu G, Ioos R (2014) Diversity of the Fusarium graminearum species complex on French cereals. Eur J Plant Pathol 138:133–148
Brent KJ, Hollomon DW (2007) Fungicide resistance: the assessment of risk. In Global Crop Protection Federation. (FRAC Monograph No. 2.); The Fungicide Resistance Action Committee Brussels: Brussels, Belgium
Castañares E, Martínez M, Cristos D, Rojas D, Lara B, Stenglein S, Dinolfo M (2019) Fusarium species and mycotoxin contamination in maize in Buenos Aires province, Argentina. Eur J Plant Pathol 155:1265–1275
Chandler EA, Simpson DR, Thomsett MA, Nicholson P (2003) Development of PCR assays to Tri7 and Tril3 trichothecene biosynthetic genes, and characterization of chemotypes of Fusarium. Physiol Mol Plant Pathol 62:355–367
Chen CJ, Wang JX, Luo QQ, Yuan SK, Zhou MG (2007) Characterization and fitness of carbendazim-resistant strains of Fusarium graminearum (wheat scab). Pest Manag Sci 63:1201–1207
Choi J-H, Lee S, Nah J-Y, Kim H-K, Paek J-S, Lee S, Ham H, Kee Hong S, Yunb S-H, Lee T (2018) Species composition of and fumonisin production by the Fusarium fujikuroi species complex isolated from Korean cereals. Int J Food Microbiol 267:62–69
Codex Alimentarius Commission (CAC) (2019). General standard for contaminants and toxins in food and feed. CXS 193–1995. 2019. Available from: https://www.fao.org/fao-who-codexalimentarius/sh-proxy/en/?lnk=1&url=https%253A%252F%252Fworkspace.fao.org%252Fsites%252Fcodex%252FStandards%252FCXS%2B193-1995%252FCXS_193e.pdf
Del Ponte EM, Moreira GM, Ward TJ et al (2022) Fusarium graminearum species complex: a bibliographic analysis and web-accessible database for global mapping of species and trichothecene toxin chemotypes. Phytopathology 112:741–751
Del Ponte EM, Spolti P, Ward TJ, Gomes LB, Nicolli CP, Kuhnem PR, Silva CN, Tessmann DJ (2015) Regional and field-specific factors affect the composition of Fusarium head blight pathogens in subtropical no-till wheat agroecosystem of Brazil. Phytopathology 105:246–254
Desjardins AE, Proctor RH (2011) Genetic diversity and trichothecene chemotypes of the Fusarium graminearum clade isolated from maize in Nepal and identification of a putative new lineage. Fungal Biol 115:38–48
Di Rienzo JA, Casanoves F, Balzarini MG, González L, Robledo CW (2011) InfoStat (versión 2011). FCA, Universidad Nacional de Córdoba, Argentina, Grupo InfoStat
Duan Y, Zhang X, Ge C, Wang Y, Cao J, Jia X, Wang J, Zhou M (2014) Development and application of loop-mediated isothermal amplification for detection of the F167Y mutation of carbendazim-resistant isolates in Fusarium graminearum. Sci Rep 4:Article 7094
Fallahi M, Saremi H, Javan-Nikkhah M, Somma S, Haidukowski M, Logrieco AF, Moretti A (2019) Isolation, molecular identification and mycotoxin profile of fusarium species isolated from maize kernels in Iran. Toxins 11:297
FDA – US Food and Drug Administration (2010). Guidance for industry and FDA: advisory levels for deoxynivalenol (DON) in finished wheat products for human consumption and grains and grain by-products used for animal feed. Available from: https://www.fda.gov/regulatory-information/search-fda-guidance-documents/guidance-industry-and-fda-advisory-levels-deoxynivalenol-don-finished-wheat-products-human
Finney DJ (1952) Probit Analysis (2nd Ed). J Inst Act 783: 388–390
Garrido CE, Hernández Pezzani C, Pacin A (2012) Mycotoxins occurrence in Argentina’s maize (Zea mays L.) from 1999 to 2010. Food Control 25:660–665
