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      Resilience of Biocontrol for Aflatoxin Minimization Strategies: Climate Change Abiotic Factors May Affect Control in Non-GM and GM-Maize Cultivars

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          Abstract

          There has been significant interest in the development of formulations of non-toxigenic strains of Aspergillus flavus for control of toxigenic strains to reduce the aflatoxin B 1 (AFB 1) contamination of maize. In the future, climate change (CC) abiotic conditions of temperature (+2–4°C), CO 2 (existing levels of 400 vs. 800–1,200 ppb), and drought stress will impact on the agronomy and control of pests and diseases. This study has examined (1) the effect of two-way interacting factors of water activity × temperature on colonization and AFB 1 contamination of maize cobs of different ripening ages; (2) the effect of non-toxigenic strains of A. flavus (50:50 inoculum ratio) on relative control of toxigenic A. flavus and AFB 1 contamination of ripening cobs; (3) post-harvest control of AFB 1 by non-toxigenic strains of A. flavus in non-GM and isogenic GM maize cultivars using the same inoculum ratio; and (4) the impact of three-way interacting CC factors on relative control of AFB 1 in maize cobs pre-harvest and in stored non-GM/GM cultivars. Pre-harvest colonization and AFB 1 production by a toxigenic A. flavus strain was conserved at 37°C when compared with 30°C, at the three ripening stages of cob development examined: milk ripe (R3), dough (R4), and dent (R5). However, pre-harvest biocontrol with a non-toxigenic strain was only effective at the R3 and R4 stages and not at the R5 stage. This was supported by relative expression of the aflR regulatory biosynthetic gene in the different treatments. When exposed to three-way interacting CC factors for control of AFB 1 pre-harvest, the non-toxigenic A. flavus strain was effective at R3 and £4 stages but not at the R5 stage. Post-harvest storage of non-GM and GM cultivars showed that control was achievable at 30°C, with slightly better control in GM-cultivars in terms of the overall inhibition of AFB 1 production. However, in stored maize, the non-toxigenic strains of A. flavus had conserved biocontrol of AFB 1 contamination, especially in the GM-maize cultivars under three-way interacting CC conditions (37°C × 1,000 ppm CO 2 and drought stress). This was supported by the relative expression of the aflR gene in these treatments. This study suggests that the choice of the biocontrol strains, for pre- or post-harvest control, needs to take into account their resilience in CC-related abiotic conditions to ensure that control of AFB 1 contamination can be conserved.

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          Most cited references36

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          Aflatoxin B1 contamination in maize in Europe increases due to climate change

          Climate change has been reported as a driver for emerging food and feed safety issues worldwide and its expected impact on the presence of mycotoxins in food and feed is of great concern. Aflatoxins have the highest acute and chronic toxicity of all mycotoxins; hence, the maximal concentration in agricultural food and feed products and their commodities is regulated worldwide. The possible change in patterns of aflatoxin occurrence in crops due to climate change is a matter of concern that may require anticipatory actions. The aim of this study was to predict aflatoxin contamination in maize and wheat crops, within the next 100 years, under a +2 °C and +5 °C climate change scenario, applying a modelling approach. Europe was virtually covered by a net, 50 × 50 km grids, identifying 2254 meshes with a central point each. Climate data were generated for each point, linked to predictive models and predictions were run consequently. Aflatoxin B1 is predicted to become a food safety issue in maize in Europe, especially in the +2 °C scenario, the most probable scenario of climate change expected for the next years. These results represent a supporting tool to reinforce aflatoxin management and to prevent human and animal exposure.
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            Influence of Field Application of an Atoxigenic Strain ofAspergillus flavuson the Populations ofA. flavusInfecting Cotton Bolls and on the Aflatoxin Content of Cottonseed

            P J Cotty (1994)
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              Effects of elevated [CO2] on maize defence against mycotoxigenic Fusarium verticillioides

              Maize is by quantity the most important C4 cereal crop; however, future climate changes are expected to increase maize susceptibility to mycotoxigenic fungal pathogens and reduce productivity. While rising atmospheric [CO2] is a driving force behind the warmer temperatures and drought, which aggravate fungal disease and mycotoxin accumulation, our understanding of how elevated [CO2] will effect maize defences against such pathogens is limited. Here we report that elevated [CO2] increases maize susceptibility to Fusarium verticillioides proliferation, while mycotoxin levels are unaltered. Fumonisin production is not proportional to the increase in F. verticillioides biomass, and the amount of fumonisin produced per unit pathogen is reduced at elevated [CO2]. Following F. verticillioides stalk inoculation, the accumulation of sugars, free fatty acids, lipoxygenase (LOX) transcripts, phytohormones and downstream phytoalexins is dampened in maize grown at elevated [CO2]. The attenuation of maize 13-LOXs and jasmonic acid production correlates with reduced terpenoid phytoalexins and increased susceptibility. Furthermore, the attenuated induction of 9-LOXs, which have been suggested to stimulate mycotoxin biosynthesis, is consistent with reduced fumonisin per unit fungal biomass at elevated [CO2]. Our findings suggest that elevated [CO2] will compromise maize LOX-dependent signalling, which will influence the interactions between maize and mycotoxigenic fungi. Elevated [CO2] increases maize susceptibility to Fusarium verticillioides proliferation but mycotoxin levels are unaltered. The attenuation of maize 13-LOXs and JA production correlates with reduced terpenoid phytoalexins and increased susceptibility. Furthermore, the attenuated induction of 9-LOXs, which have been suggested to stimulate mycotoxin biosynthesis, is consistent with reduced fumonisin per unit fungal biomass at elevated [CO2].
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                08 November 2019
                2019
                : 10
                : 2525
                Affiliations
                Applied Mycology Group, Cranfield Soil and Agrifood Institute, Environment and Agrifood Theme, Cranfield University , Bedford, United Kingdom
                Author notes

                Edited by: Mehdi Razzaghi-Abyaneh, Pasteur Institute of Iran (PII), Iran

                Reviewed by: Abdulsamie Hanano, Atomic Energy Commission of Syria, Syria; Massimo Reverberi, Sapienza University of Rome, Italy

                *Correspondence: Naresh Magan, n.magan@ 123456cranfield.ac.uk

                This article was submitted to Food Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2019.02525
                6856084
                4bc62e01-f1d0-4db0-8ccc-37e201462201
                Copyright © 2019 Gasperini, Rodriguez-Sixtos, Verheecke-Vaessen, Garcia-Cela, Medina and Magan.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 26 August 2019
                : 21 October 2019
                Page count
                Figures: 9, Tables: 3, Equations: 0, References: 43, Pages: 13, Words: 9919
                Funding
                Funded by: CAPES 10.13039/501100002322
                Funded by: CONyCIT
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                resilience,biocontrol,aflatoxins,climate change,non-toxigenic aspergillus flavus,non-gm maize,gm maize

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