Functional genomics in rice (oryza sativa l) using ac ds transposon tagging system and gene expression profiling

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FUNCTIONAL GENOMICS IN RICE (ORYZA SATIVA L.) USING AC/DS TRANSPOSON TAGGING SYSTEM AND GENE EXPRESSION PROFILING RENGASAMY RAMAMOORTHY THESIS SUBMITTED FOR THE DEGREE OF DOCTOR OF PHILOSOPHY TEMASEK LIFE SCIENCES LABORATORY NATIONAL UNIVERSITY OF SINGAPORE 2008 DEDICATED TO MY FAMILY AND FRIENDS ii ACKNOWLEDGEMENTS I came to Singapore in August 2000 to work in the Rice Functional genomics laboratory at Institute of Molecular Agrobiology (IMA) as an assistant research officer (ARO). Later I started my PhD project in August 2002 at Temasek Life Sciences Laboratory (TLL) and I am very glad today that I could finish my project in appropriate time with the satisfactory outcome of my thesis. This was achieved with collaborative efforts by many people and I would like to acknowledge my sincere thanks to them. I would like to express my profound gratitude to my supervisor Dr. Srinivansan Ramachandran (Ji) for showing his confidence in me, excellent guidance and the constant supports. Ji you are a person with immense intelligence and knowledge and surely I benefited a lot from it. I enjoyed lots of freedom you gave me to design and carry out the research work which made me a very confident and self reliant researcher. It gives me great pleasure to thank and acknowledge my thesis committee members Prof. Prakash Kumar (Dept. of Biological Sciences, National University of Singapore), Dr. Hong Yan and Dr.Yin Zhong Chao (Temasek Life Sciences Laboratory) for their helpful advice and suggestions. I would like to express my sincere thanks to Prof. Venkatesan Sundaresan (Department: Biological Sciences, University of California Davis) who gave me the opportunity to work in his lab at IMA. I take this as an opportunity to thank my very best friend Dr. C. Santhosh Kumar (Group Leader, DuPont, India) who taught me the basics of plant molecular biology and rice transformation techniques, and introduced me to the IMA. I always remember his helping nature and special care to me since we met in India, iii 1995 and I thank his wife Dr. Rajani for being a good friend and her concerns on my research progress. I am deeply indebted to Dr. Jiang ShuYe, without whom this study would have been very difficult, and his stimulating discussions, advices, generous help and the fruitful collaborations which gave us a few co-authored publications. Also I acknowledge and thank Drs. Ildiko Szeverenyi and Tatiana Kolesnik who were Research fellows in our lab in early days of my PhD study with whom I worked together with in several projects of which two were published as co-authors. I am very grateful to all my colleagues who showed lots of care and friendship particularly I would like to express my gratitude and sincerely thank Dr. V. Ramesh Anbazhagan for his critical reading of my thesis, discussions and being a very good friend of mine. I enjoyed working with other colleagues and appreciate their count less help and technical supports of Mr. Nadimuthu Kumar, Prasanna Nori Venkatesh, Ma Zhigang, Lukman Hakim Md., Ms. Kum Yoke Yeong and Lim Geok Boey. I had memorable time in Rice Functional Genomic Lab in both IMA and TLL, thanks to all my former colleagues in particularly thankful to Drs. Doris Bachmann, Leina Mary Joseph, Ritu Bhalla, Mande Kumaran, Mrs. Minne Cai, Hongfen Luan, Mr. Ling Gau Wang, Ms. Peisan Luo and Zhaung Li, Mr. Mayalagu Sevugan, Thanumalayan, Bharathi and Ms. Rajini Sreenivasan. I would like to extent my note of thanks to all the attachment students and summer trainees for their helps in this project especially thankful to Ms. Vinupriya Ganapathy and Mrs. Vanitha Jeevanantham iv My special thanks to my best friends Drs. Mithilesh Mishra, Sivakumar Neelamegam, Srinivas Ramasamy, Sriram Parasuram, and Srinivasan Ramanujam who catalyzed me for venturing into PhD program and encouraged me during my course of studies and beyond. I sincerely thank all my friends Mr. Anup and Kasthurirengan, for the critical reading of thesis. Drs. Kumar, Madhumalar and Bui Thi Ngoc Ha for their attempts to help me in the protein expression, homology modeling and GC analysis, respectively, I would like to extent my thanks to Mr. Vijay Bhaskar, Ravi, Mrs. Angs, Sumathi, and Ms He fang, for their many timely helps during this project. I am sincerely thankful to all the administration staff, store personnel, DNA sequencing laboratory, SEM facilities, Computer section, Media preparation, Electrical, Security and Cleaning service. I am grateful to TLL and Temasek holdings Singapore for their financial support. It may be appropriate to remember and thank here the people who were at SPIC