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Integration Specificity of the Retrovirus-Like Transposable Element Ty5 of Saccharomyces Sige Zou Iowa State University

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Integration Specificity of the Retrovirus-Like Transposable Element Ty5 of Saccharomyces Sige Zou Iowa State University Iowa State University Capstones, Theses and Retrospective Theses and Dissertations Dissertations 1996 Integration specificity of the retrovirus-like transposable element Ty5 of Saccharomyces Sige Zou Iowa State University Follow this and additional works at: https://lib.dr.iastate.edu/rtd Part of the Genetics Commons, Microbiology Commons, and the Molecular Biology Commons Recommended Citation Zou, Sige, "Integration specificity of the retrovirus-like transposable element Ty5 of Saccharomyces " (1996). Retrospective Theses and Dissertations. 11353. https://lib.dr.iastate.edu/rtd/11353 This Dissertation is brought to you for free and open access by the Iowa State University Capstones, Theses and Dissertations at Iowa State University Digital Repository. It has been accepted for inclusion in Retrospective Theses and Dissertations by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. INFORMATION TO USERS This manuscript has been reproduced from the microfilm master. UMI fihns the text directly fiom the original or copy submitted. Thus, some theas and dissertation copies are in typewriter &ce, vtliile others may be from ai^ type of computer printer. The quality of this reproduction is dependent upon the quality of the copy submitted. Broken or indistinct print, colored or poor quality illustrations and photographs, print bleedthrough, substandard margins, and improper alignment can adversely affect rq)roduction. In the unlikdy event that the author did not send UMI a complete nuuiuscript and there are misdng pages, these will be noted. Also, if unauthorized copyright material had to be removed, a note will indicate the deletion. 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UMI A Bell & Howell Information Company 300 North Zed) Road, Ann Aibor MI 48106-1346 USA 313/761-4700 800/521-0600 Integration specificity of the retrovirus-like transposable element Ty5 of Saccharomyces by Sige Zjoxx A dissertation submitted to the graduate faculty in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Department: Zoology and Genetics Interdepartmental Major: Molecular, Cellular and Developmental Biology Major Professor: Dr. Daniel F. Voytas Iowa State University Ames, Iowa 1996 UMI Mtunber: 9626082 UMI Microform 9626082 Copyriglit 1996, by Company. All rights reserved. Tiiis microform edition is protected against unauthorized copying under Title 17, United States Code. UMI 300 North Zeeb Road Ann Arbor, Ml 48103 ii Graduate College Iowa State University This is to certify that the doctoral dissertation of Sige Zou has met the dissertation requirements of Iowa State University Signature was redacted for privacy. mmittee Membe Signature was redacted for privacy. ommittee Jvfember Signature was redacted for privacy. CommitteVnmitteVl MemH<;r Signature was redacted for privacy. Committee Member Signature was redacted for privacy. Major Professor Signature was redacted for privacy. For the Interdepartmental Major Signature was redacted for privacy. Fo he Major Departm Signature was redacted for privacy. ra(^te College iii DEDICATION To my parents, Jian-jin Zou and Shan-ling Wu, For their instilling in me a love of doing biological research. To my wife, Hai-yin Chang, For her love and caring. To my mentor, Dr. Daniel F. Voytas, For his insight and kindness. iv TABLE OF CONTENTS ABSTRACT viii CHAPTER L GENERAL INTRODUCTION 1 The structure and organization of retroelements 3 Life cycle of retroelements 4 Consequences of retroelement integration 6 Hypotheses on the persistence of retroelements in host genomes 7 Integration specificity of retroviruses 8 Integration specificity of retrotransposons 9 Mechanisms of retroelement target specificity 10 Discovery of the S. cerevisiae retrotransposon Ty5 13 Organization of dissertation 14 References 14 CHAPTER n. THE SACCHAROMYCES RETROTRANSPOSON FAMILY, Ty5, IS ASSOCIATED WITH ORIGINS OF DNA REPLICATION AT THE TELOMERES AND THE SILENT MATING LOCUS, HMR 19 Abstract 19 Introduction 20 Materials and Methods 22 Strains 22 DNA manipulations 22 Test for DNA replication activity 23 Results 23 Distribution of the Ty5 elements in S. cerevisiae 23 S. cerevisiae Ty5 elements are associated with autonomously replicating sequences 24 Ty5 elements are of high copy number in S. paradoxus 26 V S. paradoxus Ty5 elements are associated with