Garmendia G, Pattarino L, Negrin C, Martinez-Silveira A, Pereyra S, Ward TJ, Vero S (2018b) Species composition, toxigenic potential and aggressiveness of Fusarium isolates causing Head blight of barley in Uruguay. Food Microbiol 76:426–433
Umpiérrez-Failache M, Garmendia G, Pereyra S, Rodríguez-Haralambides A, Ward T, Vero S (2013) Regional differences in species composition and toxigenic potential among Fusarium head blight isolates from Uruguay indicate a risk of nivalenol contamination in new wheat production areas. Int J Food Microbiol 166:135–140
Garmendia G, Umpierrez-Failache M, Ward TJ, Vero S (2018a) Development of a PCR-RFLP method based on the transcription elongation factor 1-α gene to differentiate Fusarium graminearum from other species within the Fusarium graminearum species complex. Food Microbiol 70:286–332
GB13078-2017 Hygienic Standard for Feeds (2017) https://apps.fas.usda.gov/newgainapi/api/report/downloadreportbyfilename?filename=Hygienic%20Standard%20for%20Feeds_Beijing_China%20-%20Peoples%20Republic%20of_10-24-10.1007/s12550-023-00498-y2017.pdf
Geiser DM, del Mar J-G, Kang S, Makalowska I, Veeraraghavan N, Ward TJ, Zhang N, Kuldau GA, O’donnell K, (2004) FUSARIUM-ID vol 1.0: A DNA sequence database for identifying Fusarium. Euro J Plant Pathol 110:473–479
Gelderblom WC, Jaskiewicz K, Marasas WF, Thiel PG, Horak RM, Vleggaar R, Kriek NP (1988) Fumonisins–novel mycotoxins with cancer-promoting activity produced by Fusarium moniliforme. Appl Environ Microbiol 54(7):1806–1811
Ivić D, Sever Z, Kumanovska B (2011) In vitro sensitivity of Fusarium graminearum, F. avenaceum and F. verticillioides to carbendazim, tebuconazole, flutriafol, metconazole and prochloraz. Pestic Phytomed (belgrade) 26:35–42
Yli-Mattila T, Sundheim L (2022) Fumonisins in African Countries Toxins 14:419
Kuhnem P, Ward T, Silva C, Spolti P, Ciliato M, Tessmann D, Del Ponte E (2016) Composition and toxigenic potential of the Fusarium graminearum species complex from maize ears, stalks and stubble in Brazil. Plant Pathol 65:1185–1191
Lanza F, Zambolim L, Veras da Costa R, Vieira Queiroz V, Cota L, da Silva D, Coelho de Souza A, Fontes Figueiredo J (2014) Prevalence of fumonisin-producing Fusarium species in Brazilian corn grains. Crop Prot 65:232–237
Lee J, Kim H, Jeon J-J, Kim H-S, Zeller K, Carter L, Leslie J, Lee Y-W (2012) Population Structure of and Mycotoxin Production by Fusarium graminearum from Maize in South Korea. Appl Environ Microbiol 78:2161–2167
Leslie JF, Summerell BA (2006) The Fusarium laboratory manual. Ames, IA, USA: Blackwell Professional
Liu SM, Chen Y, Yu JJ, Chen CJ, Wang JX, Zhou MG (2010) Transfer of the beta-tubulin gene of Botrytis cinerea with resistance to carbendazim into Fusarium graminearum. Pest Manag Sci 66:482–489
Logrieco A, Mule G, Moretti A, Bottalico A (2002) Toxigenic Fusarium species and mycotoxins associated with maize ear rot in Europe. Eur J Plant Pathol 108:597–609
Maragos C (2010) Zearalenone occurrence and human exposure. World Mycotoxin J 3:369–383
Marasas WF, Kellerman TS, Gelderblom WC, Coetzer JA, Thiel PG, van der Lugt JJ (1988) Leukoencephalomalacia in a horse induced by fumonisin B1 isolated from Fusarium moniliforme. Onderstepoort J Vet Res 55(4):197–203
Marín P, De Ory A, Cruz A, Magan N, González-Jaén MT (2013) Potential effects of environmental conditions on the efficiency of the antifungal tebuconazole controlling Fusarium verticillioides and Fusarium proliferatum growth rate and fumonisin biosynthesis. Int J Food Microbiol 165:251–258
