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ABSTRACT LEWIS, MARY HUNT. Genetic Structure of Soil ABSTRACT LEWIS, MARY HUNT. Genetic Structure of Soil Populations of Aspergillus Section Flavi and Efficacy of Biocontrol of Aflatoxin Contamination in Corn. (Under the direction of Dr. Ignazio Carbone and Dr. Peter S. Ojiambo). Corn is contaminated with aflatoxin, a carcinogenic mycotoxin, when aflatoxigenic strains within Aspergillus section Flavi infect corn kernels. Biocontrol using non- aflatoxigenic strains of A. flavus have been shown to have the greatest potential to control aflatoxin contamination in corn. However, factors that influence the efficacy of biocontrol agents in different locations are not fully understood. One factor affecting the effectiveness biocontrol could be the genetic structure of the native soil populations of Aspergillus section Flavi. In this study, we investigated how the genetic structure of native soil populations of Aspergillus section Flavi could impact the effectiveness of two commercially available biological control products in different locations in the southeastern US. Field trials were conducted in Alabama, Georgia and North Carolina in the 2012 and 2013 growing seasons. Biocontrol products AF36 and Afla-Guard® were applied to the corn at the VT stage. Soil samples were collected prior to and 1-week after biocontrol application and at harvest to determine the genetic structure of soil populations. In all states, A. flavus (61-100%) was the most dominant species within section Flavi, with A. parasiticus (<35%) being the second- most frequently isolated species. A. nomius, A. caelatus and A. tamarii were detected only in Alabama, but at very low frequencies (<5%). Multi-locus sequence typing revealed that prior to biocontrol application in North Carolina in 2012, 48% of the isolates were the same haplotype as the biocontrol strain Afla-Guard, which belongs to lineage IB, while only 6% were of the same haplotype as AF36, which belongs to lineage IC. Phylogenetic analyses revealed that strains of the Afla-Guard haplotype persisted in the field throughout the study better than strains similar to the AF36 haplotype. Similar results were observed in Alabama in 2012 and Georgia in 2013, where the percentage of isolates matching Afla-Guard increased from 36% to 68% and 12% to 95% from the pre-application sampling period to the harvest sampling period in Alabama and Georgia, respectively. Many isolates shared the same multi-locus haplotype across all three states, which provides evidence of shared patterns of descent. In addition, a two-tailed binomial test of clone-corrected mating-type data showed that populations at every sampling period, except for the Alabama pre- application sampling periods in 2012 and 2013, had a recombining population structure consistent with sexual reproduction. Aflatoxin levels in harvested grain were generally low in untreated plots (2 to 104 ppb) in all locations and years. However, significant differences in aflatoxin contamination of grain between treated and untreated plots were observed in North Carolina in 2012. Here, contamination was also significantly lower in grain from plots treated with Afla-Guard than from those treated with AF36. These results seem to suggest that matching the biocontrol product to the predominant A. flavus haplotype of the native soil population can increase efficacy of biocontrol of aflatoxin contamination. The use of biocontrol strains that are genetically similar to native soil populations may be important in the sustainable use of biological control to mitigate aflatoxin contamination in corn. © Copyright 2014 Mary Hunt Lewis All Rights Reserved Genetic Structure of Soil Populations of Aspergillus Section Flavi and Efficacy of Biocontrol of Aflatoxin Contamination in Corn by Mary Hunt Lewis A thesis submitted to the Graduate Faculty of North Carolina State University in partial fulfillment of the requirements for the degree of Master of Science Plant Pathology Raleigh, North Carolina 2014 APPROVED BY: ______________________________ Dr. Gary A. Payne Member of Advisory Committee ________________________________ ________________________________ Dr. Ignazio Carbone Dr. Peter S. Ojiambo Co-Chair of Advisory Committee Co-Chair of Advisory Committee DEDICATION To my loving parents and grandparents. ii BIOGRAPHY Mary Hunt Lewis was born June 26, 1990 in the city of Fayetteville, North Carolina. In August of 2008, Mary first stepped foot on the campus of North Carolina State University with the intent of majoring in Elementary Education. While taking a biology class as an elective her first semester, she realized her love of plants and biological sciences and changed her major to Plant Biology. During her junior year of undergrad, she joined Dr. Ignazio Carbone’s lab and aided in a research project examining mating-type