Biological control as a strategy to reduce the impact of mycotoxins in peanuts, grapes and cereals in Argentina

Mycotoxins including aflatoxins, deoxynivalenol, fumonisins and ochratoxin A are among the main fungal secondary metabolites detected as natural contaminants in South America in different commodities such as peanuts (aflatoxins), cereals (deoxynivalenol and fumonisins) or grapes (ochratoxin A). Different strategies including crop rotation, tillage practices, fungicide application and planting less susceptible cultivars are used in order to reduce the impact of these mycotoxins in both food and feed chains. The development of fungicide resistance in many fungal pathogens as well as rising of public concern on the risks associated with pesticide use led to the search for alternative environmentally friendly methods. Biological control of plant pathogens and toxigenic fungi offers an alternative that can complement chemical control in the frame of an integrated pest management to reduce the impact of mycotoxins in the food and feed chains. The advances made in Argentina on reducing the impact of toxigenic fungi and mycotoxins in peanut, grapes and cereals using the biocontrol strategy are summarised. Native bacteria, yeasts and filamentous fungi have been selected to evaluate them as potential biocontrol agents. Field trials showed that Bacillus subtilis RC 218 and Brevibacillus sp. RC 263 were effective at reducing deoxynivalenol accumulation in wheat. The application of Clonostachys rosea isolates on wheat stubble reduced Fusarium colonisation on the stubble. Bacillus amyloliquefaciens and Microbacterium oleovorans showed good activity to control both Fusarium verticillioides growth and the accumulation of fumonisins at pre-harvest stage in maize. Control of toxigenic Aspergillus flavus and aflatoxin accumulation in peanuts was achieved using a native atoxigenic Aspergillus flavus strain based on competitive exclusion of the toxigenic strains. Kluyveromyces thermotolerans strains were used as biocontrol agents to reduce the impact of Aspergillus section Nigri and ochratoxin A accumulation in grapes.

[1]  T. Shantha.  Fungal degradation of aflatoxin B1. , 1999, Natural toxins.

[2]  S. Chulze,et al.  Evaluation of potential biocontrol agent for aflatoxin in Argentinean peanuts. , 2013, International journal of food microbiology.

[3]  R. J. Cole,et al.  Aflatoxin reduction in corn through field application of competitive fungi. , 1999, Journal of food protection.

[4]  N. Magan,et al.  Accumulation of the betaine and ectoine in osmotic stress adaptation of biocontrol agents against Fusarium verticillioides in maize , 2012 .

[5]  M. L. Ramírez,et al.  Potential biocontrol agents for Fusarium head blight and deoxynivalenol production in wheat , 2007 .

[6]  S. Chulze,et al.  Strategies to reduce mycotoxin levels in maize during storage: a review , 2010, Food additives & contaminants. Part A, Chemistry, analysis, control, exposure & risk assessment.

[7]  S. Edwards,et al.  Mode of antagonism of Brevibacillus brevis against Botrytis cinerea in vitro , 2001, Journal of applied microbiology.

[8]  Lubos Polerecky,et al.  Oxygenic photosynthesis as a protection mechanism for cyanobacteria against iron-encrustation in environments with high Fe2+ concentrations , 2014, Front. Microbiol..

[9]  J. Dorner,et al.  Development and commercial use of afla-Guard®, an aflatoxin biocontrol agent , 2006, Mycotoxin Research.

[10]  Ming-guo Zhou,et al.  A major gene for resistance to carbendazim, in field isolates of Gibberella zeae , 2005 .

[11]  S. Chulze,et al.  Control of Ochratoxin A Production in Grapes , 2012, Toxins.

[12]  J. Leslie,et al.  Population genetic structure of Gibberella zeae isolated from wheat in Argentina , 2007, Food additives and contaminants.

[13]  J. Köhl,et al.  Potential of fungal antagonists for biocontrol of Fusarium spp. in wheat and maize through competition in crop debris , 2005 .

[14]  N. Magan,et al.  Impact of mild heat treatments on induction of thermotolerance in the biocontrol yeast Candida sake CPA‐1 and viability after spray‐drying , 2008, Journal of applied microbiology.

[15]  M. Mcmullen,et al.  A Unified Effort to Fight an Enemy of Wheat and Barley: Fusarium Head Blight. , 2012, Plant disease.

