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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 references 67

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          Epidemiology of Fusarium diseases and their mycotoxins in maize ears

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            Sphingolipid perturbations as mechanisms for fumonisin carcinogenesis.

            There is a great deal of evidence that altered sphingolipid metabolism is associated with fumonisin-induced animal diseases including increased apoptotic and oncotic necrosis, and carcinogenesis in rodent liver and kidney. The biochemical consequences of fumonisin disruption of sphingolipid metabolism most likely to alter cell regulation are increased free sphingoid bases and their 1-phosphates, alterations in complex sphingolipids, and decreased ceramide (CER) biosynthesis. Because free sphingoid bases and CER can induce cell death, the fumonisin inhibition of CER synthase can inhibit cell death induced by CER but promote free sphingoid base-induced cell death. Theoretically, at any time the balance between the intracellular concentration of effectors that protect cells from apoptosis (decreased CER, increased sphingosine 1-phosphate) and those that induce apoptosis (increased CER, free sphingoid bases, altered fatty acids) will determine the cellular response. Because the balance between the rates of apoptosis and proliferation is important in tumorigenesis, cells sensitive to the proliferative effect of decreased CER and increased sphingosine 1-phosphate may be selected to survive and proliferate when free sphingoid base concentration is not growth inhibitory. Conversely, when the increase in free sphingoid bases exceeds a cell's ability to convert sphinganine/sphingosine to dihydroceramide/CER or their sphingoid base 1-phosphate, then free sphingoid bases will accumulate. In this case cells that are sensitive to sphingoid base-induced growth arrest will die and insensitive cells will survive. If the cells selected to die are normal phenotypes and the cells selected to survive are abnormal, then cancer risk will increase.
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              Co-contamination of aflatoxin B1 and fumonisin B1 in food and human dietary exposure in three areas of China.

              Aflatoxins and fumonisins are ubiquitous foodborne toxicants and the co-occurrence of these mycotoxins in human foods represents a significant public health concern, which has been strongly associated with human aflatoxicosis, neural tube defects, as well as many types of primary cancers. In this study the co-contamination of aflatoxin B(1) (AFB(1)) and fumonisin B(1) (FB(1)) in food and human dietary exposure was investigated in residents of three different areas of China. A total of 209 food samples were measured for AFB(1) and FB(1). The median AFB(1) levels were 13.5, 2.3 and 1.3 µg kg(-1) and the median FB(1) levels were 2.6, 0.4 and 0.3 mg kg(-1) in corn samples collected from Huaian (a high-risk area for oesophageal cancer), Fusui (a high-risk area for liver cancer) and Huantai (a low-risk area for both oesophageal and liver cancers), respectively. The median level of AFB(1) in plant oil of Fusui was the highest (52.3 µg kg(-1)) among all food samples analysed. Co-contamination of these two mycotoxins was found in corn, rice and wheat flour. Based on measured food consumption data, the averaged daily dietary intake of AFB(1) was 0.397 µg (range = 0.269-1.218 µg) in residents of Huantai, 1.723 µg (0.224-49.772 µg) in Huaian, and 2.685 µg (1.006-14.534 µg) in Fusui. The averaged FB(1) daily dietary intake was 92.4 µg (range = 55.0-362.1 µg) for residents of Huantai, 460.0 µg (83.2-2894.5 µg) in Huaian, and 138.6 µg (30.0-10,541.6 µg) in Fusui. These data suggest that the co-exposure to AFB(1) and FB(1) in residents of rural China may contribute to the aetiology of human chronic diseases in high-risk areas.
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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
                Affiliations
                1 Department of Plant Pathology and Crop Physiology, Louisiana State University AgCenter , Baton Rouge, LA, United States
                2 Department of Entomology, Louisiana State University AgCenter , Baton Rouge, LA, United States
                3 Bacterial Foodborne Pathogens and Mycology Research Unit, USDA-ARS-NCAUR , Peoria, IL, United States
                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
                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.

                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

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