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The Origin and Molecular Evolution of Two Multigene Families: G-Protein Coupled Receptors and Glycoside Hydrolase Families

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The Origin and Molecular Evolution of Two Multigene Families: G-Protein Coupled Receptors and Glycoside Hydrolase Families University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Dissertations and Theses in Biological Sciences Biological Sciences, School of Fall 9-25-2013 THE ORIGIN AND MOLECULAR EVOLUTION OF TWO MULTIGENE FAMILIES: G-PROTEIN COUPLED RECEPTORS AND GLYCOSIDE HYDROLASE FAMILIES Seong-il Eyun University of Nebraska - Lincoln, [email protected] Follow this and additional works at: https://digitalcommons.unl.edu/bioscidiss Part of the Bioinformatics Commons, and the Evolution Commons Eyun, Seong-il, "THE ORIGIN AND MOLECULAR EVOLUTION OF TWO MULTIGENE FAMILIES: G-PROTEIN COUPLED RECEPTORS AND GLYCOSIDE HYDROLASE FAMILIES" (2013). Dissertations and Theses in Biological Sciences. 57. https://digitalcommons.unl.edu/bioscidiss/57 This Article is brought to you for free and open access by the Biological Sciences, School of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Dissertations and Theses in Biological Sciences by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. THE ORIGIN AND MOLECULAR EVOLUTION OF TWO MULTIGENE FAMILIES: G- PROTEIN COUPLED RECEPTORS AND GLYCOSIDE HYDROLASE FAMILIES by Seong-il Eyun A DISSERTATION Presented to the Faculty of The Graduate College at the University of Nebraska In Partial Fulfillment of Requirements For the Degree of Doctor of Philosophy Major: Biological Sciences Under the Supervision of Professor Etsuko Moriyama Lincoln, Nebraska August, 2013 THE ORIGIN AND MOLECULAR EVOLUTION OF TWO MULTIGENE FAMILIES: G- PROTEIN COUPLED RECEPTORS AND GLYCOSIDE HYDROLASE FAMILIES Seong-il Eyun, Ph.D. University of Nebraska, 2013 Advisor: Etsuko Moriyama Multigene family is a group of genes that arose from a common ancestor by gene duplication. Gene duplications are a major driving force of new function acquisition. Multigene family thus has a fundamental role in adaptation. To elucidate their molecular evolutionary mechanisms, I chose two multigene families: chemosensory receptors and glycoside hydrolases. I have identified complete repertoires of trace amine-associated receptors (TAARs), a member of chemosensory receptors, from 38 metazoan genomes. An ancestral-type TAAR emerged before the divergence between gnathostomes (jawed vertebrates) and sea lamprey (jawless fish). Primary amine detecting TAARs (TAAR1-4) are found to be older and have evolved under strong functional constraints. In contrast, tertiary amine detectors (TAAR5-9) emerged later, experienced higher rates of gene duplications, and experienced positive selection that could have affected ligand-binding activities and specificities. Expansions of tertiary amine detectors must have played important roles in terrestrial adaptations of therian mammals. During the primate evolution, TAAR gene losses are found to be a major trend. Relaxed selective constraints found in primate lineages of TAARs support dispensability of these primate genes. Reduced predator exposures owing to the start of arboreal life by ancestoral primates may attribute to this change. For another type of multigene family, glycoside hydrolase (GH) genes were identified in the western corn rootworm, Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae). Three GH family genes (GH45, GH48, and GH28) were found only in two coleopteran superfamilies (Chrysomeloidea and Curculionoidea) among insects (except for hemipteran GH28s), indicating their origin from horizontal gene transfer (HGT). Several independent HGTs in fungi and other insects were also detected. Two multigene families in this study are characterized with frequent gene duplications and losses, the birth-and-death process. A high rate of HGTs found in the GH family gene evolution must have accelerated functional evolution. In conclusion, this study showed that birth-and-death process, positive selection, and HGTs, all play a critical role in driving the evolution of multigene families and allow organismal adaptation to novel environmental niches. iv ACKNOWLEDGEMENTS First, I am very grateful to my advisor, Dr. Etsuko Moriyama and the members of Moriyama Lab in which I have interacted. They have provided a continual source of knowledge, guidance, and invaluable assistance in all phases of my doctorial career. I would like to sincere thank my committee members; Dr. Lawrence G. Harshman, Dr. Blair D. Siegfried, Dr. Jay F. Storz, and Dr. Hideaki Moriyama for their expert knowledge and comments. I also thank the financial and professional support from the Biological Sciences program at University of Nebraska-Lincoln. Finally, I want to thank my parents. Thank my wife, Eun Jeong Kim for her continual love, encouragement, and support during the preparation of this dissertation. Thank you my son, Ian Eyun for giving me lovely kisses and hugs. v TABLE OF CONTENTS Title …………………………………………………………………………………….