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      Low Aflatoxin Levels in Aspergillus flavus-Resistant Maize Are Correlated With Increased Corn Earworm Damage and Enhanced Seed Fumonisin

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          Abstract

          Preharvest mycotoxin contamination of field-grown crops is influenced not only by the host genotype, but also by inoculum load, insect pressure and their confounding interactions with seasonal weather. In two different field trials, we observed a preference in the natural infestation of corn earworm (CEW; Helicoverpa zea Boddie) to specific maize ( Zea mays L.) genotypes and investigated this observation. The field trials involved four maize lines with contrasting levels of resistance to Aspergillus flavus. The resistant lines had 7 to 14-fold greater infested ears than the susceptible lines. Seed aflatoxin B 1 (AF) levels, in mock- and A. flavus-inoculated ears were consistent with genotype resistance to A. flavus, in that the resistant lines showed low levels of AF (<30 ppb), whereas the susceptible lines had up to 500 ppb. On the other hand, CEW infestation showed a positive correlation with seed fumonisins (FUM) contamination by native Fusarium verticillioides strains. We inferred that the inverse trend in the correlation of AF and FUM with H. zea infestation may be due to a differential sensitivity of CEW to the two mycotoxins. This hypothesis was tested by toxin-feeding studies. H. zea larvae showed decreasing mass with increasing AF in the diet and incurred >30% lethality at 250 ppb. In contrast, CEW was tolerant to fumonisin with no significant loss in larval mass even at 100 ppm, implicating the low seed aflatoxin content as a predominant factor for the prevalence of CEW infestation and the associated fumonisin contamination in A. flavus resistant maize lines. Further, delayed flowering of the two resistant maize lines might have contributed to the pervasive H. zea damage of these lines by providing young silk for egg-laying. These results highlight the need for integrated strategies targeting mycotoxigenic fungi as well as their insect vectors for enhanced food safety.

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          Most cited references67

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          Areawide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers.

          Transgenic maize engineered to express insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) has become widely adopted in U.S. agriculture. In 2009, Bt maize was planted on more than 22.2 million hectares, constituting 63% of the U.S. crop. Using statistical analysis of per capita growth rate estimates, we found that areawide suppression of the primary pest Ostrinia nubilalis (European corn borer) is associated with Bt maize use. Cumulative benefits over 14 years are an estimated $3.2 billion for maize growers in Illinois, Minnesota, and Wisconsin, with more than $2.4 billion of this total accruing to non-Bt maize growers. Comparable estimates for Iowa and Nebraska are $3.6 billion in total, with $1.9 billion for non-Bt maize growers. These results affirm theoretical predictions of pest population suppression and highlight economic incentives for growers to maintain non-Bt maize refugia for sustainable insect resistance management.
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            Epidemiology of Fusarium diseases and their mycotoxins in maize ears

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              Influences of climate on aflatoxin producing fungi and aflatoxin contamination.

              Aflatoxins are potent mycotoxins that cause developmental and immune system suppression, cancer, and death. As a result of regulations intended to reduce human exposure, crop contamination with aflatoxins causes significant economic loss for producers, marketers, and processors of diverse susceptible crops. Aflatoxin contamination occurs when specific fungi in the genus Aspergillus infect crops. Many industries frequently affected by aflatoxin contamination know from experience and anecdote that fluctuations in climate impact the extent of contamination. Climate influences contamination, in part, by direct effects on the causative fungi. As climate shifts, so do the complex communities of aflatoxin-producing fungi. This includes changes in the quantity of aflatoxin-producers in the environment and alterations to fungal community structure. Fluctuations in climate also influence predisposition of hosts to contamination by altering crop development and by affecting insects that create wounds on which aflatoxin-producers proliferate. Aflatoxin contamination is prevalent both in warm humid climates and in irrigated hot deserts. In temperate regions, contamination may be severe during drought. The contamination process is frequently broken down into two phases with the first phase occurring on the developing crop and the second phase affecting the crop after maturation. Rain and temperature influence the phases differently with dry, hot conditions favoring the first and warm, wet conditions favoring the second. Contamination varies with climate both temporally and spatially. Geostatistics and multiple regression analyses have shed light on influences of weather on contamination. Geostatistical analyses have been used to identify recurrent contamination patterns and to match these with environmental variables. In the process environmental conditions with the greatest impact on contamination are identified. Likewise, multiple regression analyses allow ranking of environmental variables based on relative influence on contamination. Understanding the impact of climate may allow development of improved management procedures, better allocation of monitoring efforts, and adjustment of agronomic practices in anticipation of global climate change.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                23 September 2020
                2020
                : 11
                : 565323
                Affiliations
                [1] 1 Department of Plant Pathology and Crop Physiology, Louisiana State University AgCenter , Baton Rouge, LA, United States
                [2] 2 Department of Entomology, Louisiana State University AgCenter , Baton Rouge, LA, United States
                [3] 3 Bacterial Foodborne Pathogens and Mycology Research Unit, USDA-ARS-NCAUR , Peoria, IL, United States
                [4] 4 Corn Host Plant Resistance Research Unit, USDA-ARS , Mississippi State, MS, United States
                Author notes

                Edited by: George Broufas, Democritus University of Thrace, Greece

                Reviewed by: Javier Plasencia, National Autonomous University of Mexico, Mexico; Massimo Reverberi, Sapienza University of Rome, Italy

                This article was submitted to Plant Pathogen Interactions, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2020.565323
                7546873
                33101334
                cde599d9-6079-4766-89b7-73f6d002a69a
                Copyright © 2020 Chalivendra, Huang, Busman, Williams and Ham

                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
                : 24 May 2020
                : 19 August 2020
                Page count
                Figures: 4, Tables: 0, Equations: 0, References: 78, Pages: 11, Words: 6089
                Funding
                Funded by: Agricultural Research Service 10.13039/100007917
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                maize (zea mays),aspergillus flavus,fusarium verticillioides,ear rot,resistant and susceptible lines,corn earworm (helicoverpa zea boddie),aflatoxin toxicity,fumonisin tolerance

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