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Introducing an Indigenous Non-Toxigenic Aspergillus Flavus Strain Isolated from Iraqi Corn Grains As a Bio-Control Agent to Redu

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Introducing an Indigenous Non-Toxigenic Aspergillus Flavus Strain Isolated from Iraqi Corn Grains As a Bio-Control Agent to Redu University of Arkansas, Fayetteville ScholarWorks@UARK Theses and Dissertations 7-2020 Introducing an Indigenous Non-toxigenic Aspergillus flavus Strain Isolated from Iraqi Corn Grains as a Bio-Control Agent to Reduce Aflatoxin Contamination in Corn Grains Ali Almatakeez University of Arkansas, Fayetteville Follow this and additional works at: https://scholarworks.uark.edu/etd Part of the Agricultural Science Commons, Cell Biology Commons, Plant Biology Commons, and the Plant Pathology Commons Citation Almatakeez, A. (2020). Introducing an Indigenous Non-toxigenic Aspergillus flavus Strain Isolated from Iraqi Corn Grains as a Bio-Control Agent to Reduce Aflatoxin Contamination in Corn Grains. Theses and Dissertations Retrieved from https://scholarworks.uark.edu/etd/3759 This Dissertation is brought to you for free and open access by ScholarWorks@UARK. It has been accepted for inclusion in Theses and Dissertations by an authorized administrator of ScholarWorks@UARK. For more information, please contact [email protected]. Introducing an Indigenous Non-toxigenic Aspergillus flavus Strain Isolated from Iraqi Corn Grains as a Bio-Control Agent to Reduce Aflatoxin Contamination in Corn Grains A dissertation submitted in partial fulfillment of the requirements for the degree of Doctoral of Philosophy in Cell and Molecular Biology by Ali Almatakeez University of Mosul Bachelor of Science in Biology, 1998 University of Mosul Master of Science in Plant Pathology, 2001 July 2020 University of Arkansas This dissertation is approved for recommendation to the Graduate Council . ______________________________ Burton H. Bluhm, Ph.D Dissertation Director ______________________________ _______________________________ John C. Rupe, Ph.D Jackson Lay Jr. Ph.D Committee Member Committee Member ___________________________________ Griffiths G. Atungulu, Ph.D Committee Member ABSTRACT Mycotoxin contamination of cereal crops, such as maize and sorghum, is a global concern because of the potential health effects on humans and animals. Although substantial research has been conducting regarding mycotoxin prevention and mitigation, little information is available about the association of mycotoxin-producing fungi with corn and sorghum grain in Iraq. Identifying and refining indigenous atoxigenic strains to reduce mycotoxin contamination of maize and sorghum has the potential to enhance the nutritional value of these grains while reducing economic losses. However, to our knowledge, this tactic has not yet been adopted by agricultural authorities and farmers in Iraq. To survey mycotoxigenic fungi associated with corn and sorghum grain in Iraq and identify potential biological control agents ‘customized’ for Iraqi production conditions, a collection of corn and sorghum grain samples were imported from Iraq. DNA-based diagnostic analyses were integrated with morphology-dependent methods to identify seedborne mycoflora in corn and sorghum samples collected from different regions in Iraq (north, central, and south). The most common fungal genera, i.e., Fusarium spp. , Alternaria spp. , Chaetomium spp. , Penicillium spp. , and Aspergillus spp. were found frequently in both kinds of grains. However, Exserohilum , Anthracosystis, Bipolaris, Sporisorium, Curvularia, Sarocladium, Humicola, Byssochlayms, and Stenocarpella were found associated with some samples, which is the first such reporting of these genera associated with corn in Iraq. Moreover, species borders of Aspergillus spp. and Fusarium spp. were delimited successfully through multi-locus sequence typing analysis of four conserved genes within each genera ( ITS , B-tub, CaM, and RPB-2 for Aspergillus spp. and EF-1ɑ, CaM , and H3 for Fusarium spp. ). Liquid chromatography tandem mass spectrometry (LC-MS/MS) analysis of Iraqi corn and sorghum samples revealed that most samples were contaminated with relatively low levels of fumonisin-B1, ranging from 0.01-8.6 ppm. However, neither corn nor sorghum samples were contaminated with aflatoxin-B1. Also, analyses of mycotoxigenic potential of Aspergillus flavus (27 isolates) identified three non-toxigenic A. flavus isolates (A-1-9, A-4-54, and A-4-75), whereas the rest varied in aflatoxin-B1 production. However, all Fusarium species (86 isolates) produced fumonisin-B1 at different levels, ranging from high to low concentrations. This is potentially the first report of F. incarnatum and F. acuminatum (well-known as deoxynivalenol – DON- and T2 producers, respectively) producing fumonisin mycotoxins. Co-inoculation experiments between Iraqi native nontoxigenic isolates (A-1-9, A-4-54, and A-4-75) and