Environmental distribution and genetic diversity of vegetative compatibility groups determine biocontrol strategies to mitigate aflatoxin contamination of maize byAspergillus flavus

Abstract

SummaryMaize infected by aflatoxin‐producing A spergillus flavus may become contaminated with aflatoxins, and as a result, threaten human health, food security and farmers' income in developing countries where maize is a staple. Environmental distribution and genetic diversity of A . flavus can influence the effectiveness of atoxigenic isolates in mitigating aflatoxin contamination. However, such information has not been used to facilitate selection and deployment of atoxigenic isolates. A total of 35 isolates of A . flavus isolated from maize samples collected from three agro‐ecological zones of Nigeria were used in this study. Ecophysiological characteristics, distribution and genetic diversity of the isolates were determined to identify vegetative compatibility groups (VCGs). The generated data were used to inform selection and deployment of native atoxigenic isolates to mitigate aflatoxin contamination in maize. In co‐inoculation with toxigenic isolates, atoxigenic isolates reduced aflatoxin contamination in grain by > 96%. A total of 25 VCGs were inferred from the collected isolates based on complementation tests involving nitrate non‐utilizing (nit−) mutants. To determine genetic diversity and distribution of VCGs across agro‐ecological zones, 832 nit− mutants from 52 locations in 11 administrative districts were paired with one self‐complementary nitrate auxotroph tester‐pair for each VCG. Atoxigenic VCGs accounted for 81.1% of the 153 positive complementations recorded. Genetic diversity of VCGs was highest in the derived savannah agro‐ecological zone (H = 2.61) compared with the southern Guinea savannah (H = 1.90) and northern Guinea savannah (H = 0.94) zones. Genetic richness (H = 2.60) and evenness (E 5 = 0.96) of VCGs were high across all agro‐ecological zones. Ten VCGs (40%) had members restricted to the original location of isolation, whereas 15 VCGs (60%) had members located between the original source of isolation and a distance > 400 km away. The present study identified widely distributed VCGs in Nigeria such as AV0222, AV3279, AV3304 and AV16127, whose atoxigenic members can be deployed for a region‐wide biocontrol of toxigenic isolates to reduce aflatoxin contamination in maize.

Biological control of aflatoxins in Africa: current status and potential challenges in the face of climate change

“…Members of certain specific VCGs produce large quantities of aflatoxins (>10,000 µg/kg), while members of specific different VCGs produce low concentrations of aflatoxins and members of some VCGs produce no aflatoxins at all (Cotty, 1989;Joffe, 1969). VCGs composed entirely of individuals with no aflatoxin-producing ability are known as atoxigenic (Atehnkeng et al, 2016;Grubisha and Cotty, 2015). Inability of members of some VCGs to produce aflatoxins is linked to the presence of several lesions in the genome including deletions and single nucleotide polymorphisms or SNPs (Ehrlich and Cotty, 2004;Adhikari et al, 2016).…”

“…The aflatoxin reductions were associated with over 75% combined incidence of the four atoxigenic VCGs on treated maize. Among the four atoxigenic VCGs used in the experimental product, one was not frequently isolated from treated fields suggesting its unsatisfactory adaptation (Atehnkeng et al, 2016) and was replaced with a more efficient VCG in the final product trademarked as Aflasafe. After subsequent improvements in the formulation, Nigeria's National Food and Drug Administration and Control (NAFDAC) approved in 2014 the full registration of Aflasafe for use in both maize and groundnut.…”

“…Another criterion is the complete absence of toxigenic members in the selected atoxigenic VCGs (Atehnkeng et al, 2016). Critics of the use of atoxigenic A. flavus to reduce aflatoxin-producing fungi in crops have argued that a recombination event might result in highly competitive aflatoxin-producing progeny or 'superstrains' capable of producing a lot of aflatoxins (Ehrlich et al, 2015;Moore, 2015;Moore et al, 2013).…”

Aflatoxins: biosynthesis, prevention and eradication

“…(Dorner, 2009). Crops are typically infected by multiple A. flavus strains (Atehnkeng et al, 2016) and atoxigenic isolates applied on growing crops may compete with toxigenic strains during co-infection, and also interfere with the AF accumulation in plants. For certain atoxigenic isolates, competitive exclusion is sufficient to explain the AF reduction during co-infection (Hruska et al, 2014) in a pro cess that is aided by initial host interaction (Mehl and Cotty, 2011).…”

Infection with toxigenic and atoxigenic strains of Aspergillus flavus induces different transcriptional signatures in maize kernels

“…Atoxigenic strains of A. flavus were reported to reduce the contamination of aflatoxin up to 90% in maize in in-vitro studies carried out with Italian strains (Mauro et al 2015). Comparable results are reported in field trials managed in the USA and Africa (Abbas et al 2006;Atehnkeng et al 2016). Use of biocontrol products with atoxigenic A. flavus active ingredients is a proven method for reducing the aflatoxin content and will be crucial in the future; in fact, A. flavus and other aflatoxin-producing fungi thrive under the hot and dry environmental conditions recently experienced and predicted due to the ongoing climate change (Battilani et al 2016).…”