ACSs 26 S. paradoxus Ty5 elements are associated with ARS activity 27 Discussion 28 Possible mechanisms for Ty5 targeting 29 The association of Ty5 and telomeres 30 Acknowledgments 31 References 31 CHAPTER m. THE SACCHAROMYCES RETROTRANSPOSON Ty5 INTEGRATES PREFERENTIALLY INTO REGIONS OF SILENT CHROMATIN AT THE TELOMERES AND MATING LOCI 43 Abstract 43 Introduction 44 Results 47 Identification of full-length Ty5 retrotransposons in S. paradoxus 47 Sequence analysis of Ty5-5p and Ty5-6p 48 Transcription and transcript mapping of Ty5 50 Ty5-6p transposes in S. cerevisiae 51 Ty5-6p transposes preferentially to chromosome HI 53 Ty5-6p transposes preferentially to the telomeres and silent mating loci on chr m 54 Discussion 55 Sequence of Ty5-6p reveals unique features 55 Ty5-6p is transposition-competent 56 Silent chromatin is a target for Ty5 58 Ty5 as a class of sub-telomeric repeats 60 Materials and Methods 62 vi Strains 62 Endogenous Ty5 isolation and sequence determination 62 Analysis of Ty5 transcription 62 Ty5 transposition construct 63 Ty5 transposition assay 64 Chromosome analysis of Ty5 insertions 65 Mapping TyS insertions onto chr m 66 Acknowledgments 67 References 67 Genbank accession numbers 72 CHAPTER IV. THE SACCHAROMYCES RETROTRANSPOSON TyS INFLUENCES THE GENOMIC ORGANIZATION OF CHROMOSOME ENDS 86 Abstract 86 Introduction 87 Materials and methods 90 Strains 90 DNA manipulations 90 Mapping newly transposed TyS insertions 91 Results 91 Distribution of TyS insertions in S. paradoxus strain NRRL Y-17217 91 Duplication and rearrangement of sequences flanking TyS insertions in 5. paradoxus 92 Features of sequences flanking endogenous TyS insertions at the subtelomeric regions in S. cerevisiae 94 TyS preferentially transposes to subtelomeric regions in S. cerevisiae 96 Discussion 97 vii Ty5 is a subtelomeric repeat 97 Ty5 elements and X repeats 98 Transposable elements and the origin of subtelomeric repeats 99 Ty5 and the organization of subtelomeric regions 100 References 102 CHAPTER V. PREFERENTIAL INTEGRATION OF THE RETROTRANSPOSON Ty5 IS DETERMINED BY COMPONENTS OF SILENT CHROMATIN 113 References and notes 118 CHAPTER VI. GENERAL CONCLUSIONS 126 Ty5 preferentially transposes to silent chromatin 126 Ty5 integration is directed by silent chromatin 127 SIRS is important for Ty5 transposition 127 Comparison of Ty5 targeting with other retroelements 128 Significance of research on Ty5 targeting 129 viii ABSTRACT The retrotransposons and retroviruses display a strong preference in selecting integration sites. The molecular mechanisms underlying this process, however, are largely unknown. I have characterized a new retrotransposon, called Ty5, in diverse strains of Saccharomyces cerevisiae and related species. A functional element, Ty5-6p, was identified from S. paradoxus. To investigate Ty5 target preference, the locations of 13 native insertions were determined in S. cerevisiae and S. paradoxus. Twelve were found near the telomeres and the mating locus HMR. To determine if this distribution is a consequence of targeted integration, a Ty5 traiisposition assay was developed in S. cerevisiae using Ty5- 6p. The locations of 19 elements on chromosome m and six on other chromosomes were mapped. Twenty-two were near the telomeres and transcriptional silencers flanking HML and HMR, which share a common chromatin structure that represses transcription of adjacent genes (silent chromatin). These observations indicate that Ty5 preferentially transposes to silent chromatin. This target preference has likely had consequences for the genomic organization of chromosome ends. Recombination between elements is evidenced by the lack of target site duplications among riative Ty5 insertions. In addition, native elements mark telomeric regions that have been duplicated and rearranged in 5. cerevisiae and S. paradoxus. Molecular mechaiusms of Ty5 targeting were investigated in various mutants that affect silent chromatin. HMR-E is the cis-sequence required for assembly of silent chromatin at HMR and accounts for approximately 2% of de novo transpositions. Mutations at HMR-E, which disrupt silent chromatin, abolish Ty5 transposition to this region. Deletion of SIRS, a gene that encodes a protein component of silent chromatin. ix resulted in an approximately six fold decrease in transposition. By analogy to Ty3 and HIV, we hypothesize that Ty5 target preference is due to interactions between its integration complex and protein components of silent chromatin. Ty5 target preference extends the link between telomere structure and reverse transcription as carried
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