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Open Acevedo FE Thesis Sep 2016.Pdf The Pennsylvania State University The Graduate School Department of Entomology THE WEAR AND TEAR OF FEEDING: INDUCED PLANT DEFENSES BY FALL ARMYWORM HERBIVORY AND COUNTER INSECT ADAPTATION MECHANISMS A Dissertation in Entomology by Flor Edith Acevedo Bedoya 2016 Flor Edith Acevedo Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy December 2016 The dissertation of Flor Edith Acevedo was reviewed and approved* by the following: Gary W. Felton Professor of Entomology Dissertation Advisor Chair of Committee and Department Head Dawn Luthe Professor of Plant Sciences John Tooker Associate professor of Entomology James H. Marden Professor of Biology James L. Rosenberger Professor of Statistics *Signatures are on file in the Graduate School iii ABSTRACT Feeding by insect herbivores induces defense responses in plants. Numerous studies have shown that plants recognize the mechanical damage as well as a variety of herbivore-derived cues present in insect oral secretions, saliva and frass to activate the production of specific defenses responses. Plant defenses negatively affect herbivore fitness; therefore to be able to feed on plants, insects need to develop specific adaptations to overcome defenses of their hosts. This can be challenging for herbivores that feed on a wide range of plants with diverse structural and biochemical defenses. In this dissertation, I studied defense responses induced by a polyphagous herbivore in some of its host plants as well as some of its adaptation mechanisms to counter the effect of these defenses. I used the lepidopteran fall armyworm (FAW) Spodoptera frugiperda, and its host plants maize, Bermuda grass, rice and tomato as a model system. The FAW comprises two host strains that are associated with different host plants in field conditions; the corn strain is mainly associated with maize, while the rice strain is mostly associated with forage grasses and rice. I specifically tested the presence of intraspecific differences in plant defense induction by the FAW strains and the composition of their caterpillar saliva. I also investigated the effect of caterpillar-associated gut bacteria on the modulation of defense responses in different hosts. In addition, I documented morphological and developmental adaptations of the FAW larvae to cope with their host structural defenses. The results of this study show that feeding by the FAW strains induced different defense responses in maize and Bermuda grass; this plant defense induction was associated with differences in the caterpillar saliva. The saliva of the FAW strains also has divergent protein profiles and differing expression of several salivary proteins. In addition, the saliva of the FAW contains non-protein compounds that actively regulate defenses in different hosts; these include several phytohormones and other presumptive small molecules. During feeding, the FAW larvae also secrete small amounts of regurgitant, I identified two bacteria isolates in the caterpillar oral secretions that modulated defense responses in tomato and maize plants. In addition, feeding by this insect induced the production of glandular trichomes in tomato and the deposition of silica in maize and rice iv plants. As adaptive strategies to feed on Bermuda grass and rice, the FAW larvae increased their head size to house larger mandibular muscles and potentially increase the biting force needed to feed on tough leaves. I conclude that FAW feeding modulates the induction of plant biochemical and physical defenses, which in turn induced plastic physiological and morphological changes in this insect species. The results of this dissertation highlight the importance of insect physiological and morphological plastic adaptations as means to feed on different host plants. v TABLE OF CONTENTS List of Figures .......................................................................................................................... vii List of Tables ........................................................................................................................... x Acknowledgements .................................................................................................................. xi Chapter 1 Introduction ............................................................................................................. 1 Induced plant defenses ..................................................................................................... 4 References ........................................................................................................................ 7 Chapter 2 Intraspecific differences in plant defense induction by the fall armyworm strains ............................................................................................................................... 10 Abstract ............................................................................................................................ 10 Introduction ...................................................................................................................... 11 Methods ............................................................................................................................ 13 Results .............................................................................................................................. 22 Discussion ........................................................................................................................ 35 References ........................................................................................................................ 41 Chapter 3 Quantitative proteomic analysis of the fall armyworm saliva ................................. 46 Abstract ............................................................................................................................ 46 Introduction ...................................................................................................................... 47 Methods ............................................................................................................................ 49 Results .............................................................................................................................. 55 Discussion ........................................................................................................................ 59 References ........................................................................................................................ 75 Chapter 4 Phytohormones and small molecules in the fall armyworm saliva ......................... 85 Abstract ............................................................................................................................ 85 Introduction ...................................................................................................................... 86 Methods ............................................................................................................................ 88 Results .............................................................................................................................. 95 Discussion ........................................................................................................................ 105 References ........................................................................................................................ 113 Chapter 5 Fall armyworm armyworm-associated gut bacteria modulate plant defense responses .......................................................................................................................... 118 Abstract ............................................................................................................................ 118 Introduction ...................................................................................................................... 119 Methods ............................................................................................................................ 122 vi Results .............................................................................................................................. 130 Discussion ........................................................................................................................ 140 References ........................................................................................................................ 145 Chapter 6 Physical plant defenses induced by fall armyworm herbivory and insect counter adaptation mechanisms ....................................................................................... 149 Abstract ............................................................................................................................ 149 Introduction ...................................................................................................................... 150 Methods ............................................................................................................................ 153 Results .............................................................................................................................. 157 Discussion ........................................................................................................................ 167 References .......................................................................................................................
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