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Interactions Between Aspergillus Flavus and Stored-Grain Insects in Conventional and Transgenic Maize

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Interactions Between Aspergillus Flavus and Stored-Grain Insects in Conventional and Transgenic Maize Iowa State University Capstones, Theses and Graduate Theses and Dissertations Dissertations 2019 Interactions between Aspergillus flavus and stored-grain insects in conventional and transgenic maize Julie Aiza L. Mandap Iowa State University Follow this and additional works at: https://lib.dr.iastate.edu/etd Part of the Agriculture Commons, Entomology Commons, and the Plant Pathology Commons Recommended Citation Mandap, Julie Aiza L., "Interactions between Aspergillus flavus and stored-grain insects in conventional and transgenic maize" (2019). Graduate Theses and Dissertations. 17738. https://lib.dr.iastate.edu/etd/17738 This Thesis is brought to you for free and open access by the Iowa State University Capstones, Theses and Dissertations at Iowa State University Digital Repository. It has been accepted for inclusion in Graduate Theses and Dissertations by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. Interactions between Aspergillus flavus and stored-grain insects in conventional and transgenic maize by Julie Aiza L. Mandap A thesis submitted to the graduate faculty in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE Major: Plant Pathology Program of Study Committee Gary P. Munkvold, Major Professor Silvina L. Arias Richard L. Hellmich Dirk E. Maier The student author, whose presentation of the scholarship herein was approved by the program of study committee, is solely responsible for the content of this thesis. The Graduate College will ensure this thesis is globally accessible and will not permit alterations after a degree is conferred. Iowa State University Ames, Iowa 2019 ii TABLE OF CONTENTS Page LIST OF FIGURES…………………………………………………………………………………… iii LIST OF TABLES……………………………………………………………………………………. iv ABSTRACT………………………………………………………………………………………………. v CHAPTER 1. GENERAL INTRODUCTION…………………………………………………… 1 Thesis Organization…………………………………………………………………...... 1 Literature Review………………………………………………………………………… 1 Overview and Objectives……………………………………………………………… 29 Literature Cited…………………………………………………………………………… 30 CHAPTER 2. INTERACTIONS BETWEEN ASPERGILLUS FLAVUS AND STORED-GRAIN INSECTS IN CONVENTIONAL AND TRANSGENIC MAIZE…... 48 Abstract………………………………………………………………………………………. 48 Introduction………………………………………………………………………………... 49 Materials and Methods………………………………………………………………… 52 Results………………………………………………………………………………………... 58 Discussion…………………………………………………………………………………… 68 References…………………………………………………………………………………... 75 Figures and Tables………………………………………………………………………. 80 CHAPTER 3. GENERAL CONCLUSIONS.……………………………………………………. 91 iii LIST OF FIGURES Page Figure 1 Preliminary experiment on IMM with and without light……………………. 81 Figure 2 Preliminary experiment on storage at 32°C and 70-75% RH……………… 81 Figure 3 Preliminary experiment on storage at 32°C and 80-75% RH……………… Figure 4 Preliminary A. flavus levels…………………………………….……………………….... 82 Figure 5 IMM colonies on different non-Bt hybrids………………………………………… 83 Figure 6 Feeding damage caused by OK vs KS IMM………………………………………… 83 Figure 7 Indianmeal moth stages and damage………………………………………………... 84 Figure 8 Maize weevil stages and damage……………………………………………………… 84 Figure 9 Background levels of the test hybrids………………………………………………. 85 Figure 10 Survivorship of IMM and maize weevil in non-Bt R19………………………. 86 Figure 11 Mortality and growth index of IMM and MW……………………………………. 87 Figure12 Damage and grain weight loss…………………………………………………………. 88 Figure 13 A. flavus levels (CFU/g of milled grain) ……………………………………………. 89 Figure 14 Photos of A. flavus colony counts on AFPA.……………...………………………… 89 Figure 15 Aflatoxin contamination levels ………………………………………………………... 90 iv LIST OF TABLES Page Table 1 List of maize hybrids used in this study……………………………………………. 80 Table 2 List of Bt proteins evaluated and details of each protein expressed……. 80 Table 3 Background mycotoxin levels of the test hybrids ……………………………… 85 v ACKNOWLEDGEMENTS I wish to extend my sincerest gratitude to my major professor, Gary Munkvold, for providing me with this opportunity, for the unrelenting support throughout my program, and for the exceptional mentorship. I would also like to thank my committee members Silvina Arias, Richard Hellmich and Dirk Maier for their guidance. I’m so grateful to the Seed Pathology Lab members, Gabriela Morel, Fernando Marcos, Tracy Bruns, Charlie Block, especially Derrick Mayfield, for all their help in the lab and research bits of advice. Special thanks to Allan Gaul, Dai Nguyen, and Princess Mae Borja for all their assistance and support. I owe a massive thank you to the Fulbright program, the Philippine-American Educational Foundation, the