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Evolutionary Perspective of Nicotine to Nornicotine Conversion, Its Regulation and Characterization of Ein2 Mediated Ethylene Signaling in Tobacco

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University of Kentucky UKnowledge University of Kentucky Doctoral Dissertations Graduate School 2010 EVOLUTIONARY PERSPECTIVE OF NICOTINE TO NORNICOTINE CONVERSION, ITS REGULATION AND CHARACTERIZATION OF EIN2 MEDIATED ETHYLENE SIGNALING IN TOBACCO Manohar Chakrabarti University of Kentucky, [email protected] Right click to open a feedback form in a new tab to let us know how this document benefits ou.y Recommended Citation Chakrabarti, Manohar, "EVOLUTIONARY PERSPECTIVE OF NICOTINE TO NORNICOTINE CONVERSION, ITS REGULATION AND CHARACTERIZATION OF EIN2 MEDIATED ETHYLENE SIGNALING IN TOBACCO" (2010). University of Kentucky Doctoral Dissertations. 88. https://uknowledge.uky.edu/gradschool_diss/88 This Dissertation is brought to you for free and open access by the Graduate School at UKnowledge. It has been accepted for inclusion in University of Kentucky Doctoral Dissertations by an authorized administrator of UKnowledge. For more information, please contact [email protected]. ABSTRACT OF DISSERTATION MANOHAR CHAKRABARTI The Graduate School University of Kentucky 2010 EVOLUTIONARY PERSPECTIVE OF NICOTINE TO NORNICOTINE CONVERSION, ITS REGULATION AND CHARACTERIZATION OF EIN2 MEDIATED ETHYLENE SIGNALING IN TOBACCO ABSTRACT OF DISSERTATION A dissertation submitted in partial fulfillment of the requirements for the Doctor of Philosophy in Plant Physiology in the College of Agriculture at the University of Kentucky By Manohar Chakrabarti Lexington, Kentucky Director: Dr. Sharyn E. Perry, Associate Professor of Plant and Soil Sciences Lexington, Kentucky 2010 Copyright © Manohar Chakrabarti 2010 ABSTRACT OF DISSERTATION EVOLUTIONARY PERSPECTIVE OF NICOTINE TO NORNICOTINE CONVERSION, ITS REGULATION AND CHARACTERIZATION OF EIN2 MEDIATED ETHYLENE SIGNALING IN TOBACCO Nicotine, nornicotine, anabasine and anatabine are four major alkaloids in tobacco, of which nicotine is predominant. In many tobacco cultivars and also in other Nicotiana species, nicotine is converted to nornicotine, which in turn gives rise to potent carcinogen NNN. Nicotine to nornicotine conversion via nicotine-N-demethylation is mediated by the CYP82E family of P450 enzymes. Tobacco (Nicotiana tabacum) converts in senescing leaves, while its diploid progenitors N.tomentosiformis and N.sylvestris convert in both green and senescing and only in senescing leaves, respectively. Previously it has been shown that N.tomentosiformis has different active conversion loci in green and senescing leaves. The green leaf conversion enzyme CYP82E3 is inactivated in tobacco by a single amino acid substitution, while the senescing leaf converter enzyme CYP82E4 is active in tobacco, which gave tobacco a ‘senescing leaf converter’ phenotype. In nonconverter tobacco, CYP82E4 shows transcriptional silencing. The nicotine-N-demethylase gene NsylCYP82E2 involved in nicotine to nornicotine conversion in senesced leaves of N. sylvestris was isolated. NsylCYP82E2 is active in N. sylvestris, but it has become inactivated in tobacco through mutations causing two amino acid substitutions. The conversion factor from N.sylvestris was characterized and a model for the alkaloid profile evolution in the amphidiploid N.tabacum from its diploid progenitors was proposed. Regulation of conversion phenomenon was tested under different spatio-temporal conditions and various stresses. The promoter region for NtabCYP82E4 was isolated and promoter-reporter construct was used to determine that NtabCYP82E4 is specifically induced only during senescence. This pattern correlates with the nornicotine accumulation as measured by alkaloid profiling. Thus the regulatory regions of NtabCYP82E4 represent a senescence specific promoter. In another project functional characterization of tobacco EIN2 (NtabEIN2) was undertaken. EIN2 from tobacco and N.sylvestris were cloned, their genomic structure was deduced and NtabEIN2 was silenced using RNAi approach. Silenced plants showed significant delay in petal senescence and abscission; as well as anther dehiscence, pod maturation, pod size, seed yield and defense against tobacco hornworm. Mechanism of delayed petal senescence phenotype, including possible cross-talk with Auxin Response Factor 2 and potential involvement of tasiRNA3 were also investigated. KEYWORDS: Nicotine to nornicotine conversion, Polyploidy and gene silencing, Senescence- associated-genes, Ethylene, EIN2 Manohar Chakrabarti February, 2010 EVOLUTIONARY PERSPECTIVE OF NICOTINE TO NORNICOTINE CONVERSION, ITS REGULATION AND CHARACTERIZATION OF EIN2 MEDIATED ETHYLENE SIGNALING IN TOBACCO By Manohar Chakrabarti Dr. Sharyn E. Perry Director of Dissertation Dr. Arthur G. Hunt Director of Graduate