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Viewed by Maurel, 1997) CLONING AND CHARACTERIZATION OF GENES RELATED TO BETAINE SYNTHESIS, THE EFFECT OF SALT ON CELL DEATH, AND COMPETITION ON ATRIPLEX PROSTRATA A dissertation presented to the faculty of the College of Arts and Sciences of Ohio University In partial fulfillment of the requirements for the degree Doctor of Philosophy Li-Wen Wang August 2002 This dissertation entitled CLONING AND CHARACTERIZATION OF GENES RELATED TO BETAINE SYNTHESIS, THE EFFECT OF SALT ON CELL DEATH, AND COMPETITION ON ATRIPLEX PROSTRATA BY LI-WEN WANG has been approved for the Department of Environmental and Plant Biology and the College of Arts and Sciences by Allan M. Showalter Professor of Environmental and Plant Biology Leslie A. Flemming Dean, College of Arts and Sciences WANG, LI-WEN Ph.D. August 2002. Environmental and Plant Biology / Molecular and Cellular Biology Cloning and Characterization of Genes Related to Betaine, the Effect of Salt on Cell Death and Competition on Atriplex Prostrata (248 pp.) Director of Dissertation: Allan M. Showalter Soil salinity is a major concern to agriculture all over the world because excess salts in the soil inhibit crop growth. Halophytes such as Atriplex prostrata are able to grow and reproduce in saline environments. One of the reasons A. prostrata is salt- tolerant is that it accumulates osmoprotectants such as glycine betaine in the cytosol and sequesters Na+ and Cl- into the vacuoles. In higher plants, glycine betaine is synthesized via the two-step oxidation of choline catalyzed by choline monooxygenase (CMO) and betaine aldehyde dehydrogenase (BADH). The cDNAs encoding CMO and BADH are cloned from A. prostrata (ApCMO and ApBADH1, respectively) by RT-PCR and 3’-RACE. The composite cDNA, ApCMO, is 1669 bp long and encodes a full-length protein of 438 amino acids, with similar characteristics and a high degree of identity to other CMOs. The composite cDNA of A. prostrata BADH, designated as ApBADH1, is 1755 bp long and encodes a full- length protein of 500 amino acids. As in amaranth and in mangrove, Avicennia marina, there are two BADHs in A. prostrata. The second BADH, designated as ApBADH2, was discovered as a partial cDNA by RT-PCR. This ApBADH2 may be a peroxisomal BADH in A. prostrata. Both ApCMO and ApBADH1 expressions are salt-inducible and regulated in a developmental and organ-specific manner. However, ApCMO expression is ABA-independent while ApBADH1 expression may be ABA- dependent. The importance of glycine betaine was further demonstrated in a cell line of A. prostrata that does not express CMO. Approximately 70 % of these suspension- cultured cells die after being treated with 340 mM NaCl. NaCl also significantly reduces growth. Most of these cells are protected by exogenous addition of betaine indicated by reduced percentage of cell death and growth inhibition. In addition, NaCl-induced cell death in A. prostrata exhibits characteristics of programmed cell death. Since the growth of halophytes in a natural habitat is affected by both salinity and competition, the effects of intraspecific competition on growth and photosynthesis of A. prostrata are examined. The growth of A. prostrata from higher densities is inhibited as a consequence of reduced photosynthesis due to competition for light. Approved: Allan M. Showalter Professor of Environmental and Plant Biology 5 Acknowledgments The author would like to express her deep appreciation to Dr. Allan M. Showalter and Dr. Irwin A. Ungar for their enthusiastic guidance and encouragement throughout this research. To them and to Dr. Ivan K. Smith and Dr. Frank Horodyski I give thanks for serving on my dissertation committee and reading and editing of this manuscript. The author is indebted to Dr. Howard Dewald for advice and help on glycine betaine quantification with HPLC. I would also like to thank Dr. Shuxia Li and Dr. Ayyappan Nair for their help at earlier stage of my study. To all the other graduate students in the lab, I thank them for their interactions. I am also grateful to other faculty, staff members and graduate students in the Department of Environmental and Plant Biology and in the Molecular and Cellular Biology Program. The financial support from the department and the program is appreciated as well. Finally, I would like to thank my family and friends for their patient support. 6 Table of Contents Page Abstract................................................................................................................... 3 Acknowledgments .................................................................................................. 5 Table of Contents ................................................................................................... 6 List of Tables.......................................................................................................... 9 List of Figures.........................................................................................................11 List of Abbreviations..............................................................................................15 Chapter 1. Introduction ..........................................................................................18 1.1 Salinity: a world problem .....................................................................19 1.2 Halophytes: the solution .......................................................................20 1.3 Mechanisms of salt tolerance ...............................................................21 1.3.1 Morphological and developmental levels of salt tolerance .....21 1.3.2 Cellular and molecular levels of salt tolerance.........................23 1.4 Improvement of salt tolerance in crops ................................................33 1.5 In this research......................................................................................36 Chapter 2. Cloning and Expression of Choline Monooxygenase in Atriplex prostrata ...............................................................................................38 Abstract..........................................................................................................39 Introduction ..................................................................................................40 Material and Methods....................................................................................45 7 Page Results ...........................................................................................................53 Discussion......................................................................................................83 Chapter 3. Cloning and Expression of Betaine Aldehyde Dehydrogenase in Atriplex prostrata .................................................................................91 Abstract..........................................................................................................92 Introduction ..................................................................................................93 Material and Methods....................................................................................95 Results ...........................................................................................................101 Discussion......................................................................................................136 Chapter 4. Effects of Intraspecific Competition on Growth and Photosynthesis of Atriplex prostrata.............................................................................140 Abstract..........................................................................................................141 Introduction ..................................................................................................142 Material and Methods....................................................................................144 Results ...........................................................................................................146 Discussion......................................................................................................157 Chapter 5. Cell Death and Growth Inhibition Induced by NaCl in Suspension- Cultured Cells of Atriplex prostrata.....................................................169 Abstract..........................................................................................................170 Introduction ..................................................................................................171 8 Page Material and Methods....................................................................................173 Results ...........................................................................................................177 Discussion......................................................................................................212 Chapter 6. Summary and Conclusion.....................................................................223 Bibliography ...........................................................................................................232 Appendix I. Components in MS (M5524) and McCown’s (M6774) media ..........248 9 List of Tables Page Table 1-1. Functions and synthesis of selected osmolytes...............................28 Table 1-2. Summary of metabolic engineering for salt tolerance....................34 Table 1-3. Summary of genetic engineering with non-osmolytes for salt tolerance..........................................................................................35 Table 2-1. Primers used in cloning Atriplex
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