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Open Casper.Pdf The Pennsylvania State University The Graduate School Department of Crop and Soil Sciences PLANT-INSECT (LEPIDOPTERA) INTERACTION IN MAIZE A Dissertation in Agronomy by Wen-Po Chuang 2012 Wen-Po Chuang Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy May 2012 ii The dissertation of Wen-Po Chuang was reviewed and approved* by the following: Dawn S Luthe Professor of Crop and Soil Sciences Dissertation Advisor Chair of Committee Surinder Chopra Associate professor of Crop and Soil Sciences Kathleen Brown Professor of Horticulture John E. Carlson Professor of Forest Resources Yinong Yang Associate professor of Plant Pathology Jack Watson Professor of Crop and Soil Sciences Interim Head of the Department of Crop and Soil Sciences *Signatures are on file in the Graduate School iii ABSTRACT Plants are frequently challenged by insect herbivores and have developed sophisticated defense mechanisms to counter their attack. Which insect elicitors can be recognized by plants and which plant proteins are involved in plant defense against insects are two big questions for plant scientists. In this dissertation, I would like to address these two questions by using maize (Zea mays) and fall armyworm (Spodoptera frugiperda) as a model system. Although chewing insects cause extensive mechanical damage to plants, this does not account for the entire effect of herbivory. Caterpillar oral secretions, including saliva and regurgitant, trigger herbivore defense responses in plants. Several herbivore-associated molecular patterns (HAMPs) have been found in insect regurgitant. However, there is an argument whether caterpillar larvae actually regurgitate on maize leaves during feeding on maize. Thus, I examined fall armyworm larval saliva to determine if it is an important elicitor of herbivore defenses in maize. Analyses indicated that very little regurgitant was deposited on the maize leaf during caterpillar feeding. Furthermore, caterpillar regurgitant failed to trigger plant defense-related genes in maize. Whereas, leaf tissue immunoblots indicated that glucose oxidase, an abundant saliva protein, was deposited on the leaf when caterpillars fed there. The effect of caterpillar saliva on maize defense gene expression was determined by allowing ablated (no saliva) and non-ablated (saliva present) caterpillars to feed in the maize whorl. The results showed that feeding by unablated caterpillars significantly increased the expression of plant genes involved in jasmonate biosynthesis pathway and direct defenses. Furthermore, saliva-induced bioassay showed that compared to plants fed on unablated larvae, plants fed by ablated larvae did not induce sufficient direct defense to significantly retard larval growth. Furthermore, the saliva-responsive maize protein profile has been identified from the proteomics analysis. The results of this study show that caterpillar saliva is an important elicitor for triggering herbivore defenses in maize. Another research project was to discover a new way to find plant proteins that defend against insect herbivores. Some important plant defense proteins iv have been found that can resist digestive proteases in the insect gut and are eliminated in the frass. We used mass spectrometry to identify several maize proteins in fall armyworm frass that may play a role in herbivore defense, including ribosome-inactivating protein 2 (RIP2). Ribosome-inactivating proteins (RIPs) act by depurinating residues on ribosomal RNA and thereby inhibit translation. Since RIP2 was found in frass, we proposed that it might be involved in defending maize from herbivore attack. Immunoblot analysis indicated that RIP2 is initially synthesized as an inactive proenzyme that can be cleaved to the active form by larval gut extracts. Also, results indicated that the expression of RIP2 was induced by FAW larval feeding, but not mechanical wounding. The proenzyme form of RIP2 was detected in 13 maize inbred lines and two teosinte subspecies. This data indicates that RIP2 expression in response to insect feeding is a wide spread phenomenon in maize. Quantitative-RT-PCR and immunoblot analysis indicated that RIP2 is rapidly induced (1 hour) following caterpillar attack and remains at the wound sites for four days after caterpillar removal. Phytohormone application assays determined that RIP2 expression was regulated by several different phytohormones, including ethylene, JA and ABA. It appears that there is no consistent pattern of hormonal regulation of RIP-like protein expression. The expression profile of RIP2 in maize vegetative stage was examined. The data showed that RIP2 is expressed locally and during maize vegetative development. Furthermore, when purified recombinant RIP2 was directly tested against fall armyworm larvae in bioassays, the data indicated that the amount of RIP2 typically found in the leaf after caterpillar attack could significantly retard caterpillar growth. We concluded that RIP2 plays an important role in protecting maize against insect herbivores. With these two studies, I was able to take a further step toward understanding the interaction of plant-insect relationship. Key words: plant-insect interaction, maize (Zea mays), fall armyworm (Spodoptera frugiperda), saliva, ribosome-inactivating protein 2 (RIP2) v TABLE OF CONTENTS LIST OF FIGURES ......................................................................................................... viii LIST OF TABLES ........................................................................................................... x ACKNOWLEDGEMENTS ............................................................................................. xi Chapter 1 Introduction ............................................................................................................. 1 Chapter 2 Literature review ..................................................................................................... 4 Plant defense .................................................................................................................... 4 Constitutive and induced defenses ........................................................................... 5 Direct and indirect defense ....................................................................................... 5 Mechanical wounding versus caterpillar feeding ............................................................. 7 Insect elicitors .................................................................................................................. 9 HAMPs ..................................................................................................................... 9 Saliva ........................................................................................................................ 9 Regurgitant ............................................................................................................... 11 Plant antinutritive proteins ............................................................................................... 12 Chapter 3 Fall armyworm (Spodoptera frugiperda) saliva is an important elicitor of herbivore defenses in maize ............................................................................................. 15 Introduction ...................................................................................................................... 15 Results .............................................................................................................................. 18 Little regurgitant is detected on caterpillar-fed maize leaves ................................... 18 Caterpillars salivate on maize leaves........................................................................ 19 Caterpillar regurgitant failed to trigger plant defense-related genes in maize ......... 20 Saliva induces plant defense-related genes in maize ................................................ 21 Performance of larvae on previously fed maize leaves ............................................ 22 Structure of the spinneret and collection of saliva ................................................... 23 Discussion ........................................................................................................................ 23 Materials and methods ..................................................................................................... 27 Plant materials and insect rearing ............................................................................. 27 Fluorescence detection of regurgitant ...................................................................... 28 Ablation of spinneret ................................................................................................ 29 Quantitative RT-PCR ............................................................................................... 29 Tissue printing .......................................................................................................... 30 Saliva-induced bioassays .......................................................................................... 30 Feeding area calculation ........................................................................................... 31 Scanning electron microscopy ................................................................................. 31 Chapter 4 Ribosome-inactivating protein 2 protects maize against insect herbivores ............. 43 Introduction .....................................................................................................................
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