native Iraqi toxigenic isolate (A-15-49) or the reference A. flavus NRRL 3357 substantiated the competitive ability of the Iraqi native nontoxigenic isolates to suppress aflatoxin biosynthesis in toxigenic strains. Aflatoxin-B1 was suppressed by approximately 99.2% compared to control treatments in which toxigenic isolates were inoculated individually. This is the first report of indigenous non-toxigenic A. flavus isolates from Iraq with documented biological control activity against toxigenic strains. Further investigations are required to evaluate the performance of these isolates in corn fields in Iraq. ACKNOWLEDGMENTS Foremost, praise to Allah the almighty for blessing me with the strength, patience, health, protection, and guidance that enabled me to reach this last stage of my Ph. D journey. Also, I would like to express my sincere appreciation to my wife (Eman) for bearing the hardships of being expatriated and in charge of unlimited home tasks. She supported me unconditionally, and always stills my spring with high spirits and cheerfulness. An extended thanks to my parents, brothers, and sisters in Iraq who never stopped praying to Allah to bring me academic success. I would also like to express my gratitude to my advisor, Dr. Burton H. Bluhm, for guiding me when facing obstacles, and to the professors of my advisory committee (Dr. John C. Rupe, Dr. Jackson Lay Jr., and Dr. Griffiths G. Atungulu) for their valuable advice and assistance during my studies. A special appreciation for Dr. Nadeem A. Ramadan who collected samples for my research with brotherly spirit and sent them to the US, overcoming stiff hurdles and a difficult situation in Iraq from 2014-2015. At this moment, many people that deserve to be acknowledged come to mind, especially my colleagues in the college (Mahmood, Haitham, Moafaq, Thaer and Adil), my best friends in life (Salih, Ashraf, Mahmood, Khalid, Hussein, Mohammed), and the list goes on. However, thanks to all of you for everything you have done, even it was just keeping me in your prayers. Lastly, my full appreciation for my children Alhasan, Mena, Mohammed, and Adam who graciously tolerated my roller coaster of emotions during these past few years. TABLE OF CONTENTS Chapter 1 Literature review .…………………………………………………………. 1 Global importance of corn and sorghum………………………………………………………….1 Plant pathogenic fungi.…………………………………...……………………………………….2 Impact of fungal pathogens on corn and sorghum grain.……………………………………….…4 Aspergillus flavus Link……………………………………………………………………………6 Aflatoxins………………………………………………………………………………………….8 The aflatoxin biosynthetic gene cluster…………………………………………………………...8 Significance of aflatoxin contamination…………………………………………………………10 Fusarium verticillioides (Sacc) Nirenberg…………………………………………………….....12 Fumonisins……………………………………………………………………………………….14 The fumonisin biosynthetic gene cluster………………………………………………………...15 Significance of fumonisin contamination………………………………………………………..17 Management of mycotoxins in maize grains…………………………………………………….19 Justification and objectives………………………………………………………………………22 References………………………………………………………………………………………..24 Chapter 2: Survey of fungi associated with corn and sorghum in Iraq……………………..39 Abstract…………………………………………………………………………………………..39 Introduction………………………………………………………………………………………40 Materials and methods…………………………………………………………………………...41 Sample collection………………………………………………………………………………...41 Isolation and preliminary identification of seed-borne fungi…………………………………....43 DNA extraction and analysis…………………………………………………………………….44 Preparation of fungal tissue……………………………………………………………………...44 Extraction of genomic DNA……………………………………………………………………..44 PCR and DNA analysis…………………………………………………………………………..45 Multi-locus sequence typing (MLST) of Aspergillus and Fusarium isolates……………………46 Construction of phylogenetic trees………………………………………………………………47 Results and discussion……………………………………………………..…………………….48 References………………………………………………………………………………………..63 Chapter 3: The mycotoxigenic potential of Aspergillus flavus and four Fusarium species isolated from corn and sorghum grain from Iraq …………………………………………….70 Abstract…………………………………………………………………………………………..70 Introduction…………………………………………………………………………………...….71 Materials and Methods……………………………………...……………………………………73 Optimization of mycotoxin extraction and analysis……………………………………………..73 Overview of analytical approach………………………………………………………..……….73 Preparation of analytical standards…………………………………………………………..…..73 Optimizing mycotoxin extraction parameters………………………………………………...….73 LC-MS/MS setting and analysis…………………………………………………………………74 Assessment the mycotoxin-content of corn and sorghum samples……………………………...74 Moisture content determination………………………………………………………………….74 Preparing samples for extraction………………………………………………………………...75 Mycotoxin extraction and LC-MS/MS analysis…………………………………………………75 Differentiation between toxigenic and atoxigenic isolates………………………………………75 Preparation of cracked
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