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Computer-Assisted Discovery and Characterization of Rice

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Computer-Assisted Discovery and Characterization of Rice COMPUTER-ASSISTED DISCOVERY AND CHARACTERIZATION OF RICE TRANSPOSABLE ELEMENTS INCLUDING THE FIRST ACTIVE MINIATURE- INVERTED REPEAT TRANSPOSABLE ELEMENT (MITE) by NING JIANG (Under the direction of Susan R. Wessler) ABSTRACT The availability of draft sequences for the two subspecies of rice (Oryza sativa, japonica cv. Nipponbare and indica cv. 93-11) has significantly accelerated our understanding of transposable elements in the rice genome. The research described in this dissertation was performed with the expanding rice genomic database. First, 30 Mb of rice genomic sequence was analyzed to study the insertion preference of rice miniature inverted-repeat transposable elements (MITEs), numerically the most abundant elements in rice. Among the 6600 MITEs identified, > 10% were present as nested insertions (multimers) with the proportion of multimers differing among MITE families. The data suggest possible mechanisms underlying the formation of MITE multimers. The second part of this dissertation concerns Dasheng, a novel non-autonomous long terminal repeat (LTR) element with over 1000 copies. Two hundred and fifteen elements were mapped to all twelve rice chromosomes, where more than half of the elements were located in the heterochromatic regions around centromeres. By searching 100 Mb rice genomic sequences including the almost completely assembled chromosome 1, Dasheng elements were found to have inserted five times more frequently into pericentromeric regions than other regions. These features suggest Dasheng may serve as molecular markers for this marker-poor region of the genome. Finally, 187 Mb of genomic sequence was analyzed in a computational approach to isolate the first active DNA transposons from rice and the first active MITE from any organism. The 430 bp mPing, a Tourist-like MITE, was shown to be actively transposing in a cell culture line. Database searches identified a family of related transposase- encoding elements (called Pong) that were also activated to transpose in the same cells. Virtually all new insertions of mPing and Pong elements were into low copy regions of the genome. Intriguingly, the mPing MITEs have preferentially amplified since domestication in cultivars adapted to environmental extremes, a situation reminiscent of McClintock's genomic shock theory for transposon activation. The isolation of an active MITE family and putative autonomous elements may provide a valuable tagging population for gene discovery and allow us to address long-standing questions about the mechanisms underlying the birth, spread and death of MITEs. INDEX WORDS: MITE, LTR retrotransposon, activity, insertion preference, transpson display COMPUTER-ASSISTED DISCOVERY AND CHARACTERIZATION OF RICE TRANSPOSABLE ELEMENTS INCLUDING THE FIRST ACTIVE MINIATURE- INVERTED REPEAT TRANSPOSABLE ELEMENT (MITE) By NING JIANG B.S., Najing University, China, 1983 M.S., Jiangsu Agricultural College, China, 1986 A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY ATHENS, GEORGIA 2002 © 2002 Ning Jiang All Rights Reserved COMPUTER-ASSISTED DISCOVERY AND CHARACTERIZATION OF RICE TRANSPOSABLE ELEMENTS INCLUDING THE FIRST ACTIVE MINIATURE- INVERTED REPEAT TRANSPOSABLE ELEMENT (MITE) By NING JIANG Approved: Major Professor: Susan R. Wessler Committee: Kelly Dawe Mike Scanlon Zheng-Hua Ye John McDonald Electric Version Approved: Gordhan L. Patel Dean of the Graduate School The University of Georgia August 2002 DEDICATION To my parents, for the 2000 days and nights that I couldn’t be around you. iv ACKNOWLEDGEMENTS I would like to express my deep gratitude to my major professor, Sue Wessler, for her guidance, advice, support, and patience. I am especially grateful to her for the suggestion that I switch my research focus from maize to rice, and for her tremendous help with my writing and presentation. I am also indebted to my committee members: Kelly Dawe, John McDonald, Michael Scanlon, and Zheng-Hua Ye for their valuable advice and help. I thank the past and present members of the Wessler lab: Lane Arthur, Amy Bouck, Alexandra Casa, Bo Edwards, Cedric Feschotte, Dawn Holligan, Jianping Hu, Yun Hu, Ed Kentner, Yanhong Liu, Zenaida Magbanua, Alex Nagel, Mark Osterlund, Ryan Peeler, Ellen Pritham, Tesheka Stevenson, Lakshmi Swamy, Liangjiang Wang, Qiang Zhang, and Xiaoyu Zhang for their help and friendship. Especially, I thank Dawn for her effort in maintaining the lab, Cedric for helping me with advice on literature and writing, Liangjiang and Qiang for technical assistance, and Xiaoyu for his tremendous help in almost every aspect of my research. Special thanks also to some past and current