[16]  G. Bergstrom,et al.  Biological control of Fusarium graminearum. , 2003 .

[17]  J. Gilbert,et al.  Overview of some recent research developments in fusarium head blight of wheat , 2013 .

[18]  S. Chulze,et al.  Molecular characterization of Aspergillus section Flavi isolates collected from peanut fields in Argentina using AFLPs , 2007, Journal of applied microbiology.

[19]  M. Etcheverry,et al.  Field Studies on the Relationship between Fusarium verticillioides and Maize (Zea mays L.): Effect of Biocontrol Agents on Fungal Infection and Toxin Content of Grains at Harvest , 2011 .

[20]  K. Ehrlich.  Non-aflatoxigenic Aspergillus flavus to prevent aflatoxin contamination in crops: advantages and limitations , 2014, Front. Microbiol..

[21]  G. Salerno,et al.  Occurrence of Different Species of Fusarium from Wheat in Relation to Disease Levels Predicted by a Weather-Based Model in Argentina Pampas Region , 2011, Mycopathologia.

[22]  R. H.,et al.  Use of Bacillus subtilis as biocontrol agent . VI . Phytohormone-like action of culture filtrates prepared from plant growth-promoting Bacillus amyloliquefaciens FZB 24 , FZB 42 , FZB 45 and Bacillus subtilis FZB 37 , 2005 .

[23]  N. Magan,et al.  Accumulation of the compatible solutes, glycine–betaine and ectoine, in osmotic stress adaptation and heat shock cross‐protection in the biocontrol agent Pantoea agglomerans CPA‐2 , 2005, Letters in applied microbiology.

[24]  P. Battilani,et al.  Phyllosphere grapevine yeast Aureobasidium pullulans reduces Aspergillus carbonarius (sour rot) incidence in wine-producing vineyards in Greece , 2008 .

[25]  S. Vaughn,et al.  Cyclic lipopeptide profile of three Bacillus subtilis strains; antagonists of Fusarium head blight , 2011, The Journal of Microbiology.

[26]  S. Chulze,et al.  Biocontrol of Bacillus subtilis against Fusarium verticillioides in vitro and at the maize root level. , 2005, Research in microbiology.

[27]  Lichao Sun,et al.  Antagonistic Action of Bacillus subtilis Strain SG6 on Fusarium graminearum , 2014, PloS one.

[28]  P. Battilani,et al.  Review on pre- and post-harvest management of peanuts to minimize aflatoxin contamination , 2014 .

[29]  A. Dalcero,et al.  Biocontrol as a strategy to reduce the impact of ochratoxin A and Aspergillus section Nigri in grapes. , 2011, International journal of food microbiology.

[30]  M. Etcheverry,et al.  Production of Fusarium verticillioides biocontrol agents, Bacillus amyloliquefaciens and Microbacterium oleovorans, using different growth media: evaluation of biomass and viability after freeze-drying , 2012, Food additives & contaminants. Part A, Chemistry, analysis, control, exposure & risk assessment.

[31]  J. Sørensen,et al.  Pseudomonas frederiksbergensis sp. nov., isolated from soil at a coal gasification site. , 2000, International journal of systematic and evolutionary microbiology.

[32]  S. E. Tjamos,et al.  Aspergillus niger and Aspergillus carbonarius in Corinth Raisin and Wine‐Producing Vineyards in Greece: Population Composition, Ochratoxin A Production and Chemical Control , 2004 .

[33]  M. Etcheverry,et al.  Impact of bacterial biological control agents on fumonisin B1 content and Fusarium verticillioides infection of field-grown maize , 2010 .

[34]  Yanni Yin,et al.  Biological control of aflatoxin contamination of crops , 2008, Journal of Zhejiang University SCIENCE B.

[35]  M. Etcheverry,et al.  Biological control of fumonisins production in maize at field level. , 2013 .

[36]  J. Pitt,et al.  Mycotoxins in Australia: biocontrol of aflatoxin in peanuts , 2006, Mycopathologia.

[37]  C. Magnoli,et al.  Fungal and mycotoxin contamination in Bt maize and non-Bt maize grown in Argentina. , 2009 .