distributions of populations of Aspergillus flavus. During her time as an undergraduate, she participated in several summer internships and gained a better understanding of research in the plant sciences. The first was at the University of Nebraska-Lincoln in the summer of 2010 under the direction of Dr. Donald Weeks, where she first learned about plant pathology through her project which involved purifying TAL-effector proteins. The second was at the Boyce Thompson Institute (BTI) at Cornell University for the summer of 2011. Here, Mary worked on a project that examined the regulation of the R gene CPR30. Through her experiences at these internships, Mary realized the importance of plant disease research and, after graduating with her BS in 2012, chose to pursue her MS in plant pathology. After being offered a research assistantship in the Department of Plant Pathology at North Carolina State University, she worked on a project examining how population genetics affect the efficacy of biological control of aflatoxin contamination in corn under the direction of Dr. Ignazio Carbone and Dr. Peter S. Ojiambo. iii ACKNOWLEDGMENTS I would first like to thank Gary Payne for showing me fungus-infected corn kernels on a random day that I had to stop in his office when I was an undergraduate in the fall semester of 2009. I never would have known about this field of research if it were not for the inspiring conversation we had about mycotoxins and food safety. I would also like to thank my major co-advisors Dr. Peter Ojiambo and Dr. Ignazio Carbone, who have had unyielding patience with me during my time here at North Carolina State. I wish also to thank Dr. Gary Payne for his role on my graduate research committee. Also, I want to thank collaborators who worked on this project, Dr. Kira Bowen and Dr. Austin Hagan of Auburn University, Dr. Robert Kemerait of the University of Georgia and Dr. Ronnie Heiniger of North Carolina State University for conducting the field experiments and collecting of soil samples in their states. Sincere thanks also go to Rakhi Singh in Dr. Carbone’s lab and Greg Obrian in Dr. Payne’s lab for their guidance and advice with the laboratory work. The financial support from the Aflatoxin Mitigation Center of Excellence (AMCOE) is highly acknowledged. I also could not have done this without my dear friends who come from all parts of my life. To Heather Pierce, who has been away at graduate school in St. Kitts, thank you for being my music twin, for “winning” the internet when it comes to finding the perfect funny images on stressful days and for knowing my story. To my closest fellow plant pathologist friends, Alyssa Koehler and Emma Lookabaugh, thank you for planning very necessary get- togethers where we share our favorite recipes, new craft ideas and our thoughts on graduate school and the future. To Leslie Johnson, my longtime friend from Governor’s School, thank iv you for being a fabulous college roommate and for introducing me to a cupcake bakery that also sells wine. To those I have not exclusively named: “Too often we underestimate the power of a touch, a smile, a kind word, a listening ear, an honest compliment, or the smallest act of caring, all of which have the potential to turn a life around.”- Leo Buscaglia. v TABLE OF CONTENTS LIST OF TABLES ............................................................................................................ vii LIST OF FIGURES ........................................................................................................... ix CHAPTER 1: LITERATURE REVIEW ............................................................................ 1 1.1 CORN ........................................................................................................................ 1 1.2 TAXONOMY AND BIOLOGY OF ASPERGILLUS ............................................... 2 1.3 PATHOGEN ECOLOGY.......................................................................................... 5 1.4 PRODUCTION OF AFLATOXINS BY ASPERGILLUS SECTION FLAVI........... 6 1.5 MANAGEMENT OF AFLATOXIN CONTAMINATION IN CORN .................... 9 1.6 RATIONALE AND JUSTIFICATION................................................................... 12 LITERATURE CITED .................................................................................................. 15 CHAPTER 2 ..................................................................................................................... 22 2.1 ABSTRACT ............................................................................................................ 22 2.2 INTRODUCTION ................................................................................................... 22 2.3 MATERIALS AND METHODS ...........................................................................
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