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Cyanide Metabolism, Postharvest Physiological Deterioration and Abiotic Stress Tolerance in Cassava (Manihot Esculenta Crantz)

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Cyanide Metabolism, Postharvest Physiological Deterioration and Abiotic Stress Tolerance in Cassava (Manihot Esculenta Crantz) Cyanide Metabolism, Postharvest Physiological Deterioration and Abiotic Stress Tolerance in Cassava (Manihot esculenta Crantz) DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Tawanda Zidenga Graduate Program in Plant Cellular and Molecular Biology The Ohio State University 2011 Dissertation Committee: Professor Richard Sayre (Adviser) Professor Rebecca S. Lamb Professor Jyan-Chyun Jang Professor Randall Scholl Copyright by Tawanda Zidenga 2011 Abstract Cassava (Manihot esculenta Crantz) is one of the six most important crops in the world, and an important staple for more than 800 million people. Its tolerance to drought and poor soils make an important food security crop especially in sub-Saharan Africa, while its high starch content has made it attractive as a biofuel feedstock. However, cassava produces potentially toxic levels of cyanogenic glycosides and undergoes rapid postharvest physiological deterioration (PPD) within 72 hours of harvest, shortening its shelf-life. The major cyanogenic glycoside in cassava is linamarin (95%). Linamarin is made from valine in the leaves and translocated to the roots where it is believed to contribute to the reduced nitrogen pool of the plant. Linamarin in the roots is hydrolyzed during mechanical damage by linamarase to acetone cyanohydrin, which breaks down spontaneously into cyanide and acetone at pH > 5.0 or temperatures > 35°C. The first objective of this project was to analyze the activities of enzymes involved in nitrogen and cyanide metabolism in cassava in order to understand the effect of cyanogenic potential on nitrogen metabolism. We compared the activity of nitrate reductase, a key enzyme in nitrogen metabolism, in wild-type lines and transgenic low cyanogen lines. The results show that nitrate reductase activity is 3X higher in low cyanogen plants than in wild-type lines, suggesting that cyanogenesis provides a significant source of reduced nitrogen which has to be compensated for by nitrate reduction in low cyanogen plants. In addition, β-cyanoalanine synthase (CAS), nitrilase and rhodanese assays confirmed that CAS is the ii key cyanide metabolizing enzyme in cassava roots, with 3X more activity in the roots compared to shoots, while rhodanese had no detectable activity in cassava roots. We concluded from these assays that the β-cyanoalanine synthase pathway is active in cassava roots, and is likely to be the route for assimilation of cyanide into free amino acids. The second objective was to investigate the potential of redirecting cyanide from cyanogenesis in cassava roots to the production of free amino acids by overexpressing two genes involved in cyanide metabolism; CAS and nitrilase 4 (NIT4). Transgenic plants generated using each of these strategies had limitations because of effects on other pathways, which will be discussed. The third objective was to investigate the role of cyanogenesis in oxidative stress and PPD in cassava. PPD in cassava is marked by an initial oxidative burst, followed by vascular discoloration, ultimately rendering the crop unpalatable. Effective transgenic strategies for extending the shelf-life of cassava require an understanding of the causes of the early events, especially the oxidative burst. We show a causal link between cyanogenesis, which occurs upon mechanical damage in cassava, and accumulation of reactive oxygen species which trigger PPD. By measuring ROS accumulation in transgenic low cyanogen plants and as well as biochemically complementing the low cyanogens by adding 5 mM potassium cyanide, we show that the oxidative burst in cassava roots is cyanogen-induced. In light of these data, we have generated transgenic plants expressing codon-optimized Arabidopsis thaliana Alternate Oxidase (AOX), a cyanide resistant terminal oxidase in the mitochondrial respiratory chain in plants, as a strategy to control PPD by reducing the cyanide-induced ROS accumulation. The transgenic AOX plants show a 10-14X reduction in ROS iii accumulation compared to wild type plants, with at least two week extension in shelf– life. The final objective was to test these AOX transgenic lines for tolerance to abiotic stress. The production of ROS is one of the earliest detectable responses of plants to abiotic stresses. Since AOX blocks ROS accumulation, we tested the hypothesis that AOX overexpression protects cassava plants from abiotic stress. Our results show marked tolerance to waterlogging and salt stress, suggesting AOX as a strategy to extend shelf-life of cassava while providing stress tolerance. iv For my mother. v Acknowledgments I received help and support from many people during the course of this project and it will be impossible to list them all here, so first I must say thanks to everyone I interacted with for the support and encouragement. I am grateful especially to my advisor Dr. Richard Sayre for the continued guidance throughout the project, for the opportunity to be part of a great program (BioCassava Plus) and for his patience and encouragement; To my committee members; Dr. Rebecca Lamb, Dr. Randy Scholl and Dr. JC Jang for their support, suggestions and willingness to accommodate me in their schedules. I also want to thank my fellow graduate students in the lab; Anil Kumar, Zoee Perrine and Elisa Leyva-Guerrero with whom I shared many lively discussions. Thanks to the Sayre lab members past and present who have given their assistance and encouragement; Uzoma Ihemere, Sathish Rajamani, Vanessa Falcao, Shayani Peris and Narayanan Narayanan. Thanks also to Hangsik Moon, who was involved in the early part of the AOX project; Dimuth Siritunga, whose work on cyanogenesis my project rested upon; Matt Stephens, Mary-Ann Abiado, Shantha Peris and Jennifer Norris, who, at different stages kept the lab working. And to the interns I have worked with during my years in graduate school; Tony Galleinstein, Reid Rice and Solomon Afuape, not only for the help vi they offered in parts of my project, but for challenging me to refine my understanding of biology as I worked with them. I would also like to thank all the people in the facilities I have used especially the greenhouse stuff at Ohio State department of Plant Cellular and Molecular Biology (PCMB) and the Donald Danforth Plant Science Center (DDPSC), Microscopy Facilities at Ohio State and DDPSC. vii Vita August 1977 ...................................................Born, Gweru, Zimbabwe 2001................................................................B.S. Agriculture, University of Zimbabwe 2003................................................................Visiting Scholar, The Ohio State University 2004 to present ..............................................Graduate Research Associate, Department of Plant Cellular and Molecular Biology, The Ohio State University 2008 to present ..............................................Visiting Graduate Student, Donald Danforth Plant Science Center, St Louis, MO Fields of Study Major Field: Plant Cellular and Molecular Biology viii Table of Contents Abstract ............................................................................................................................... ii Acknowledgments.............................................................................................................. vi Vita ................................................................................................................................... viii List of Tables ................................................................................................................... xiv List of Figures .................................................................................................................. xvi Chapter 1: Introduction ................................................................................................. 1 1.1 Cassava and food security .................................................................................... 1 1.2 Propagation........................................................................................................... 5 1.3 Cyanogenesis ........................................................................................................ 8 1.3.1 Sources of cyanide in plants ......................................................................... 8 1.3.2 Linamarin biosynthesis and breakdown ...................................................... 11 1.3.3 Role of cyanogenic glycosides in plants ..................................................... 13 1.3.4 Translocation of linamarin .......................................................................... 14 1.3.5 Dietary cyanide causes health disorders ..................................................... 19 1.4 Postharvest physiological deterioration ............................................................. 23 1.4.1 Cassava response to wounding in comparison with other crops................. 23 ix 1.4.2 Biochemical events during cassava PPD .................................................... 25 1.4.3 Oxidative damage during PPD .................................................................... 27 1.5 Strategies for controlling PPD............................................................................ 33 1.5.1 Storage conditions ....................................................................................... 33 1.5.2 Cassava processing ....................................................................................
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