[38]  P. Battilani,et al.  Biological Interactions to Select Biocontrol Agents Against Toxigenic Strains of Aspergillus flavus and Fusarium verticillioides from Maize , 2009, Mycopathologia.

[39]  M. Boehm,et al.  Selection and evaluation of the potential of choline-metabolizing microbial strains to reduce Fusarium head blight , 2006 .

[40]  J. Köhl,et al.  Biocontrol and population dynamics of Fusarium spp. on wheat stubble in Argentina , 2013 .

[41]  S. Baker,et al.  New Insight into the Ochratoxin A Biosynthetic Pathway through Deletion of a Nonribosomal Peptide Synthetase Gene in Aspergillus carbonarius , 2012, Applied and Environmental Microbiology.

[42]  J. Dorner,et al.  Separate and combined applications of nontoxigenic Aspergillus flavus and A. parasiticus for biocontrol of aflatoxin in peanuts , 2007, Mycopathologia.

[43]  G. Schatzmayr,et al.  Global occurrence of mycotoxins in the food and feed chain: facts and figures , 2013 .

[44]  P. Ojiambo,et al.  Field efficacy of a mixture of atoxigenic Aspergillus flavus Link:Fr vegetative compatibility groups in preventing aflatoxin contamination in maize (Zea mays L.) , 2014 .

[45]  L. Bullerman,et al.  Anti-aflatoxigenic activity of Lactobacillus casei pseudoplantarum. , 1997, International journal of food microbiology.

[46]  M. L. Ramírez,et al.  Osmotic stress adaptation, compatible solutes accumulation and biocontrol efficacy of two potential biocontrol agents on Fusarium head blight in wheat. , 2009 .

[47]  M. Schmidt-Heydt,et al.  Effect of Kluyveromyces thermotolerans on polyketide synthase gene expression and ochratoxin accumulation by Penicillium and Aspergillus , 2013 .

[48]  L. Osborne,et al.  Fusarium head blight biological control with Lysobacter enzymogenes strain C3 , 2006 .

[49]  N. Magan,et al.  Impact of environmental factors and fungicides on growth and deoxinivalenol production by Fusarium graminearum isolates from Argentinian wheat , 2004 .

[50]  Cl Wilson,et al.  BIOLOGICAL CONTROL OF POSTHARVEST DISEASES OF FRUITS AND VEGETABLES: AN EMERGING TECHNOLOGY* , 1989 .

[51]  G. Scorzetti,et al.  Cryptococcus nodaensis sp nov, a yeast isolated from soil in Japan that produces a salt-tolerant and thermostable glutaminase , 1999, Journal of Industrial Microbiology and Biotechnology.

[52]  P. Cotty.  Influence of field application of an atoxigenic strain of Aspergillus flavus on the populations of A. flavus infectiing cotton bolls and on the aflatoxin content of cottonseed , 1994 .

[53]  P. Ojiambo,et al.  Evaluation of atoxigenic isolates of Aspergillus flavus as potential biocontrol agents for aflatoxin in maize , 2008, Food additives & contaminants. Part A, Chemistry, analysis, control, exposure & risk assessment.

[54]  S. Vogelgsang,et al.  On-farm experiments over 5 years in a grain maize/winter wheat rotation: effect of maize residue treatments on Fusarium graminearum infection and deoxynivalenol contamination in wheat , 2011, Mycotoxin Research.

[55]  R. Castoria,et al.  Strains of Aureobasidium pullulans can lower ochratoxin A contamination in wine grapes. , 2008, Phytopathology.

[56]  R. J. Cole,et al.  Effect of application of nontoxigenic strains of Aspergillus flavus and A. parasiticus on subsequent aflatoxin contamination of peanuts in storage , 2002 .

[57]  L. Covarelli,et al.  Effect of prothioconazole-based fungicides on Fusarium head blight, grain yield and deoxynivalenol accumulation in wheat under field conditions , 2012 .

[58]  J. Gilbert,et al.  Evaluation of different fungicides for control of fusarium head blight in wheat inoculated with 3ADON and 15ADON chemotypes of Fusarium graminearum in Canada , 2013 .

[59]  M. Gobbetti,et al.  Antimould activity of sourdough lactic acid bacteria: identification of a mixture of organic acids produced by Lactobacillus sanfrancisco CB1 , 1998, Applied Microbiology and Biotechnology.