Studies February, 2010 RULES FOR THE USE OF DISSERTATIONS Unpublished dissertation submitted for the Doctor’s degree and deposited in the University of Kentucky Library are as a rule open for inspection, but are to be used only with due regard to the rights of the authors. Bibliographical references may be noted, but quotations or summaries of parts may be published only with the permission of the author, and with the usual scholarly acknowledgements. Extensive copying or publication of the dissertation in whole or in part also requires the consent of the Dean of the Graduate School of the University of Kentucky. A library that borrows this dissertation for the use by its patrons is expected to secure the signature of each user. Name Date DISSERTATION Manohar Chakrabarti The Graduate School University Of Kentucky 2010 EVOLUTIONARY PERSPECTIVE OF NICOTINE TO NORNICOTINE CONVERSION, ITS REGULATION AND CHARACTERIZATION OF EIN2 MEDIATED ETHYLENE SIGNALING IN TOBACCO DISSERTATION A dissertation submitted in partial fulfillment of the requirements for the Doctor of Philosophy in Plant Physiology in the College of Agriculture at the University of Kentucky By Manohar Chakrabarti Lexington, Kentucky Director: Dr. Sharyn E. Perry, Associate Professor of Plant and Soil Sciences, Lexington, Kentucky 2010 Copyright © Manohar Chakrabarti 2010 DEDICATION This dissertation is dedicated to the memory of two very special people, who have significant influence in my life- my grandfather Sri Gour Chandra Chakrabarti and my teacher Dr. Pranab Kumar Gayen ACKNOWLEDGEMENTS My journey at the University of Kentucky would not have become fruitful without the advice and assistance of some special persons. I am really indebted to Dr. Balazs Siminszky for providing me an opportunity to pursue my doctoral research in his lab and for his constant support for helping me to have a grasp of basic molecular biology and to develop the ability to think independently. I am grateful to Dr. Sharyn Perry for her untiring support both before and after I joined her lab. Special thanks to Dr. Perry for accommodating me in her lab, when I was in need. I would like thank Dr. Lowell Bush for his advice and suggestion regarding my projects and also I would like to acknowledge his lab’s generous help with the alkaloid analysis. I am grateful to my committee members Dr. David Hildebrand and Dr. Subba Reddy Palli for their valuable suggestions on my research. I am thankful to Dr. Carol Baskin for agreeing to serve as external examiner for my defense. I would like to thank Dr. Guiliang Tang and his lab for helping me to gain some expertise on small RNA research. I would like to acknowledge the help from Dr. Ralph Dewey’s lab at North Carolina State University. Thanks to Dr. Robert Geneve and his lab for helping me with microscopy and ethylene experiments, and Plant Disease Diagnostic Lab for assisting with the pathogen identification. I am grateful to Dr. Michael Barrett and William Witt for allowing me to use the weed science lab and greenhouse space. I would like to thank all my lab members, including Lily Gavilano, Nicholas Coleman, Karen Meekins and Brittany Swatzel from Siminszky lab, and Yumei Zheng and Kate Mitchell from Perry lab. I am grateful to the Department of Plant and Soil Sciences for providing me graduate research assistantship and for funding my research. I would like to thank all my teachers, staffs of the Department of Plant and Soil Sciences and my friends at UK for their help during my tenure at UK. Special thanks to Dr. Sitakanta Pattanaik for his constant support both in professional and personal spheres. I learned a lot from him, which will help me to evolve as a better researcher in future. Finally, I would like to thank my parents, sister and brother-in-law for their constant support for all through these years. Without their help I could not even think of making up to this level today. iii Table of Contents Acknowledgements………………………………………………………………………………... iii Table of contents……………………………………………………………………………………iv List of tables……………………………………………………………………………..................vii List of figures……………………………………………………………………………………. viii List of files………………………………………………………………………………………… x Chapter 1. Literature Review………………………………………………………………………. 1 1.1. Tobacco alkaloids……………………………………………………………………..1 1.1.1. Alkaloid profile in the genus Nicotiana…………………………………………. 1 1.1.2. Biosynthesis of nicotine and nicotine related alkaloids…………………………. 2 1.1.3. Tobacco and health issues………………………………………………………. 4 1.1.4. Early years of nicotine to nornicotine conversion research…………...........…… 6 1.1.5. Biochemical and molecular characterization of N demethylation of nicotine.......8 1.1.6. Cytochrome P450s in alkaloid biosynthesis…………………………………….10 1.1.7. Spatio-temporal distribution of nicotine to nornicotine conversion…………… 13 1.2. Ethylene: biosynthesis,
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