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Abstract Regulation of Methyl Farnesoate During the Life History of the Tadpole Shrimp, Triops Longicaudatus

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Abstract Regulation of Methyl Farnesoate During the Life History of the Tadpole Shrimp, Triops Longicaudatus ABSTRACT REGULATION OF METHYL FARNESOATE DURING THE LIFE HISTORY OF THE TADPOLE SHRIMP, TRIOPS LONGICAUDATUS Methyl farnesoate (MF) is a terminal effector in crustaceans but is the immediate precursor to Juvenile Hormone III (JH) in insects. The insect JH model is well established and is commonly used for comparison with MF functions in crustaceans. MF and JH have two primary effects; to inhibit the differentiation of adult structures maintaining larval morphology, and to enhance reproduction in adults. MF is degraded by MF esterase (MFE). Studies in insects maintain that the rate of JH degradation is inversely related to JH titer. However, there exist no comprehensive studies of MFE activity in crustaceans. Previous studies have demonstrated that dietary MF administration on the tadpole shrimp, Triops longicaudatus (Crustacea: Branchiopoda), will delay gonad growth and oocyte development. We have assayed the rates of MF degradation by MFE throughout the life history of the tadpole shrimp, as well as following the administration of dietary MF. We have found that MFE levels are low in young juveniles but rise near maturity, supporting the function of MF as a juvenilizing factor in this organism. In adults, we find that MFE is inversely correlated with reproductive output supporting the function of MF as an enhancer of reproduction. Dietary MF suppressed MFE rates in late juveniles supporting the observed physiological effects of previous studies, as well as suggesting that the tadpole shrimp does not develop resistance to dietary MF. Michael Ray Gledhill August 2010 REGULATION OF METHYL FARNESOATE DURING THE LIFE HISTORY OF THE TADPOLE SHRIMP, TRIOPS LONGICAUDATUS by Michael Ray Gledhill A thesis submitted in partial fulfillment of the requirements for the degree of Master of Science in Biology in the College of Science and Mathematics California State University, Fresno August 2010 APPROVED For the Department of Biology: We, the undersigned, certify that the thesis of the following student meets the required standards of scholarship, format, and style of the university and the student's graduate degree program for the awarding of the master's degree. Michael Ray Gledhill Thesis Author Brian Tsukimura (Chair) Biology Larry Riley Biology Joy J. Goto Chemistry For the University Graduate Committee: Dean, Division of Graduate Studies AUTHORIZATION FOR REPRODUCTION OF MASTER’S THESIS X I grant permission for the reproduction of this thesis in part or in its entirety without further authorization from me, on the condition that the person or agency requesting reproduction absorbs the cost and provides proper acknowledgment of authorship. Permission to reproduce this thesis in part or in its entirety must be obtained from me. Signature of thesis writer: ACKNOWLEDGMENTS I would like to thank all of the people that contributed to this research. I would first like to thank my advisor, Dr. Brian Tsukimura, for his feedback, guidance, patience, and support. I would also like to thank my committee members, Drs. Larry Riley and Joy Goto, for their feedback, time, and generosity. I would also like to thank the members of my lab who contributed to portions of this project: Mike Tran, Nagaraju Kotagiri, Vanessa Gonzales, Marcos Duran, Alan Terusaki, and Jake Weins. Thank you for your patience during lab meetings, and helping when needed. Thank you Teresa Lee and family for all of the aid and support you provided. Funding for this project was provided by many generous donors. First and foremost, the California Agricultural Technology Institute made this study possible. This project was further funded by The College of Mathematics and Science and the Department of Biology at CSU, Fresno, the California Rice Research Board, the Crustacean Society, and the Society for Integrative and Comparative Biology. And finally, thank you Mike Erins for graciously allowing us access to your rice field to collect soil and animals. TABLE OF CONTENTS Page LIST OF TABLES . vii LIST OF FIGURES . viii INTRODUCTION . 1 Arthropod Juvenilizing and Reproductive Factors . 1 Juvenile Hormone Model . 4 Methyl Farnesoate . 5 Class Branchiopoda . 6 Tadpole Shrimp . 9 Juvenoid Regulation . 11 Study Objectives . 15 MATERIAL AND METHODS . 17 Animal Care . 17 MF Degradation Assay . 18 MF Pellet Construction . 20 Molecular Sequencing . 20 RESULTS . 25 Baseline MFE Rates of the Tadpole Shrimp . 25 MFE Rates in MF-Treated Tadpole Shrimp . 29 MF Liposome Pellets . 31 Farnesoic Acid o-Methyl Transferase . 31 DISCUSSION . 33 MFE Regulation during Normal Development of Tadpole Shrimp . 33 Effect of Exogenous MF on MFE Activity in T. longicaudatus . 38 vi Page Tadpole Shrimp Control . 42 Origins of Branchiopoda and Insecta . 43 REFERENCES . 46 APPENDICES . 60 A. FIGURE 8 . 61 B. FIGURE 9 . 63 LIST OF TABLES Table Page 1. Various Pellet Diet Formulations . 21 2. List of Primers . 23 LIST OF FIGURES Figure Page 1. Chemical Structures and Pathway of Methyl Farnesoate and Juvenile Hormone III . 