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Metabolic Engineering of Plants by Manipulating Polyamine Transport and Biosynthesis

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Metabolic Engineering of Plants by Manipulating Polyamine Transport and Biosynthesis METABOLIC ENGINEERING OF PLANTS BY MANIPULATING POLYAMINE TRANSPORT AND BIOSYNTHESIS Sheaza Ahmed A Dissertation Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY December 2017 Committee: Paul Morris, Advisor Andrew T Torelli Graduate Faculty Representative Vipa Phuntumart Scott Rogers George Bullerjahn ii ABSTRACT Paul Morris, Advisor Transport is an essential component of the regulation of polyamines, but to date only one family of Polyamine Uptake Transporters (PUTs) have been characterized in plants, and their impact on polyamine regulation has not been defined. Here we show that knockout mutants of put5 in A. thaliana, promote early flowering and result in plants with smaller leaves, thinner stems, and fewer flowers. In contrast, heterologous expression of the rice gene OsPUT1 in A. thaliana using the Put5 promoter at 22°C produced plants with larger leaves, a two-week delay of flowering and more flowers and siliques. Similar effect on leaf size, flowering time and number of siliques also were observed in transgenic plants with constitutive expression of OsPUT1 or OsPUT3. The delay of flowering was associated with significantly higher levels of spermidine and spermidine conjugates in the leaves prior to flowering. These experiments outline the first genetic evidence for the control of flowering by polyamines. How polyamine levels control the timing of flowering at a molecular level is not yet known, but this delay of flowering has been demonstrated to be upstream of the stimulation of flowering by the gibberellin and temperature sensitive response pathways. It has been assumed that there exists a single cytosolic pathway for the synthesis of putrescine in A. thaliana. Here we show that A. thaliana and Glycine max, have a chloroplast- localized putrescine biosynthetic pathway. This pathway comprises of arginine decarboxylase iii and an agmatinase to synthesize putrescine from arginine. Analysis of expression data suggests that it is the major route of putrescine synthesis in response to stress signals. Since compartmentation of polyamines has been demonstrated to play an essential role in polyamine homeostasis, the identification of other types of polyamine transporters is a critical knowledge gap. We show here that PDR11 is an important long-distance transporter of polyamines in plants and that OCT5 functions as a vacuolar transporter for polyamines. Taken , these findings will accelerate interest in manipulating polyamine metabolism to generate more stress responsive crop plants. iv Dedicated to my wonderful and loving family. v ACKNOWLEDGMENTS The last five years has been a period of intense learning for me, not only in the scientific filed, but on a personal level as well. I would like to thank all the people who have supported and helped me throughout this period. Firstly, I would like to express my sincere gratitude to my advisor Dr. Paul Morris for the continuous support and guidance during my Ph.D., for his patience, motivation, and immense knowledge. His guidance has helped me during the time of research and in writing of this dissertation. I could not have imagined having a better advisor and mentor than him. Besides my advisor, I would like to thank the rest of my dissertation committee members: Dr. Vipa Phuntumart, Dr. Scott Rogers, Dr. George Bullarjahn and Dr. Andrew Torelli for their insightful comments and encouragement, but also for the hard question which incented me to widen my research from various perspectives. I would also like to thank the faculty and staff members of the biology department for being very helpful and supportive. I thank my fellow lab mates: Dr. Jigar Patel, Dr. Lingxiao Ge, Menaka Ariyaratne, Chandra Sarkar, Nilanjana Chakrabarti and all the amazing undergraduate students who worked with me on various projects. I am extremely grateful for the stimulating discussions, endless help and support, and for all the fun we have had in the last five years. Last but not the least, I would like to thank my family: my parents and my brothers for supporting me spiritually throughout my Ph.D. and my life in general. v TABLE OF CONTENTS Page CHAPTER I. INTRODUCTION ......................................................……………………… 1 1.1. What Are Polyamines? ......................…………………………………………. 1 1.1.1. Polyamine Biosynthesis ....................................................................... 2 1.1.2. Polyamine Catabolism ......................................................................... 4 1.1.3. Polyamine Transport ............................................................................ 6 1.2. Polyamine and Development .............................................................................. 8 1.2.1. Role of spermidine in cell division ...................................................... 9 1.2.2. Role of thermospermine in vascular development............................... 10 1.3. References ........................................................................................................... 12 CHAPTER II. ALTERED EXPRESSION OF POLYAMINE TRANSPORTERS REVEALS A ROLE FOR SPERMIDINE IN THE TIMIMG OF FLOWERING AND OTHER DEVELOPMENTAL RESPONSE PATHWAYS ................................................................ 21 2.1. Abstract…………………………………………. .............................................. 21 2.2. Introduction …………………………………………………………………… 22 2.3. Methods and Materials ........................................................................................ 24 2.3.1. Plant material and growth conditions .................................................. 24 2.3.2. Phenotypic analysis .............................................................................. 25 2.3.3. Gene expression analysis ..................................................................... 26 2.3.4. GUS analysis ........................................................................................ 26 2.3.5. Subcellular localization of PUTs ......................................................... 26 2.3.6. Polyamine analysis............................................................................... 27 vi 2.3.7. Statistical analysis ................................................................................ 28 2.4. Results ............................................................................................................ 29 2.4.1. Promoter analysis of AtPUT5 .............................................................. 29 2.4.2. Subcellular localization of PUTs by transient expression in N. benthamiana ............................................................................................................ 29 2.4.3. Phenotypic changes resulting from altered expression of PUTs ......... 29 2.4.4. Constitutive expression of PUTs delays senescence ........................... 30 2.4.5. Effect of PUT expression on polyamine levels in rosette leaves ......... 31 2.4.6. Gibberellins suppress the delay of flowering in pPUT5:OsPUT1 plants 32 2.5. Discussion ........................................................................................................... 32 2.6. Acknowledgement .............................................................................................. 37 2.7. Accepted Manuscript .......................................................................................... 37 2.8. References ........................................................................................................... 39 CHAPTER III. THE EFFECT OF HIGH TEMPERATURE ON THE DELAY OF FLOWERING IN PUT5 PLANTS… ...................................................……………………. 54 3.1. Polyamines and Abiotic stresses ......................................................................... 54 3.1.1. High-Temperature Stress ..................................................................... 54 3.1.2. Low-Temperature Stress ...................................................................... 55 3.1.3. Drought Stress ...................................................................................... 55 3.1.4. High Salinity Stress.............................................................................. 56 3.2. High temperature suppresses the delay of flowering in PUT5:OsPUT1 plants . 57 3.3. References ........................................................................................................... 59 vii CHAPTER IV. DUAL FUNCTIONING OF PLANT ARGINASES PROVIDES A THIRD ROUTE FOR PUTRESCINE SYNTHESIS ............................……………………………. 65 4.1. Abstract ............................................................................................................ 65 4.2. Introduction ......................................................................................................... 66 4.3. Materials and Methods ........................................................................................ 68 4.3.1. Phyre2 analysis .................................................................................... 68 4.3.2. Phylogenetic analysis ........................................................................... 68 4.3.3. DNA sources and constructs ................................................................ 68 4.3.4. Subcellular localization analysis .......................................................... 69 4.3.5. Yeast complementation assays ............................................................ 70 4.3.6. Growth rate of yeast strains without polyamine
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