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The Pennsylvania State University The Graduate School College of Agricultural Sciences HORMONAL PRODUCTS IN COCKROACH EMBRYOS; HOST SPECIFICITY OF ENTOMOPATHOGENIC NEMATODES AND THE EFFECT OF SURFACE COAT PROTEINS FROM NEMATODES ON INSECT IMMUNITY A Thesis in Entomology by Xinyi Li © 2005 Xinyi Li Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy August 2005 The thesis of Xinyi Li was reviewed and approved* by the following: Diana L. Cox-Foster Professor of Entomology Thesis Advisor Chair of Committee A. Daniel Jones Senior Scientist of Chemistry Kelli Hoover Associate Professor of Entomology Liwang Cui Assistant Professor of Entomology Stephen L. Rathbun Associate Professor of Statistics Gary Felton Professor of Entomology Head of the Department of Entomology *Signatures are on file in the Graduate School iii ABSTRACT My thesis is composed of two parts. One part is the research on hormonal products in cockroach embryos. This part was conducted under the guidiance of Dr. Glenn L. Holbrook. The other part is focused on the effects of surface coat proteins of entomopathogenic nematodes on insect immunity. Dr. Diana L. Cox-Foster guided me through the second part of my research and has served as my thesis advisor. Abstract I Juvenile hormone (JH), produced by the corpora allata (CA), regulates molting and reproduction in many insects, including cockroaches. It is known, however, that JH is produced only after dorsal closure, a conspicuous event in embryogenesis. Dorsal closure is an important physiological change in embryos. I found that the ratio of dorsal closure to embryo development time was consistent (about 45% of total embryo development) across most cockroach species. This conservation was linked to reproductive biology of the cockroaches. The only viviparous cockroach, Diploptera punctata, completed dorsal closure at 20.8 % of embryo development time. Blattella germanica, whose reproductive mode is different from other oviparity cockroaches, finished its dorsal closure at 38.5 % of embryo development time. Other oviparous and ovoviviparous cockroaches completed dorsal closure at similar percentages of the embryo development time. It is reported that embryonic CA produce both JH and its immediate precursor methyl farnesoate (MF) in Nauphoeta cinerea. Using a radiochemical assay, the present iv research found that cockroach embryos produced and released both JH and MF across all three reproductive modes. These include Periplaneta americana, Eurycotis floridana, Blaberus discoidalis, Byrsotria fumigata, Rhyparobia maderae, Nauphoeta cinerea, and Diploptera punctata. I also found that the control of conversion of MF into JH by epoxidase, the last step of biosynthesis of JH, is species dependent. These results suggest that the conversion of MF into JH is a rate-limiting step and was species specific. Abstract II Entomopathogenic nematodes (EPNs) are good candidates for biological-control agents for soil-dwelling insects. Infective juveniles (IJ) of EPNs enter insect hosts and release symbiotic bacteria that kill the hosts. Insects defend against EPNs by a rapid cellular immune response that includes encapsulation and melanization, which kills EPNs. EPNs have to overcome insects’ innate immunity to survive and reproduce. This study was designed to understand host immune responses to two species of nematodes, Heterorhabditis bacteriophora and Steinernema glaseri, and the relationship of immunity to host specificity. I hypothesized that EPNs induce or suppress the immune responses in their host based on their surface coat proteins (SCPs). The insect hosts I tested were immature stages of wax worm Galleria mellonella, oriental beetle larvae Exomala orientalis, Japanese beetle larvae Popillia japonica, tobacco horn worm larvae Manduca sexta, northern masked chafer larvae Cyclocephala borealis, and adult house cricket Acheta domesticus. I found that H. bacteriophora and S. glaseri infected and reproduced in their susceptible hosts well. In these hosts, EPNs were melanized and encapsulated at low v percentages and a high percentage of EPNs were free-moving. In the resistant hosts, most EPNs were melanized and encapsulated and few EPNs were free moving. S. glaseri NC strain was more successful compared to the S. glaseri FL strain in the same hosts. These results suggest the nematodes elicited immune responses in hosts that correlated with their infectivity. I also found that hemocytes from M. sexta, a susceptible host, recognized S. glaseri at a low percentage during the first hour post nematode introduction. After 24 hours, H. bacteriophora escaped recognition of hemocytes from G. mellonella, a susceptible host. I demonstrated that different species and strains of EPNs had different SCPs. I isolated and characterized the SCPs from S. glaseri NC strain. These SCPs suppressed immune responses in the oriental beetle larva, a susceptible host for S. glaseri, thus protecting H. bacteriophora from being killed in the same host, as it normally would be. Immuno-suppression was dose-dependent. Also, multiple injections of the SCPs protected H. bacteriophora better in Oriental beetle larvae. In a nondenatured state, two isolated SCPs in the SCPs of S. glaseri each conveyed this immuno-suppressive effect. The two SCPs were composed of smaller proteins when separated on two dimensional PAGE. Hemocytes of oriental beetle larvae started degrading after exposure to the proteins for 3 hours. Some of the SCPs from S. glaseri NC strain were sequenced and one of them was enolase, which is also secreted by other parasites. vi TABLE OF CONTENTS List of figures ........................................................................................................................ix List of tables .........................................................................................................................xi Acknowledgements ..............................................................................................................xii Chapter 1: Overview of hormonal products in cockroach embryos ...............................1 1.1 Introduction .......................................................................................................2 1.1.1 Overview of Juvenile hormone in insects and cockroaches ...............2 1.1.1.1 The insect corpora allata and juvenile hormone .................2 1.1.1.2 Juvenile hormone in cockroach embryos .............................4 1.1.1.3 Methyl farnesoate, the JH precursor in cockroach embryos ...............................................................................................5 1.1.1.4 Variation in JH and MF in embryos .....................................6 1.1.2 Overview of cocoroach reproductive modes and phylogeny ..............8 1.1.2.1 Reproductive biology of cockroaches ...................................8 1.1.2.2 Phylogeny of cockroaches studied .........................................8 1.1.3 Overview of radio chemical assay .........................................................10 1.2 Hormonal products of cockroach embryos .....................................................11 1.2.1 Dorsal closure and cockroach embryo development ..........................11 1.2.2 Methyl farnesoate and Juvenile hormone production in cockroach embryos ...............................................................................................13 1.2.3 Farnesol Stimulation of hormonal production in cockroach embryos ...............................................................................................15 Refereneces ..............................................................................................................23 Chapter 2 Dorsal closure, reproduction, juvenile hormone and methyl farnesoate production in cockroach embryos ..............................................................................27 Abstract ....................................................................................................................28 Introduction .............................................................................................................29 vii Material and methods .............................................................................................35 Results ......................................................................................................................42 Discussion ................................................................................................................56 Acknowledgement ...................................................................................................60 References ................................................................................................................61 Chapter 3: Overview of insect immunity and entomopathogenic nematodes ...............66 3.1 Introduction .......................................................................................................67 3.1.1 Overview of insect innate immunity .....................................................67 3.1.1.1 Insect hemocytes and cellular immunity ................................69 3.1.1.2 Insect humoral immunity, antimicrobial peptides and signalling pathways ..............................................................74 3.1.1.3 Recognition of nonself .............................................................84 3.1.2 Overview of Entomopathogenic nematodes .........................................83 3.1.2.1 Biology of Entomopathogenic nematodes ..............................87
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  • Post-Feeding Physiology in Rhodnius Prolixus: the Possible Roles of Calcitonin-Like Diuretic Hormone (Or DH31) and Fglamide-Related Allatostatins

    Post-Feeding Physiology in Rhodnius Prolixus: the Possible Roles of Calcitonin-Like Diuretic Hormone (Or DH31) and Fglamide-Related Allatostatins

    Post-feeding physiology in Rhodnius prolixus: The possible roles of calcitonin-like diuretic hormone (or DH31) and FGLamide-related allatostatins by Meet Zandawala A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Department of Cell and Systems Biology University of Toronto © Copyright by Meet Zandawala 2014 Post-feeding physiology in Rhodnius prolixus: The possible roles of calcitonin-like diuretic hormone (or DH31) and FGLamide-related allatostatins Meet Zandawala Doctor of Philosophy Department of Cell and Systems Biology University of Toronto 2014 Abstract Unfed Rhodnius prolixus (Order: Hemiptera) are in a state of arrested development. Blood- gorging results in short-term physiological/endocrinological changes that are essential to the survival of the insect, and also triggers several crucial developmental processes such as molting, growth and reproduction. Two neuropeptides that potentially play a role in this post-feeding physiology are FGLamide-related allatostatins (FGLa/ASTs) and calcitonin-like diuretic hormone (CT/DH). In order to determine the roles of these neuropeptides, I cloned and characterized their cDNA sequences and those of their cognate G protein-coupled receptors. I showed that both these neuropeptides are predominantly expressed in the central nervous system and are capable of being released into the haemolymph as hormones following feeding. I have also characterized two functionally different receptors for Rhopr-CT/DH, for the first time in any insect, and one receptor for Rhopr-FGLa/ASTs. Spatial expression analyses of these receptor transcripts revealed a wide distribution of the receptors in tissues associated with post-feeding physiology. Examination of their physiological effects using various biological assays revealed that these two neuropeptides may play indirect roles, but not direct roles during the rapid post- ii feeding diuresis and also may be involved with long term physiological changes such as metamorphosis and egg production.