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The Role of Auxin and Ethylene in Adventitious Root Formation in Arabidopsis and Tomato

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The Role of Auxin and Ethylene in Adventitious Root Formation in Arabidopsis and Tomato THE ROLE OF AUXIN AND ETHYLENE IN ADVENTITIOUS ROOT FORMATION IN ARABIDOPSIS AND TOMATO BY POORNIMA SUKUMAR A Dissertation Submitted to the Graduate Faculty of WAKE FOREST UNIVERSITY GRADUATE SCHOOL OF ARTS AND SCIENCES in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY In the Department of Biology May 2010 Winston-Salem, North Carolina Approved By: Gloria K. Muday, Ph.D., Advisor Examining Committee: Brenda S. J. Winkel, Ph.D., Chair Susan E. Fahrbach, Ph.D. Anita K. McCauley, Ph.D. Brian W. Tague, Ph.D. ACKNOWLEDGMENTS “Live as if you were to die tomorrow. Learn as if you were to live forever.” Mohandas Gandhi First and foremost, I would like to thank my advisor Dr Gloria Muday for all her help with scientific as well as several aspects of my graduate student life. I appreciate your constant encouragement, support, and advice throughout my graduate studies. I owe my passion for science and teaching to your incessant enthusiasm and challenges. I am grateful to my committee members, Dr Brian Tague, Dr Susan Fahrbach, Dr Anita McCauley, and Dr Brenda Winkel for their encouragement, and assistance. I am indebted to you for providing valuable suggestions and ideas for making this project possible. I appreciate the friendship and technical assistance by all my lab mates. In particular, I like to thank Sangeeta Negi for helping me with tomato research and making the lab more fun. I am grateful to Dan Lewis for his advice and help with figuring out imaging and molecular techniques, and Mary Beth Lovin for her sincere friendship and positive thoughts. I thank Hanya Chrispeels, Jonathan Isley, and Monica Jenks for being there for me everyday. I also acknowledge all the financial support for travel, facilities and opportunities provided by the Department of Biology. I am obliged to my father Sukumara Kurup, my mother Dr Sujatha, my brother Dr Kumar, my sister in law Dr Menon, my twin Dr Sukumar, and my brother in law Dr Mohanan for their relentless love, encouragement, and support. They are my ideals and I hope I can be as successful as them one day. Finally, I like to thank the higher power for guiding me, giving me strength, and for helping me making the right choices. ii TABLE OF CONTENTS ACKNOWLEDGMENTS………………………………………………………………...ii TABLE OF CONTENTS………………………………………………………………...iii LIST OF TABLES………………………………………………………………………..vi LIST OF FIGURES……………………………………………………………………...vii ABSTRACT……………………………………………………………………………...ix CHAPTER I……………………………………………………………………………….1 INTRODUCTION………………………………………………………………...1 Environmental factors regulate adventitious root formation……………...1 Development of adventitious roots………………………………………..3 Auxin transport, synthesis, and signaling regulates lateral root development……………………………………………………………….4 Positional specificity of lateral root formation……………………………7 Ethylene signaling and synthesis regulates root development…………….8 Treatment with exogenous hormones alters adventitious root formation…9 Positional specificity of adventitious root formation…………………….11 Auxin-ethylene crosstalk involved in adventitious root formation………12 Use of genetics to study adventitious root formation……………………13 Literature cited…………………………………………………………...15 CHAPTER II……………………………………………………………………………..26 Polar auxin transport mediated by ABCB19 and PIN1 regulates adventitious root formation in Arabidopsis. iii Abstract…………………………………………………………………..27 Introduction………………………………………………………………28 Results……………………………………………………………………33 Discussion………………………………………………………………..62 Methods…………………………………………………………………..69 Literature cited…………………………………………………………...75 CHAPTER III……………………………………………………………………………85 Auxin-ethylene cross talk drives adventitious root formation in Arabidopsis Abstract…………………………………………………………………..86 Introduction………………………………………………………………87 Results……………………………………………………………………92 Discussion………………………………………………………………118 Methods…………………………………………………………………123 Literature cited………………………………………………………….129 CHAPTER IV…………………………………………………………………………..136 Genetic dissection of the role of the ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato Abstract…………………………………………………………………137 Introduction……………………………………………………………..138 Results…………………………………………………………………..143 Discussion………………………………………………………………165 Methods…………………………………………………………………171 Literature cited………………………………………………………….175 iv CHAPTER V…………………………………………………………………………...183 CONCLUSION…………………………………………………………………183 Literature cited………………………………………………………………….195 APPENDIX……………………………………………………………………………..198 Introduction……………………………………………………………………..198 Results…………………………………………………………………………..200 Discussion………………………………………………………………………208 Methods…………………………………………………………………………210 Literature