Masiello M, Somma S, Ghionna V, Logrieco A, Moretti A (2019) In vitro and in field response of different fungicides against Aspergillus flavus and Fusarium species causing ear rot disease of maize. Toxins 11:11
van der Westhuizen L, Shepard G, Scussel V, Costa L, Vismer H, Marasas RJ, W, (2003) Fumonisin contamination and Fusarium incidence in corn from Santa Catarina. Brazil J Agric Food Chem 51:5574–5578
McCormick SP, Stanley AM, Stover NA, Alexander N (2011) Trichothecenes: from simple to complex mycotoxins. Toxins 3:802–814
Mendes de Souza M, Sulyok M, Freitas-Silva O, Soares S, Brabet C, Machinski M, Leiko B, Azevedo E, Krska R, Schuhmache R (2013) Cooccurrence of mycotoxins in maize and poultry feeds from Brazil by liquid chromatography/tandem mass spectrometry. Sci World J 2013:427369
Methol M (2021) Maíz y sorgo: situación y perspectivas. In Anuario de OPYPA, pp193. Available from: https://www.gub.uy/ministerio-ganaderia-agricultura-pesca/comunicacion/publicaciones/anuario-opypa-2021/anuario-opypa-2021
MGAP, Resolución S/N/001 (2001) Límites máximos de DON en alimentos para animales. https://www.gub.uy/ministerio-ganaderia-agricultura-pesca/institucional/normativa/resolucion-sn001-limitesmaximos-don-alimentos-para-animales
Mulè G, Susca A, Stea G, Moretti A (2004) Specific detection of the toxigenic species Fusarium proliferatum and F. oxysporum from asparagus plants using primers based on calmodulin gene sequences. FEMS Microbiol Lett 230:235–240
Munkvold GP, Desjardins AE (1997) Fumonisins in maize: can we reduce their occurrence? Plant Dis 82:556–565
Munkvold GP (2003) Epidemiology of Fusarium diseases and their mycotoxins in maize ears. Eur J Plant Pathol 109:705–713
O’Donnell K, Cigelnick E, Nirenberg HI (1998) Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia 90:465–493
Pan D, Calero N, Mionetto A, Bettucci L (2013) Trichothecene genotypes of Fusarium graminearum from wheat in Uruguay. Int J Food Microbiol 162:120–123
Pan D, Mionetto A, Calero N, Reynoso MM, Torres A, Bettucci L (2016) Population genetic analysis and trichothecene profiling of Fusarium graminearum from wheat in Uruguay. Genet Mol Res 15:1–11
Pasquali M, Beyer M, Logrieco A et al (2016) A European database of Fusarium graminearum and F. culmorum trichothecene genotypes. Front Microbiol 7:406. https://doi.org/10.3389/fmicb.2016.00406
Piñero S, Silva G, Scott P, Lawrence G, Stack M (1997) Fumonisin levels in Uruguayan corn products.J. Assoc off Anal Chem Int 80:825–829
Ward T, Bielawski JP, Kistler HC, Sullivan E, O’Donnell K (2002) Ancestral polymorphism and adaptive evolution in the trichothecene mycotoxin gene cluster of phytopathogenic Fusarium. Proc Natl Acad Sci USA 99:9278–9283
Pestka JJ (2010) Deoxynivalenol: Mechanisms of action, human exposure, and toxicological relevance. Arch Toxicol 84:663–679
Picot A, Barreau C, Pinson-Gadais L, Caron D, Lannou C, Richard-Forget F (2010) Factors of the Fusarium verticillioides-maize environment modulating fumonisin production. Crit Rev Microbiol 36:221–231
Pirgozliev SR, Edwards SG, Hare MC, Jenkinson P (2002) Effect of dose rate of azoxystrobin and metconazole on the development of Fusarium head blight and the accumulation of deoxynivalenol (DON) in wheat grain. Eur J Plant Pathol 108:469–478
Zhou D, Wang X, Chen G, Sun S, Yang Y, Zhu Z, Duan C (2018) The major Fusarium species causing maize ear and kernel rot and their toxigenicity in Chongqing. China Toxins 10:90