Commission on Higher Education, and the University of the Philippines Los Baños for funding and investing their trust on me to do graduate studies here in the US. Finally, a big thanks to my ever-supportive family, friends, and loved ones. To God be the Glory! vi ABSTRACT Grain quality of maize after harvest is reduced primarily by mold and insect infestations. If grain temperature and moisture conditions are not controlled, Aspergillus flavus colonization and associated aflatoxin contamination can increase. Indianmeal moth (Plodia interpunctella Hübner) and maize weevil (Sitophilus zeamais Motschulsky), stored- grain pests in the Order Lepidoptera and Coleoptera, respectively, directly feed on kernels thereby predispose grain to fungal colonization and mycotoxin contamination. The presence of Bt proteins in maize, as a result of deterred insect activity, has been shown to indirectly reduce mycotoxin contamination in the field. Insect-mold interactions have been studied thoroughly in the field but not in storage, particularly the effect of lepidopteran events on Indianmeal moth and coleopteran events on maize weevil. Preliminary experiments were conducted to optimize Indianmeal moth infestation methods. Storage conditions were established based on temperature and humidity ranges common in the tropics, which would also be conducive to A. flavus growth, aflatoxin production, and insect development. The main experiments were then performed using Bt and non-Bt maize hybrids conditioned to 16-17% moisture content. The grains were artificially inoculated with A. flavus at two different levels of inoculum, i.e., 106 and 105 spores/ml. Indianmeal moth and maize weevil were infested into the grains in separate jars with and without A. flavus inoculation. After 28 days of storage, no Indianmeal moth or maize weevil survived in the transgenic hybrids with lepidopteran and coleopteran events, respectively. A. flavus caused increased mortality, reduced survivorship, and growth indices of both Indianmeal moth and maize weevil. Hence, percent grain damage and weight loss were higher in the uninoculated grain because of greater insect feeding than the inoculated grain. Colonization vii of grain by A. flavus was not significantly different between treatments with or without insect infestation, likely because A. flavus suppressed insect activity at these inoculum levels. A. flavus-insect interactions were influenced by the presence of Bt proteins in the maize grain. Insect infestations increased levels of aflatoxin contamination in the non-Bt hybrid inoculated with 106 spores/ml, but did not affect aflatoxin levels in Bt hybrids. These results indicate that Bt protection against storage insects can reduce the risk of high levels of aflatoxins in grain. 1 CHAPTER 1. GENERAL INTRODUCTION Thesis Organization This thesis is composed of an abstract followed by three chapters. The first chapter provides the significance of this study and a literature review of maize, insects, fungi, and mycotoxins with a focus on conventional and transgenic maize, Aspergillus flavus and two stored-grain insects, Indianmeal moth (Plodia interpunctella Hübner) and maize weevil (Sitophilus zeamais Motschulsky). The second chapter contains protocol development, preliminary and main experimental results, and discussion. The third chapter provides a general summary of the research. Literature Review Conventional and transgenic maize as grain In global cereal grain production, maize (Zea mays L.) comes third after wheat and rice. Maize production has increased for the past decade (Golob et al., 2004) with maize and soybean accounting for an average of 55% of seed expenditures in the United States (US) from 1996 to 2006 (Roucan-Kane & Gray, 2009). The US has led the world in maize production since 1961 up to present. In 2017, US was again the highest producer of maize with 371M tons, followed by China, and Brazil with 259M and 98M tons, respectively (FAOSTAT). Maize is a major staple food grain throughout the world, particularly in Sub- Saharan Africa, Latin America, and Asia (Smale et al., 2011). 2 Maize is mainly used for human food consumption in developing countries. It is also used as feedstock and as raw material in many value-added products such as bioethanol, sorbitol, dextrose, glucose, and oil. Agronomic management of maize-grain fields and seed- crop fields is similar, but the latter is more intensive because of its higher value (Beck, 2002). Maize seed is produced as a hybrid crop and is stored separately from grain in industrialized countries; however, in most developing countries, grain and seed are not clearly distinguished from each other and they are stored together (Pingali & Pandey, 2001). The main objective in grain storage is to minimize economic losses by preserving grain quality and meeting nutritional and product
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