[60]  J. Dorner.  Biological Control of Aflatoxin Contamination of Crops , 2004 .

[61]  Á. Mesterházy,et al.  Role of Fungicides, Application of Nozzle Types, and the Resistance Level of Wheat Varieties in the Control of Fusarium Head Blight and Deoxynivalenol , 2011, Toxins.

[62]  D. M. Hinton,et al.  Biological control of Fusarium moniliforme in maize. , 2001, Environmental health perspectives.

[63]  C. Pezzani,et al.  Mycotoxins occurrence in Argentina's maize (Zea mays L.), from 1999 to 2010 , 2012 .

[64]  M. Ongena,et al.  Bacillus lipopeptides: versatile weapons for plant disease biocontrol. , 2008, Trends in microbiology.

[65]  S. Droby,et al.  Evaluation of the use of sodium bicarbonate, potassium sorbate and yeast antagonists for decreasing postharvest decay of sweet cherries , 2001 .

[66]  P. D. Blankenship,et al.  Effect of Inoculum Rate of Biological Control Agents on Preharvest Aflatoxin Contamination of Peanuts , 1998 .

[67]  G. Khodakaramian,et al.  Biological control of Fusarium graminearum on wheat by antagonistic bacteria , 2006 .

[68]  K. Naehrer,et al.  A Three-Year Survey on the Worldwide Occurrence of Mycotoxins in Feedstuffs and Feed , 2012, Toxins.

[69]  F. Doohan,et al.  Bacterium-mediated control of Fusarium head blight disease of wheat and barley and associated mycotoxin contamination of grain , 2009 .

[70]  B. Zimmerli,et al.  Ochratoxin A in table wine and grape-juice: occurrence and risk assessment. , 1996, Food additives and contaminants.

[71]  R. Castoria,et al.  Aureobasidium pullulans (LS-30) an antagonist of postharvest pathogens of fruits: study on its modes of action , 2001 .

[72]  M. Boehm,et al.  Selection and Evaluation of Microorganisms for Biocontrol of Fusarium Head Blight of Wheat Incited by Gibberella zeae. , 2001, Plant disease.

[73]  A. Logrieco,et al.  Isolation of epiphytic yeasts with potential for biocontrol of Aspergillus carbonarius and A. niger on grape. , 2006, International journal of food microbiology.

[74]  V. Cogliano.  International Agency for Research on Cancer (IARC) , 2018, The Grants Register 2019.

[75]  M. Boehm,et al.  Greenhouse and Field Evaluation of Biological Control of Fusarium Head Blight on Durum Wheat. , 2002, Plant disease.

[76]  J. Dorner.  Management and prevention of mycotoxins in peanuts , 2008, Food additives & contaminants. Part A, Chemistry, analysis, control, exposure & risk assessment.

[77]  J. Postma,et al.  Stepwise screening of microorganisms for commercial use in biological control of plant-pathogenic fungi and bacteria , 2011 .

[78]  M. Boehm,et al.  Field testing of antagonists of Fusarium head blight incited by Gibberella zeae , 2004 .

[79]  H. Junge,et al.  Use of Bacillus subtilis as biocontrol agent. IV. Salt-stress tolerance induction by Bacillus subtilis FZB24 seed treatment in tropical vegetable field crops, and its mode of action , 2001 .

[80]  R. J. Cole,et al.  Evaluation of biological control formulations to reduce aflatoxin contamination in peanuts , 2003 .

[81]  R. Zablotowicz,et al.  Comparison of major biocontrol strains of non-aflatoxigenic Aspergillus flavus for the reduction of aflatoxins and cyclopiazonic acid in maize , 2011, Food additives & contaminants. Part A, Chemistry, analysis, control, exposure & risk assessment.

[82]  R. M. Zablotowicz,et al.  Biocontrol of aflatoxin in corn by inoculation with non-aflatoxigenic Aspergillus flavus isolates , 2006 .

[83]  W. M. Dawson,et al.  Field Evaluation of Fungal Competitors of Fusarium culmorum and F. graminearum, Causal Agents of Ear Blight of Winter Wheat, for the Control of Mycotoxin Production in Grain , 2004 .