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A Study of C - Repeat Binding Factors (CBF) Associated with Low Temperature Tolerance Locus in Winter Wheat

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A Study of C - Repeat Binding Factors (CBF) Associated with Low Temperature Tolerance Locus in Winter Wheat A study of C - repeat binding factors (CBF) associated with low temperature tolerance locus in winter wheat. A Thesis Submitted to the College of Graduate Studies and Research In Partial Fulfillment of the Requirements For the Degree of Doctor of Philosophy In the Department of Plant Sciences University of Saskatchewan Saskatoon, Saskatchewan By Parul Jain © Copyright Parul Jain, April, 2013. All rights reserved PERMISSION TO USE In presenting this thesis in partial fulfillment of the requirements for a Postgraduate degree from the University of Saskatchewan, I agree that the Libraries of this university may make it freely available for inspection. I further agree that permission for copying of this thesis in any manner, in whole or in part, for scholarly purposes may be granted by professor or professors who supervised my thesis work or, in their absence, by the Head of the Department or the Dean of the College in which my thesis work was done. It is understood that any copying or publication or use of this thesis or parts thereof for financial gain shall not be allowed without my written permission. It is also understood that due recognition shall be given to me and to the University of Saskatchewan in any scholarly use which may be made of any material in my thesis. Requests for permission to copy or to make other use of material in thesis in whole or part should be addressed to: Head of the Department of Plant Sciences 51 Campus Drive University of Saskatchewan Saskatoon, Saskatchewan, Canada S7N 5A8 i ABSTRACT Winter wheat has several advantages over spring varieties, higher (25 % more) yield, efficient use of spring moisture, reduction of soil erosion by providing ground cover during the fall and early spring, rapid initial spring growth to out - compete weeds and circumvent the peak of Fusarium head blight infections by flowering early. Winter wheat is planted in early autumn when it germinates and developing seedlings acclimate to cold. The crown survives under snow cover and in spring rapidly grows into a vigorously growing plant for grain to be harvested in summer. However, the harsh Canadian prairie winters require that winter wheat has increased cold hardiness and improved winter survival to reduce losses from sudden cold snaps during winter and spring. Low temperature (LT) tolerance is one of the major components of cold hardiness. Genetic mapping studies have revealed a major quantitative trait locus (Fr-A2) at wheat chromosome 5A which can explain at least 50 % of LT tolerance in wheat. Physical mapping of 5A LT QTL in a hardy winter wheat cv Norstar revealed a cluster of at least 23 C - repeat binding factors (CBF) coinciding with peak of Fr-A2 QTL. The objective of this study is biochemical, and molecular characterization of CBF co - located at Fr-A2 to identify key CBF participating in conferring LT tolerance in winter wheat. A comparative analysis of CBF gene cluster at the Fr-A2 collinear region among Poaceae members showed an expansion in the number of CBF genes with increased LT tolerance. Rice, a cold sensitive member, had only three CBF genes, whereas cold hardy winter wheat cv Norstar has 23 CBF genes. Amino acid sequence - based cluster analysis of complete CBF genes, or their major functional components such as the AP2 - DNA binding domain and C - terminal trans - activation domain, divide Norstar CBF into Pooideae specific clades. However, analyses of Norstar CBF amino acid sequences of different functional groups revealed a shift in clade members. These results suggest divergence of CBF functions which could lead to possible differences / similarity in the regulon activated by a CBF in a specific group. The 15 CBF genes from winter wheat cv Norstar were expressed in E. coli to produce recombinant TrxHisS - CBF fusion proteins in adequate quantities for structural and functional assays. All CBF fusion proteins could be recovered in the E. coli soluble phase of cell extract, ii except that the CBF17.0 fusion protein could only be recovered with 6 M urea extraction. Eleven of the 15 CBF fusion proteins were very stable in heat (98 oC), 10 % SDS and 6 M urea treatment. The five other CBF members were very labile under native conditions, but were stable in E. coli cell extracts or when extracted under denaturing conditions. Most of the CBF recombinant proteins in denaturing gel electrophoresis migrated slower than expected from their predicted molecular mass, based on amino acid sequence. The slow migration could be associated to their elongated protein structure as determined by dynamic light scattering (DLS). CBF 12.2 and CBF 17.0 were highly resistant to denaturation and retained their secondary structure in these conditions as determined by circular dichroism (CD) spectra. The high stability of these two CBF proteins may be important for cold acclimation or maintenance of cold hardiness in