2 2. Life History of the Tadpole Shrimp, Triops longicaudatus . 10 3. Conservation of Farnesoic Acid o-Methyl Transferase (FAMeT) Sequence within Crustacea . 13 4. Rate of MF Degradation with Age . 26 5. Tadpole Shrimp Oogensis. 27 6. MFE Rate throughout Early Oogenesis . 28 7. Correlation of MFE Rate and Reproduction in Adult Tadpole Shrimp 30 8. Prolonged Food Deprivation Induces MFE and is Reversible with Feeding . 62 9. Partial FAMeT cDNA Sequence from Sicyonia ingentis . 64 INTRODUCTION Arthropod Juvenilizing and Reproductive Factors Arthropod juvenilizing factors were first discovered in the hemipteran insect, Rhodnius prolixus (Wigglesworth, 1934). Brains of young larvae transplanted into older larvae inhibited metamorphosis. The region responsible for this inhibition is the corpora allata, a group of paired organs at the base of the brain (Wigglesworth, 1940). The compound responsible for this delay in development, called juvenile hormone (JH), was later isolated (Williams, 1956). Experiments on the physiology of JH maintained that its presence in larval insects was part of the “status quo” for normal larval development (Williams, 1963). Immediately prior to metamorphosis, JH levels decline to nominal levels (Gilbert et al., 2000). Juvenile hormone also affects other physiological functions in insects. Its initial alternate role was in vitellogenesis (Wigglesworth, 1936), and was shown to directly induce vitellogenin production from the fat body and uptake into developing oocytes (Engelmann, 1970; Davey, 1981; Wyatt et al., 1987). JH is also positively correlated with other reproductive activities such as pheromone production (Blomquist and Dillwith, 1983), male courtship behavior (Loher and Huber, 1966), and female receptivity (Ringo et al., 1991). Determination of the molecular structure of JH paved the way for more precise analysis of JH titer and regulation (Röller et al., 1967). Between 1975 and 1985, at least 7 review articles were published, many of which dealt with the titer, roles, and regulation of JH in individual species (De Kort and Granger, 1981; Laufer and Borst, 1983; Tobe and Stay, 1985). There are multiple isoforms of JH, the most common being JH III, all of which share a methyl ester, a terpene chain, 2 and at least one epoxide group (Fig. 1). All isoforms of JH exhibit similar functions in metamorphosis, reproductive maturation, and behavior (Gilbert et al., 2000). Fig. 1: Chemical Structures and Pathway of Methyl Farnesoate and Juvenile Hormone III. In crustaceans, pro-reproductive effectors were discovered through experimentation in aquaculture. In 1905, surgical removal, or ablation, of the eyestalk was found to increase the frequency of molting (Zeleny, 1905). This procedure was also found to enhance ovarian maturation, becoming a common practice in crustacean aquaculture (Panouse, 1943; Brown and Jones, 1947, 1949). The X-organ sinus gland complex of the eyestalk was found to inhibit a paired group of organs at base of the mandibles called the mandibular organ (MO) (LeRoux, 1968). The MO is now known to secrete pro-reproductive effectors (Laufer et al., 1987; Borst and Tsukimura, 1991; Tsukimura, 2001). 3 It was presumed that the major secretory product of the MO in crustaceans would be a JH analog, similar to insects. However, no isoforms of JH were found in crustaceans (Laufer et al., 1987; Chang, 1993). It was determined that methyl farnesoate (MF), the precursor to JH III in insects, was the terminal hormone in this pathway and a secretory product of the MO (Laufer et al., 1987; Borst et al., 1987). The two terpenoids differ only by an epoxide group (Fig. 1). Therefore, it appears that during the evolutionary development of insects and crustaceans, insects derived an additional step in this pathway, while crustaceans continued to use MF. MF does not appear to accumulate in or be secreted from insect corpora allata, suggesting that the conversion of MF to JH III is not a rate limiting step in JH synthesis (Tobe and Stay, 1977). Although the epoxide group increases the polarity and therefore solubility in hemolymph, JH binding proteins are known to be essential for the protection of JH from epoxidase and esterase enzymes while in the hemolymph (Gilbert et al., 2000). The effects of MF in crustaceans parallel the effects of JH in insects. MF has been shown to control maturation, ionic balance, embryogenesis, and reproductive activities such as oocyte development, morphogenesis, and behavior (Laufer and Biggers, 2001; Laufer et al., 2005; Lovett et al., 2006). Many crustaceans are even responsive to JH, but typically require orders of magnitude higher concentrations of JH to produce similar effects (Schneiderman and Gilbert, 1958; Gomez et al., 1973; Payen and Costlow, 1977; Hinsch, 1981; Templeton and Laufer, 1983; Hertz and Chang, 1986). Despite the similar effects, JH has been much more extensively studied than MF. This is, in no small part, due to the agricultural impact of insect pests and potential reproductive control that JH experimentation may bring. Because of 4 these physiological as well as structural similarities, MF functions are often based on the juvenile hormone model.
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