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Phosphatidylinositol-3-Kinase in Tomato (Solanum Lycopersicum. L) Fruit and Its Role in Ethylene Signal Transduction and Senescence

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Phosphatidylinositol-3-Kinase in Tomato (Solanum Lycopersicum. L) Fruit and Its Role in Ethylene Signal Transduction and Senescence Phosphatidylinositol-3-Kinase in Tomato (Solanum lycopersicum. L) Fruit and Its Role in Ethylene Signal Transduction and Senescence by Mohd Sabri Pak Dek A Thesis presented to The University of Guelph In partial fulfilment of requirements for the degree of Doctor of Philosophy in Plant Agriculture Guelph, Ontario, Canada © Mohd Sabri Pak Dek,June, 2015 ABSTRACT PHOSPHATIDYLINOSITOL-3-KINASE IN TOMATO (SOLANUM LYCOPERSICUM. L) FRUIT AND ITS ROLE IN ETHYLENE SIGNAL TRANSDUCTION AND SENESCENCE Mohd Sabri Pak Dek Co-Advisors: University of Guelph, 2015 Professor G. Paliyath Professor J. Subramanian The ripening process is initiated by ethylene through a signal transduction cascade leads to the expression of ripening-related genes and catabolism of membrane, cell wall, and storage components. One of the minor components in membrane phospholipids is phosphatidylinositol (PI). Phosphatidylinositol-3-kinase (PIK) is an enzyme that phosphorylates PI at the 3-OH position of inositol head group to produce phosphatidylinositol 3-phosphate (PI3P). Phosphorylation of PI may be an early event in the ethylene signal transduction pathway that generates negatively charged domains on the plasma membrane. PI3P domains may potentially serve as a docking site for phospholipase D (PLD) after ethylene stimulation. It is hypothesized that ethylene stimulation may activate PI3K resulting in enhanced level of phosphorylated phosphatidylinositol. However, the properties and function of PI3K is not well understood in plants. In the present study, the effect of PI3K inhibition during tomato fruit ripening was evaluated. This study demonstrated that PI3K activity is required for normal ripening process of the fruit. Inhibition of PI3K activity using wortmannin significantly reduced tomato ripening process. The inhibitory effect of wortmannin was similar in magnitude to that obtained with 1-methylcyclopropene (1-MCP), an ethylene receptor blocker. This observation was further supported by genetic modification of PI3K gene expression in tobacco via stable transformation. PI3K overexpression (OX), and downregulation of PI3K with short hairpin antisense (sh) constructs, affected ethylene biosynthesis in flowers. PI3K OX resulted in increased levels of ethylene production and accelerated flower senescence. Meanwhile, down regulation of PI3K inhibited ethylene biosynthesis and prolonged the flower shelf life. Subcellular localization by GFP fluorescence in transgenic plants showed that PI3K was preferentially localized at the plasma membrane, nucleolus and inner part of stomata, based on the tissue. Further characterization of PI3K C2 domain revealed that this protein could bind to all phosphoinositides including PI, and its own phosphorylated products. This suggests that PI3K C2 domain enables the translocation of PI3K from cytosol to plasma membrane, and potentially other endomembranes. In conclusion, PI3K activity is required for fruit ripening, potentially acting via membrane phospholipid catabolism in conjunction with PLD, and releasing the downstream signal transduction process from suppression by CTR. Key words: C2 domain. ethylene, phosphatidylinositol 3-kinase, ripening, senescence, signal transduction, tomato iv In the name of God and Beloved Prophet Peace and Blessings be Upon Him… v ACKNOWLEDGEMENTS First and foremost, all gratitude goes to the God, who has given me the chance and capability to complete this research. I would like to express my deepest gratitude to my advisor and my co-advisor, Professor Gopinadhan Paliyath and Professor Jayasankar Subramanian and for giving me an opportunity to work in their laboratory, their guidance, suggestions, and patience throughout the research. My sincere thank goes to Dr. Sherif Sherif, Dr. Priya Padmanabhan, and Dinesh Kumar Selvaraj for valuable discussions and providing suggestions during my research. I also extend my gratitude to Professor. Marica Bakovic and Dr. Jim Todd for participating in my PhD advisory committee. Their valuable suggestions and constructive criticisms made my research become smoother and more productive. To my beloved lab mates, Ramany Paliyath, Valsala Kallidumbil, Dr. Krishnaraj Tiwari, Dr. Ajila Chandran Matheyambath, Renu Chandrasekaran, Dr. Azizah Misran, and Dr. Julieta Correa-Betanzo, thanks for all the moments and support that we have shared in the lab as a family. My thanks to all professors in Plant Agriculture Department, in particular, Dr Praveen Saxena, Dr. Katerina Jordan, Dr. Gale Bozzo, Dr. Barry Shelp and Dr. Manish Raizada for allowing me to work in their labs, and for the valuable help from their staff and students. My thanks go to my sponsor, Government of Malaysia and Universiti Putra Malaysia for awarding a scholarship and