cited………………………………………………………………….212 CURRICULUM VITAE………………………………………………………………..213 v LIST OF TABLES Table I-I: Effect of application of different hormones on adventitious root formation...10 Table II-I: Auxin from the shoot is important for adventitious root formation………...39 Table II-II: Root excision alters ABCB19:GFP fluorescence…………………………..55 Table A-I: Changing local auxin maxima from apical end to basal end changes the position of adventitious root formation…………………………………………………203 vi LIST OF FIGURES Figure II-1: Removal of basal portion of hypocotyl and root increases adventitious root formation in Arabidopsis………………………………………………………………...34 Figure II-2: Adventitious roots emerge from pericycle tissues of the hypocotyl………35 Figure II-3: Effect of scr1 and shr1 mutations on adventitious root formation………...38 Figure II-4: The effect of IAA on adventitious root formation…………………………41 Supplemental Figure II-1: Free IAA levels…………………………………………...45 Figure II-5: Auxin signaling and transport are required for adventitious root formation…………………………………………………………………………………46 Supplemental Figure II-2: Transcript abundance of IAA signaling and IAA transport genes……………………………………………………………………………………..49 Figure II-6: PIN1 transcription and pABCB19::ABCB19:GFP protein accumulation is enhanced with excision…………………………………………………………………..53 Figure II-7: Phosphorylation regulates localization of adventitious roots……………...58 Figure III-1: Ethylene negatively affects adventitious root formation and is induced with excision…………………………………………………………………………………..93 Figure III-2: Ethylene can inhibit auxin induction of adventitious root formation……..97 Supplemental Figure III-1: Adventitious roots formed in intact or root excised in wild type and, etr1-1................................................................................................................100 Figure III-3: Ethylene inhibits IAA transport and free IAA levels in hypocotyls…….102 Figure III-4: Flavonoids are induced with excision and negatively regulates adventitious root formation…………………………………………………………………………..106 vii Figure III-5: Ethylene induces flavonoids in hypocotyls and effect of ethylene on adventitious root formation is partially dependent on flavonoids……………………...109 Supplemental Figure III-2: Relative transcript levels of CHS in Col and eto1-1…….113 Figure III-6: Ethylene regulation of auxin transport proteins mediating auxin transport required for adventitious root formation………………………………………………..115 Figure IV-1: Lateral root formation in tomato is influenced by mutations that alter ethylene signaling and synthesis. Roots were grown for 8 days on nutrient agar……...144 Figure IV-2: ACC reduces root initiation in Pearson, but not in the Nr mutant………147 Figure IV-3: Ethylene enhances adventitious root formation in tomato hypocotyls…..151 Figure IV-4: In tomato roots acropetal and basipetal IAA transport are positively regulated by ethylene…………………………………………………………………...154 Figure IV-5: Ethylene alters basipetal auxin transport in tomato hypocotyls.……………………………………………………………………………...157 Figure IV-6: In tomato roots free IAA content is reduced two days after 1 µM ACC treatment………………………………………………………………………………..160 Figure IV-7: Effect of ethylene on free IAA content in tomato hypocotyls…………...161 Figure IV-8: Nr has altered responses to auxin in both lateral and adventitious root formation………………………………………………………………………………..163 Figure V-1: Model for excision induced adventitious root formation…………………190 Figure V-II: Cell model for excision induced adventitious root formation…………...192 Figure A-1: Shifting auxin maxima from apex to base of hypocotyl explant can change the position of adventitious root formation and auxin accumulation…………………..201 Figure A-2: Acropetal auxin transport can be observed after polarity reversal………..206 viii ABSTRACT Sukumar, Poornima ROLE OF AUXIN AND ETHYLENE IN ADVENTITIOUS ROOT FORMATION IN ARABIDOPSIS AND TOMATO Dissertation under the direction of Gloria K.Muday, Ph.D., Professor of Biology Adventitious roots emerge from aerial plant tissues. Although important for clonal propagation of commercially important crop species, few studies have explored the mechanisms driving the development of these roots. This thesis research explored the hormonal controls and molecular mechanisms of adventitious root formation in Arabidopsis thaliana (Arabidopsis) and Solanum lycopersicum (tomato). Removal of the hypocotyl base and root from Arabidopsis seedlings enhanced the frequency of adventitious root formation. ACC treatment and mutations that cause enhanced ethylene synthesis reduced adventitious root formation in Arabidopsis, but enhanced adventitious root formation in tomato, with opposite effects found in ethylene insensitive mutations. These results are consistent with ethylene oppositely regulating adventitious root formation in these two species,
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