Science Foundation (SSF), India where I started research as my carrier. In particular, I would like the express my gratitude to Drs. K.K.Narayanan, SP.Palaniappan, and George Thomas, who were my group leaders during my five years stay there. Also I would like to extent my sincere thanks to Drs. T.S.Lokeswari, Wheeta Hopper, C.B.Nirmala and Valli Akela who were other group leaders and my well wishers. In the same time, I would like to thank all my SSF friends especially Drs. Loganathan and Saravanakumar. Most importantly, I would also like to thank my family for the support they provided me all my life and in particular, I must acknowledge and thank my wife Mrs. v Angayarkanni and my son Eswarsriram for making my life wonderful and exciting with their love and understanding. Last but not least I would like to thank God for giving me the opportunity, strength and courage to fulfill my dream. vi TABLE OF CONTENTS Title page і Acknowledgements ііi Table of contents νіi Summary xііі List of publications xviii List of figures xіx List of tables xxіi List of abbreviations xxіv CHAPTER 1: Introduction 1.1 Importance of Rice, a model plant for monocots 1.2 Rice Production and Challenges associated with it 1.2.1 Abiotic stresses 1.2.2 Biotic stresses 1.2.3 Challenges in rice production 1.2.4 Strategies to alleviate pressure on rice production 1.3 Genomics 1.4 Bioinformatics 1.5 Plant genome sequencings and annotations 1.6 Transcriptomics 1.7 Proteomics 1.8 Metabolomics 10 vii 1.9 Phenomics 11 1.10 Forward and reverse genetics 12 1.11 Types of mutagenesis to study the gene functions 13 1.12 The insertional mutagenesis: T-DNA vs Transposons 15 1.13 Transposon tagging 18 1.14 Ac/Ds transposon system for functional genomics in rice (Oryza sativa L) 19 1.15 Aim of the project 20 CHAPTER 2: Materials and methods 2.1 2.2 Plant materials 21 2.1.1 Stresses and phytohormone treatments 21 Sexual hybridizations and generation of transposants 22 2.2.1 22 Selection of Ds transposants by GFP and Basta Screens 2.3 Visible phenotype screens 23 2.4 Rescue analysis of semi-dwarf mutant with phytohormones 23 2.5 Cryo-scanning electron microscopy and cell size determinations 24 2.6 Genomic DNA extractions 24 2.7 RNA extractions and cDNA synthesis 26 2.8 Database searches and domain detection of predicted members of GRAM, RIP and WRKY domain gene families 26 2.9 Primer designing, PCR, TAIL-PCR, RT-PCR and Quantitative RT-PCR 27 2.10 Thermal asymmetric interlaced PCR (TAIL-PCR) and FSTs 36 2.11 Reciprocal PCR 36 2.12 Sequencing 36 viii 2.13 Analysis of transposition events in individual panicles 37 2.14 Molecular cloning of OsCYP96B4 gene and its promoter 40 2.15 Rice transformation using Agrobacterium tumefaciens mediated method 40 2.16 Southern blot analysis 44 2.17 Northern blot analysis 45 2.18 Protein purification and Western blot analysis 46 2.19 Histochemical staining for studying Glucuronidase expression 46 2.20 Statistical Analysis 47 2.21 Hetrologous expression of OsCYP96B4 in Schizosaccharomyces pombe 47 2.22 Lipid extraction, gas chromatography and mass spectroscopy analysis 48 CHAPTER 3: A comprehensive transcriptional profiling of three different gene families in rice 3.1 GRAM-Domain Gene Family 3.1.1 Background 49 3.1.2 Genome-wide identification of genes encoding GRAM domaincontaining proteins in rice 51 Expression profile of GRAM-domain genes in different tissues of rice under normal growth conditions 51 3.1.3 3.1.4 3.2 Expression profile of GRAM domain genes upon ABA treatment and under various biotic and abiotic stresses 57 RIP-domain gene family 3.2.1 Background 3.2.2 Genome wide identification of RIP gene family members in rice 3.2.3 Expression of OsRIP genes in different rice tissues at normal growth conditions 66 68 71 ix 3.2.4 3.3 75 WRKY Gene Family of transcription factors 3.3.1 Background 80 3.3.2 Genome wide identification of WRKY gene family members in rice 82 Expression profile of WRKY genes in different tissues at normal growth conditions by RT-PCR 84 Expression profile of WRKY genes under various abiotic and phytohormone treatments by RT-PCR analyses 86 WRKY genes regulated by abiotic stresses, phytohormones and the combinations of abiotic stress and phytohormones 90 3.3.3 3.3.4 3.3.5 3.4 Expression profile of OsRIP genes upon ABA treatment and undervarious biotic and abiotic stresses Discussion 3.4.1 Identification and highly divergent expression patterns of GRAM domain gene family 98 3.4.2 The RIP family members were ancient but not ubiquitous 99 3.4.3 Tissue-specific and stress-induced expression patterns coincide with the,developmental stages sensitive to various environmental factors 100 3.4.4 OsRIP genes may be potentially useful for developing new plant varieties with higher tolerance to various stresses 101 3.4.5 Annotation of WRKY genes in rice genome 101 3.4.6 Possible roles of WRKY genes under normal growth conditions 102 3.4.7 WRKY genes expression in response to abiotic stresses 103 3.4.8 WRKY gene signaling pathways mediated by various hormones 103 CHAPTER 4: Generation of Ds transposon lines and Ac/Ds transposition behavior in rice (Oryza sativa L) genome 4.1 Background 106 x Kurata, N., Miyoshi, K., Nonomura, K., Yamazaki, Y. and Ito, Y. 