Ponce-García N, Serna-Saldivar SO, Garcia-Lara S (2018) Fumonisins and their analogues in contaminated corn and its processed foods - a review. Food Addit Contam Part A 35:2183–2203
QinP XuJ, Jiang Y, Hu L, van der Lee T, Waalwijk C, Zhang W, Xu X (2020) Survey for toxigenic Fusarium species on maize kernels in China. World Mycotoxin J 13:213–223
Reddy K, Salleh B, Saad B, Abbas H, Abel C, Shier W (2010) An overview of mycotoxin contamination in foods and its implications for human health. Toxin Rev 29:3–26
Reynoso MM, Ramirez ML, Torres A, Chulze S (2011) Trichothecene genotypes and chemotypes in Fusarium graminearum strains isolated from wheat in Argentina. Int J Food Microbiol 145:444–448
Salay E, Mercadante A (2002) Mycotoxins in Brazilian corn for animal feed: occurrence and incentives for the private sector to control the level of contamination. Food Control 13:87–92
Sampietro D, ApudI G, BelizánI M, VattuoneI M, Catalán C (2013) Toxigenic potential of Fusarium graminearum isolated from maize of northwest Argentina. Braz J Microbiol 44:2
Sampietro DA, Díaz CG, González V, Vattuone MA, Ploper LD, Catalán CA, Ward T (2011) Species diversity and toxigenic potential of Fusarium graminearum complex isolates from maize fields in northwest Argentina. Int J Food Microbiol 145:359–364
Scauflaire J, Mahieu O, Louvieaux J, Foucart G, Renard F, Munaut F (2011) Biodiversity of Fusarium species in ears and stalks of maize plants in Belgium. Eur J Plant Pathol 131:59–66
Scoz LB, Astolfi P, Reartes DS, Schmale DG, Moraes MG, Del Ponte EM (2009) Trichothecene mycotoxin genotypes of Fusarium graminearum sensu stricto and Fusarium meridionale in wheat from southern Brazil. Plant Pathol 58:344–351
Scussel V, Savi G, Freitas Costas L, Mendonça J, Manfio D, Bittencourt K, Aguiar K, Stein S (2014) Fumonisins in corn (Zea mays L.) from Southern Brazil. Food Addit Contam: Part B 7:151–155
Spolti P, Del Ponte EM, Dong Y, Cummings JA, Bergstrom GC (2014) Triazole sensitivity in a contemporary population of Fusarium graminearum from New York wheat and competitiveness of a tebuconazole-resistant isolate. Plant Dis 98:607–613
Stumpf R, dos Santos J, Gomes L, Silva C, Tessmann D, Ferreira F, Machinski Junior M, Del Ponte E (2013) Fusarium species and fumonisins associated with maize kernels produced in Rio Grande do Sul State for the 2008/09 and 2009/10 growing seasons. Braz J Microbiol 44:89–95
Sundheim L, Tsehaye H (2015) Fumonisin in Zambia and neighboring countries in a changing climate. Adv Environ Res 39:69–84
Sundlof SF, Strickland C (1986) Zearalenone and zeranol: potential residue problems in livestock. Vet Hum Toxicol 28:242–250
Tateishi H, Miyake T, Mori M, Kimura R, Sakuma Y, Saishoji T (2010) Sensitivity of Japanese Fusarium graminearum species complex isolates to metconazole. J Pestic Sci 35:419–430
Tava V, Prigitano A, Cortesi P, Esposto MC, Pasquali M (2021) Fusarium musae from diseased bananas and human patients: susceptibility to fungicides used in clinical and agricultural settings. J Fungi (basel) 7:784
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This work was financed by the Agencia Nacional de Investigación e Innovación (ANII), project number FSA-I-2017–1-139531.
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del Palacio, A., Corallo, B., Simoens, M. et al. Major Fusarium species and mycotoxins associated with freshly harvested maize grain in Uruguay. Mycotoxin Res 39, 379–391 (2023). https://doi.org/10.1007/s12550-023-00498-y
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DOI: https://doi.org/10.1007/s12550-023-00498-y