members in Dawe lab, McDonald lab, and Scanlon lab: Nathan Bowen, Suneng Fu, Evelyn Hiatt, Jiabing Ji, King Jordan, Caroline Lawrence, Gene McCarthy, Nina Schubert, Hongguo Yu, and Cathy Zhong. I am very grateful to our collaborators: Zhirong Bao and Sean Eddy (Washington University), Susan McCouch and Svieta Temnykn (Cornell University), Zhukang Cheng and Jiming Jiang (University of Wisconsin), Rod Wing (Clemson University), Jingdong v Liu and Wei Wu (Monsanto), and Hirohiko Hirochika (National Institute of Agrobiological Resources, Japan). Susan, Svieta, and Jiming are particularly helpful in sharing their knowledge, resources and technique, whereas Zhirong’s input has dramatically changed the way that I design experiments and address questions. This dissertation would be totally different without his help. I thank Orville Lindstrom and Michael Dirr for their instruction and support for my initial study in University of Georgia. Finally, I thank my husband, Ping Wang, and my son, Weitian Wang, for their love and understanding. Thanks also to my friends: David Erikson, Cong Li, Song Lin, Angie Vineyard, Yuefang Wang, Donglin Zhang and Yingxia Zhang for their help and support. vi TABLE OF CONTENTS Page ACKNOWLEDGEMENTS .................................................................................................. v CHAPTER 1. INTRODUCTION AND LITERATURE REVIEW....................................................... 1 Transposable elements are major components of eukaryotic genomes……….. ............ 2 The targeting specificity and distribution of TEs……………………………................ 4 Rice and its TEs............. ………………………………………………………………..6 Outline for this dissertation……………………………………………………............. 8 References ........... ………………………………………………………………………9 2. INSERTION PREFERENCE OF MAIZE AND RICE MINIATURE-INVERTED REPEAT TRANSPOSABLE ELEMENTS (MITES) AS REVEALED BY THE ANALYSIS OF NESTED ELEMENTS............. ………………………………………15 Introduction ............ …………………………………………………………………….16 Results ............ ………………………………………………………………………….18 Discussion ............. ……………………………………………………………………..38 Materials and Methods.............. ………………………………………………………..44 Acknowledgments.............. …………………………………………………………….48 References ............. ……………………………………………………………………..50 Supplemental data ............. ……………………………………………………………..57 vii 3. DASHENG: A RECENTLY AMPLIFIED NONAUTONOMOUS LTR ELEMENT THAT IS A MAJOR COMPONENT OF PERICENTROMERIC REGIONS IN RICE……………………………………………………………………………........ 59 Abstract………………………………………………………………………... ........ 60 Introduction…………………………………………………………………… ......... 61 Materials and Methods………………………………………………………............ 63 Results and Discussion………………………………………………………............ 68 Acknowledgments……………………………………………………………........... 94 Literature Cited……………………………………………………………….. ......... 95 4. AN ACTIVE DNA TRANSPOSON FAMILY IN RICE……………………......... 103 Abstract………………………………………………………………………... ...... 104 Introduction……………………………………………………………………. ...... 105 Results…………………………………………………………………………. ...... 106 Discussion…………………………………………………………………….. ....... 121 Methods………………………………………………………………………......... 125 References……………………………………………………………………... ...... 128 Acknowledgments……………………………………………………………......... 132 Supplemental data…………………………………………………………….. ....... 134 5. CONCLUDING REMARKS (CONCLUSIONS)………………………………… 136 Study TEs in the genomic era……………………………………………. .............. 137 Target site preference of TEs in the rice genome………………………….............. 141 References………………………………………………………………… ............. 144 viii APPENDIX P INSTABILITY FACTOR: AN ACTIVE MAIZE TRANSPOSON SYSTEM ASSOCIATED WITH THE AMPLIFICATION OF TOURIST-LIKE MITES AND A NEW SUPERFAMILY OF TRANSPOSASES…………………………………......... 145 ix CHAPTER 1 INTRODUCTION AND LITERATURE REVIEW 1 Transposable elements are major components of eukaryotic genomes Transposable elements (TEs) are DNA sequences capable of moving from one locus to another within their host genomes. Originally discovered by Barbara McClintock in the 1940s (McClintock, 1948; McClintock, 1949), TEs have been found in the genomes of all organisms tested (Capy et al., 1998). On the basis of their transposition mechanisms, TEs fall into two classes. Class I elements are characterized by their movement via an RNA intermediate during transposition. A DNA copy of the RNA intermediate is produced by reverse transcriptase and is integrated into a new locus in the host genome using other element-encoded proteins. Based on their structural features, class I TEs are further divided into two subclasses: LTR (long terminal repeat) elements and non-LTR elements. LTR elements, as exemplified by Ty elements in yeast (Boeke et al., 1985), have properties similar to retroviruses, including the LTR. Non-LTR elements, on the other hand, are not
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