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Sundaresan and S Ramachandran Establishing an efficient Ac/ Ds tagging system in rice: large-scale analysis of Ds flanking sequences The Plant Journal (2004) 37, 301-314 xviii LIST OF FIGURES Figure 2.1 Constructs used in this study 41 Figure 2.2 Construct used for dsRNAi analyses 42 Figure 3.1A Structural organizations of three different GRAM domain-containing proteins in rice 53 Figure 3.1B Similar expression. .. of gene expressions and regulations and thus to narrow down specific genes that can combat multiple stresses 1.3 Genomics Genomics is a discipline focusing on the study of poly deoxyribonucleic acid (DNA) molecules within a single cell of an organism Genomics includes intensive 4 efforts to determine the entire set of DNA sequences and fine genetic mapping of genomes, as well as the analysis of the information... both factors, suggesting an interaction between abiotic stress and hormone signaling Based on our expression analysis, we suggest that each member from GRAM domain, RIP and WRKY gene families may play a specialized roles in a specific tissue or stress condition and may function as a regulator of environmental and hormonal signaling A two-element Ac/ Ds gene trap system was successfully established in rice. .. climatic factors, which damages many crop species and every year about two thirds of the world’s land is facing the low temperatures including freezing Cold reduces the cultivated land area as well as the growing seasons of crops including rice Cold increases the solute concentration and decreases the availability of liquid water for plant growth Low temperature affects rice in both seedling and heading... transposons silencing during the propagation of parental lines at least up to T5 generation Moreover, the stably transposed Ds element was active even at F5 generation, since Ac could remobilize Ds element as indicated by the footprint analysis of several revertants The BAR gene expression was monitored from F3 to F6 generations in more than thousand lines Strikingly, substantial transgene silencing was not... Venkatesh, Minne Cai and Srinivasan Ramachandran Genomewide survey of the RIP domain family in Oryza sativa and their expression profiles under various abiotic and biotic stresses Plant Mol Biol 67: 603-614 (2008) 2 Rengasamy Ramamoorthy, Shu-Ye Jiang, Nadimuthu Kumar, Prasanna Nori Venkatesh and Srinivasan Ramachandran A Comprehensive Transcriptional Profiling of the WRKY Gene Family in Rice under... mutagenesis techniques were used for functional genomics in rice We examined the expression profile of rice genes by transcriptomic approach to identify novel genes which were responsive to multiple stresses like abiotic and/ or biotic stresses In another approach, the maize Ac/ Ds transposable element system was utilized to generate a large pool of Ds insertion lines This thesis consists of different... observed in all the generations tested We analyzed the timing of transposition during rice development and provide evidence that Ds transposes xv late after tiller formation The secondary transposition events were ruled out by analyzing possible footprints with reciprocal PCRs Our study validates the Ac/ Ds system as a tool for large-scale mutagenesis in rice We propose that harvesting rice seeds from individual... suggesting a defect in cell elongation Flanking sequence tag analysis showed the Ds insertion into OsCYP96B4 gene This gene was devoid of intron and encoded a 60.5 kDa protein Segregation analysis revealed that the phenotype co-segregated with the Ds and revertants confirmed that the dwarf phenotype was due to the insertion of Ds element into OsCYP96B4 gene The exogenous treatment of brassinosteroid and . FUNCTIONAL GENOMICS IN RICE (ORYZA SATIVA L.) USING AC/ DS TRANSPOSON TAGGING SYSTEM AND GENE EXPRESSION PROFILING RENGASAMY RAMAMOORTHY . gene signaling pathways mediated by various hormones 103 CHAPTER 4: Generation of Ds transposon lines and Ac/ Ds transposition behavior in rice (Oryza sativa L) genome 4.1 Background 106. approaches, it is imperative to identify and functionally characterize rice genes through functional genomics. In the present investigation transcriptomics and transposon insertional mutagenesis
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