approving my study leave. My thanks go to others sponsors including Manton Memorial Scholarship and June and Keith Leaver Scholarship from the OAC, University of Guelph. Last but not least, to all my family and friends, in particular, my lovely wife Adilah and daughter, Aisyah, my dad and mom, all brothers and sisters, thanks for your love and support. Finally, thanks to everyone who helped me to make this research, a success. vi TABLE OF CONTENTS ABSTRACT ii ACKNOWLEDGMENTS v TABLE OF CONTENTS vi LIST OF TABLES xi LIST OF FIGURES xii LIST OF ABBREVIATIONS xviii PAGE INTRODUCTION xxi Research Hypothesis xxvii Research Objectives xxvii CHAPTER I LITERATURE REVIEW 1 1.1 Ripening and senescence in fruits 1 1.2 Signal transduction during ripening 3 1.3 Inhibition of ethylene-regulated gene expression during fruit ripening 8 1.4 The function and roles of biomembrane in ripening and senescence 12 1.5 Phosphatidylinositol metabolism in senescence 16 1.6 Mammalian phosphatidylinositol 3-kinase (PI3K) 24 1.7 Phosphatidylinositol 3-kinases (PI3K) in plant growth and development 26 1.8 Structural characterization of plant phosphatidylinositol 3-kinase 29 1.9 Inhibition of phosphatidylinositol 3 kinase by wortmannin 32 CHAPTER II 34 EFFECT OF PHOSPATIDYLINOSITOL 3-KINASE INHIBITION DURING 34 SOLANUM LYCOPERSICUM (TOMATO) RIPENING 2.1 Introduction 34 2.2 Materials and Methods 39 vii 2.2.1 Fruit materials and treatments 39 2.2.2 Measurement of ethylene and respiration rate 40 2.2.3 Firmness 41 2.2.4 Tomato colour index 41 2.2.5 Lycopene 41 2.2.6 Weight loss 42 2.2.7 Real time-polymerase chain analysis 42 2.2.8 Statistical analysis 45 2.3 Results 45 2.3.1 Phosphatidylinositol related gene expression during 45 tomato fruit ripening 2.3.2 Physiological changes in tomatoes during storage 47 2.3.3 Colour index 47 2.3.4 Firmness 50 2.3.5 Ethylene production 50 2.3.6 Respiration 53 2.3.7 Lycopene content 53 2.3.8 Weight loss 56 2.3.9 Quantitative analysis of gene expression by Real-time PCR 56 2.3.10 Expression analysis of genes involved in ethylene biosynthesis 56 2.3.11 Expression analysis of genes involved in ethylene 61 signal transduction 2.3.9.3 Expression analysis of genes involved in 64 carotenoid biosynthesis 2.3.9.4 Expression analysis of genes involved in PI metabolism 67 2.4 Discussion 70 viii 2.4.1 Comparison of physiological changes on tomatoes in 70 response to wortmannin, hexanal and 1-MCP treatments 2.4.2 Genes involved in ethylene biosynthesis and signaling 73 2.4.3 Differences in the expression of genes involved in 74 phospholipid metabolism 2.4.4 Proposed mechanism of inhibition of PI3K mediated 75 inhibition/suppression of ripening and senescence 2.5 Conclusions 77 CHAPTER III 78 MODULATION OF Sl-PHOSPHATIDYLINOSITOL 3-KINASE (Sl-PI3K) 78 ENHANCES ETHYLENE BIOSYNTHESIS AND SENESCENCE IN NICOTIANA TABACUM 3.1 Introduction 78 3.2 Materials and Methods 81 3.2.1 Total RNA extraction and cDNA synthesis 81 3.2.2 Construction of the PI3K overexpression vector 81 and short-hairpin antisense plasmids 3.2.3 Agrobacterium tumefaciens-mediated transformation 83 3.2.4 Triple-response assay 83 3.2.5 Ethylene measurement 84 3.2.6 Extraction and genomic DNA 84 3.2.7 Gene expression analyses 84 3.2.8 Subcellular localization of PI3K 84 3.2.9 Statistical Analyses 85 3.3 Results 85 3.3.1 Cloning of Solanum lycopersicum PI3K cDNA 85 ix 3.3.2 Subcellular localization of PI3K in tobacco seedlings 88 3.3.3 PI3K expression and developmental characteristics of 92 tobacco flowers 3.3.4 Developmental and senescence characteristics of flowers 94 3.3.5 Ethylene production from tobacco flowers 97 3.3.6 Ethylene-related gene expression analysis 99 3.3.7 Triple response in tobacco seedlings 101 3.4 Discussion 101 3.4.1 PI3 Kinases in plants 101 3.4.2 Cloning and characterization of Solanum lycopersicum PI3K 104 3.4.3 PI3K in ethylene signal transduction 105 3.4.4 Subcellular localization of PI3K 108 3.5 Conclusions 112 CHAPTER IV 113 CHARACTERIZATION OF SOLANUM LYCOPERSICUM (TOMATO) 113 PHOSPHATIDYLINOSITOL 3-KINASE C2 DOMAIN 4.1 Introduction 113 4.2 Materials and Methods 118 4.2.1 Total RNA extraction and cDNA synthesis 118 4.2.2 Construction of PI3K C2 domain plasmid 118 4.2.3 Expression and purification of the PI3K C2-His domain 119 4.2.4 PI3K C2 domain binding measurement with phospholipid 120 strip and array 4.2.5 Effect of calcium and pH on PI3K C2 domain conformation 121 changes x 4.2.6 Transient expression of Sl-PI3K:GFP 122 4.2.7 Conformational analysis of PI3K C2 domain 123 4.2.8 Statistical Analyses 123 4.3 Results 123 4.3.1 Cloning and expression of Sl-PI3K C2 domain 123 4.3.2 Phospholipid binding properties 125 4.3.3 Effect of calcium and pH on lipid binding affinity of the 127 PI3K-C2 domain 4.3.4 Effect of calcium and pH on the Sl-PI3K C2 domain conformation 131 4.3.5 Subcellular localization of Sl-PI3K 131 4.3.6 Structural analysis of Sl-PI3K C2 domain 134 4.4 Discussion 140 4.5 Conclusion 153 CHAPTER V 155 GENERAL CONCLUSION AND FUTURE RECOMMENDATIONS 155 REFERENCES 158 APPENDIX 210 xi L IST OF TABLES Table 2.1.
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