wheat. CBF proteins are transcription factors that bind to the dehydration-responsive element / C-repeat element (DRE / CRT) motif (CCGAC). Ten of the 15 Norstar recombinant CBFs whether purified under native or denaturing conditions showed in vitro binding to the CRT motif. Within hours of cold exposure (4 oC) the native CBF increased their affinity to CRT interaction which could be due to changes in the CBF secondary structures. Some of the CBF for binding preferred the core GGCCGAC motif while others preferred TGCCGAC. Similarly binding assays with truncated CBF revealed that for some CBF proteins, the second signature motif (DSAWR) and remaining C - terminal were not needed, while for others a considerable portion of the C - terminal region was needed for binding. Norstar CBF 12.1 has a memory of cold experience, and upon exposure to cold, has a high and immediate affinity to CRT elements. A homolog CBF12.2 in less cold - hardy winter wheat cv Cappelle - Desprez had a non - functional protein due to a R → Q substitution in a highly conserved residue within the AP2 domain. Several of the cv Norstar CBFs showed increased activity under LT and denaturing conditions, which may be the reason for the greater cold hardiness in Norstar. In conclusion, detailed and extensive analyses of CBF in this study characterized their structure and function relationships, which are important for understanding and improving LT tolerance in plants. The identification of specific CRT binding motifs and two CBFs which were very stable under adverse conditions may be prime candidates for further study to improve LT tolerance in plants. iii ACKNOWLEDGEMENTS I sincerely thank my supervisor Dr. Ravindra N. Chibbar for his guidance, encouragement and his trust throughout the entire research project. My sincere thanks to Dr. Monica Båga for her guidance and critical inputs during my research. Also, my sincere thanks to my advisory committee members, namely, Dr. Brian Fowler, Dr. Bruce Coulman, Dr. Rosalind Bueckert and Dr. Sean Hemmingsen for their advice and constructive suggestions. I am grateful to Dr. R. Sammynaiken and Mr. Jason Maley, Saskatchewan Structural Sciences Centre, University of Saskatchewan, for their help in protein characterization studies. Financial support during my studies from Department of Plant Sciences, Canada Research Chairs program, Genome Canada, and Western Grains Research Foundation and NSERC Collaborative Research and Development grant (CRDPJ 406114-10) is gratefully acknowledged. I want to thank all my colleagues / friends in Molecular Crop Quality group for their help during my studies. I would like to thank my family for their support and encouragement. iv TABLE OF CONTENTS PERMISSION TO USE i ABSTRACT ii ACKNOWLEDGEMENTS iv TABLE OF CONTENTS v LIST OF TABLES xi LIST OF FIGURES xii LIST OF ABBREVIATIONS xv LIST OF APPENDICES xvii CHAPTER 1 1 INTRODUCTION 1 1.1 Winter wheat - low temperature (LT) tolerance 1 1.2 Hypothesis 4 1.3 Objectives 4 CHAPTER 2 5 LITERATURE REVIEW 5 2.1 Wheat 5 2.1.1 Origin and domestication of wheat 5 2.1.2 Winter wheat production in Canada 6 2.2 Assessment of cold tolerance 7 2.2.1 Winter survival in the field 7 2.2.2 Freezing tolerance tests 8 2.3 Cold and freezing injury in plants 9 2.3.1 Causes of freezing damage 9 2.3.2 Factors affecting ice nucleation 10 v 2.4 General strategies to avoid frost damage 11 2.5 Perception of low temperature 12 2.5.1 Cold sensing in non - plant species 12 2.5.2 Cold sensing in plants 13 2.6 Effect of LT stress on photosynthesis 15 2.7 Cold acclimation 17 2.7.1 Developmental traits affecting cold acclimation 19 2.7.1.1 The role of vernalization 20 2.7.1.2 The role of light conditions 22 2.7.1.3 The role of earliness per se genes 23 2.7.1.4 The role of phytohormones 24 2.8 Transcriptome adjustment during cold acclimation 28 2.9 Metabolome reprogramming during LT stress 30 2.10 COR genes in winter wheat 31 2.11 Genetic mapping of cold - tolerance traits in wheat 34 2.12 The AP2 / ERF superfamily 36 2.12.1 Transcriptional regulation of CBF expression 42 2.12.2 Post - transcriptional regulation 43 2.12.3 Translational and post - translational regulation 44 2.13 The CBF regulon 45 CHAPTER 3 48 CLUSTER ANALYSIS OF C - REPEAT BINDING FACTORS (CBFs) OF SELECTED POACEAE FAMILY MEMBERS 48 3.1 Abstract 48 3.2 Introduction 48 vi 3.3 Material and Methods 51 3.3.1 CBF sequences 51 3.3.2 Cluster analysis of CBF sequences 51 3.3.3 Hydrophobic cluster analysis (HCA) 52 3.4 Results 52 3.4.1 Comparative analysis of co - linear regions at CBF - locus in Poaceae 52 3.4.2 Amino acid - level cluster analysis of CBFs 60 3.4.3 Cluster analyses of amino terminal region 65 3.4.4 Cluster analysis on the basis of AP2 - DNA binding domain sequence 65 3.4.5 Cluster analysis on the basis of C - terminal trans - activation domain sequence 68 3.4.6 Bioinformatic analysis of wheat CBFs 68 3.4.7 Bioinformatic analysis of signature sequences 73 3.4.8 Hydrophobic Cluster Analysis (HCA) 76 3.5 Discussion 81 CHAPTER 4 85 PROPERTIES OF RECOMBINANT CBF PROTEINS PRODUCED IN ESCHERICHIA COLI 85 4.1 Abstract 85 4.2 Introduction 85 4.3 Material and Methods 88 4.3.1 E.
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