….. i Abstract …………………………………………………………………………………… ii Acknowledgements ……………………………………………………….………..…….. iv Table of Contents ………………………………………………………………………… v List of Tables ……….....………………………………………………………..….…….. xi List of Figures …………………………………………………………………………... xii Abbreviations ..…………………………………………………………………..…........ xiv Chapter 1 Introduction …………………………………………………………………... 1 1.1 Overview of multigene family and objectives ……..……………………………... 1 1.1.1 Gene duplications and multiple family ……..……...……………………... 1 1.1.2 Concerted evolution and the birth-and-death model ………….…………... 3 1.1.3 Horizontal gene transfer ……………………………….…..……………... 4 1.1.4 Objectives of the research …………..………………..….…………..……... 5 1.2 G-protein-coupled receptors superfamily ……....………..…………………………... 6 1.2.1 Classification of GPCRs …………............................……………………... 8 1.2.2 Chemosensory receptors ………………….……………...………………... 9 1.2.3 Chemosensory organs and receptors in vertebrates and insect ……….. 11 1.2.4 Trace amine-associated receptors …………….........………………….. 13 1.2.5 Molecular evolution of CRs …………………......……………………... 16 1.2.6 Origin of GPCRs in the basal metazoan ……......……………………...... 17 vi 1.3 Glycoside hydrolase families ……………………..………………………………... 19 1.3.1 Plant cell walls degradation and cellulase ……………………….………. 19 1.3.2 Endogenous insect cellulolytic enzymes ………..……..…………….…... 21 1.3.3 Classification of glycoside hydrolases and their distribution in metazoans and insects ………………………………………..……..………………….…... 22 1.3.4 Molecular evolution and origin of insect glycoside hydrolase families .... 28 1.4 Organization of the dissertation ……………………...………..…..………………... 29 1.5 Literature cited ………………..…………………………………………….………... 31 Chapter 2 Molecular Evolution and Functional Divergence of Trace Amine– Associated Receptors ……………………………………………..……………………... 53 2.0 Abstract for Chapter 2 ………..…………………………………..…………………... 54 2.1 Background ………………………………………………………………………... 55 2.2 Results and discussion …...…………………………………………...…………... 57 2.2.1 Identification of TAAR genes ………………………….………...……... 57 2.2.2 Synteny of TAAR loci among tetrapod species ……….…….……...…... 58 2.2.3 Origin and early evolution of TAARs ……………...….………………... 58 2.2.4 Evolution of TAAR subfamilies in tetrapods ……......………………... 60 2.2.5 Therian TAAR subfamilies ………………...….………………………... 63 2.2.6 Gain and loss of TAAR genes among mammals ……....………………... 64 2.2.7 Functional differentiation among TAAR subfamilies …………………... 67 vii 2.2.8 Different evolutionary patterns in primary and tertiary detecting TAARs .………….……………………………………………….…………...…….. 68 2.2.9 Positive-selection sites are located in the potential ligand-binding sites in the TAAR proteins ……..………………………………………………... 70 2.2.10 Changes of amino acid properties in positive-selection sites ……………..………………………………………………….…….……... 72 2.3 Conclusion …………………………………………………………………….…... 73 2.4 Material and methods ………………………………………………………………... 74 2.4.1 Query and genome sequences ………….………………………………... 74 2.4.2 TAAR gene mining ………….…………………………………………... 75 2.4.3 TAAR signature motif ……………………………………………………... 76 2.4.4 Multiple sequence alignments ………………….………………………... 77 2.4.5 Phylogenetic analysis …………………………..…………………………... 78 2.4.6 Transmembrane protein topology prediction ……….…..………………... 78 2.4.7 Tests of selection patterns …….…..……………………………………... 79 2.4.8 Analysis of selection on amino acid properties …….…..……………... 80 2.4.9 Protein structural homology modeling …………………………………... 81 2.5 Acknowledgements ……………..………………………………………………..…... 82 2.6 Literature cited ……………………………………….….…………….……………... 83 viii Chapter 3 Pseudogenizations of Trace Amine–Associated Receptor Genes in Primates ......................................................................................................................... 97 3.0 Abstract …………………………………………….……………………..…......…... 98 3.1 Background …………………………………………….………………………..…... 99 3.2 Results and discussion …...……………………………….………...…………..... 100 3.2.1 Identification of TAAR genes in primates …..………….……….....….... 101 3.2.2 Phylogenetic analysis of primate TAARs ……….…….…….……...…... 101 3.2.3 Pseudogenizations of TAARs in primates …………….…………....….. 102 3.2.4 Dispensability of primate TAARs …………………......……..………... 105 3.2.5 Selection patterns among TAAR subfamilies ….………..……..……... 106 3.2.6 Different selective forces operating on TAAR subfamilies ……....…... 107 3.2.7 Positive-selection sites located in the potential ligand-binding sites ….. 108 3.3 Conclusion ……………………………………………………………..…….…... 110 3.4 Material and methods ……………………………………………………..……... 110 3.4.1 Genome sequences and TAAR gene mining …………………………... 111 3.4.2 Multiple sequence alignments and phylogenetic analysis ……………..
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