By Jonathan I. Watkinson. Virginia Polytechnic Institute and State University. Doctor of Philosophy Horticulture

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1 Characterization of two genes, trehalose-6-phosphate synthase/phosphatase and nucleotide binding protein, shown to be differentially regulated in roots of Cypripedium parviflorum var. pubescens grown with a mycorrhizal fungus Thanatephorus pennatus By Jonathan I. Watkinson Virginia Polytechnic Institute and State University Doctor of Philosophy Horticulture Dr. Gregory Welbaum (Chair) Dr. Eric Beers Dr. Richard Veilleux Dr. Orson Miller Dr. Stephen Scheckler Defense April 23, 2002 Blacksburg, VA Keywords: Sugar, symbiosis, orchid, differential display, transformation, Arabidopsis thaliana Copyright 2002, Jonathan I. Watkinson

2 Characterization of two genes, trehalose-6-phosphate synthase/phosphatase and nucleotide binding protein, shown to be differentially regulated in roots of Cypripedium parviflorum var. pubescens grown with a mycorrhizal fungus Thanatephorus pennatus Jonathan I. Watkinson Abstract The analysis of gene changes associated with formation of the mycorrhizal symbiosis between orchid and fungi could have broad implications for plant pathogen interactions. Fungi associated with North American terrestrial orchids were once included in the pathogenic genus Rhizoctonia. This suggests that orchids are able to overcome or utilize normally pathogenic pathways to establish symbioses. A differential display technique was employed to analyze gene changes in orchid in response to a fungus. Samples of RNA from roots of Cypripedium parviflorum var. pubescens (CyPP) grown in the presence or absence of a mycorrhizal fungus; Thanatephorus pennatus, were analyzed using AFLP differential display. Forty-four fragments were selected out of 5000 as being differentially expressed, but only 15 sequences were obtained. Most showed homology to ribosomal genes. Two represented genes believed to be regulated by the mycorrhizal interaction: trehalose-6-phosphate synthase/phosphatase (Tps), which showed down-regulation and nucleotide binding protein (NuBP), which showed upregulation. The Tps partial clone identifies 2100 bp at the 3' end of the gene and encodes a protein of 667 amino acids. The NuBP gene is approximately 1200bp in length and encodes a protein of 352 amino acids. The Tps gene exists in multiple copies with high expression in roots and low expression in rhizomes and leaves. The NuBP gene exists as a single copy and has a low level of expression in rhizomes and leaves. Expression of Tps is induced by sucrose, but reduced by trehalose. Cultivation of CyPP with nonmycorrhizal fungi did not affect expression of Tps or NuBP. Trehalose induced NuBP expression whereas sucrose did not. A second species of mycorrhizal fungi induced expression of NuBP but reduced expression of Tps. Analysis of Tps expression in Arabidopsis was done using promoter:gus fusions. The Tps promoter:gus plants revealed that Tps expression is constitutive in roots. Regulation of Tps driven GUS is expressed throughout seedlings. GUS was not detected in leaves of older plants but was detected in anthers and stigmatic surfaces of flowers. Expression of GUS driven by Tps showed a strong wound response and was present in the junction between siliques and pedicels. ii

3 This research was funded in part by grants from the Virginia Nurseryman's Association. Support was also provided through the Henry H. Budd award from the Virginia Agriculture Council. iii

4 Dedication I would like to dedicate this dissertation to my father, Dr. Ian Watkinson. He instilled in me the great love I have for the natural world and taught me to be curious about its many intricacies. His achievement 30 years ago has always been an inspiration to me. His many achievements since then continue to be inspirations. I hope that I can be such a mentor to my children so that they too can enjoy the wonders of this world on which we live. iv

5 Acknowledgements I would like to acknowledge the support of my advisor, Dr. Greg Welbaum. He has been invaluable in helping me to accomplish the work associated with this project. He has also broadened my professional development by allowing me the opportunity to work on grant proposals and to supervise summer interns. I would also like to thank my committee. Dr. Eric Beers, Dr. Richard Veilleux, Dr. Orson Miller and Dr. Stephen Scheckler. They have been of great assistance and have helped guide the direction of my project. I would like to thank the many people in the Horticulture department who have made my time here a fun and enriching experience. I would like to thank Maura Wood for her help with the dissertation and with many other things over the last four years. Finally, I would like to thank my wife, Christine, without whom this dissertation would not have been possible. She displayed understanding, incredible patience and support throughout. I did it for you. v

6 Two roads diverged in a wood, and I, I took the one less traveled by, And that has made all the difference. - Robert Frost vi

7 Table of Contents Abstract.ii Dedication.iv Acknowledgements.v Table of Contents vii List of Tables....ix List of Figures..x Chapter 1 Introduction: Biology of orchids and the orchid mycorrhizal interaction...1 Orchid Biology..1 Seed Germination..2 Mycorrhizal Interactions 4 Pathogenic and Symbiotic Considerations 7 Molecular Biological Considerations 8 Rationale and Sigificance..9 Chapter 2 The use of differential display to identify changes in gene expression brought about by the interaction of a mycorrhizal fungus with a North American terrestrial orchid 11 Introduction 11 Material and Methods 12 Results 16 Discussion..17 Figures 21 Chapter 3 Analysis of trehalose-6-phosphate synthase/phosphatase and nucleotide binding protein in Cypripedium parviflorum var pubescens 30 Introduction 30 Materials and Methods...31 Results 33 Discussion..35 Figures 40 Chapter 4 Analysis of expression of trehalose-6-phosphate synthase/phosphatase and nucleotide binding protein in Arabidopsis using promoter:gus fusions..53 Introduction 53 Materials and Methods 54 vii

8 Results..57 Discussion 58 Figures..61 Summary 71 References.74 Vita..85 viii

9 List of Tables Table 2-1. Random upstream primers used in fluorescence differential display..21 Table 2-2. Putative identities of genes isolated from AFLP-cDNA differential display...27 Table 3-1. Primers used for RACE and RT-PCR analysis of gene expression Table 4-1. List of components for media used to grow E. coli and Agrobacterium for use in cloning of AtTps and AtNuBP promoter:gus fusions and in in planta transformation..61 ix

10 List of Figures Figure 2-1. Agarose gel analysis to confirm amplification of cdna from imbibed and non-imbibed seeds of Goodyera pubescens using differential display PCR. 21 Figure 2-2. Fluorescence differential display of imbibed and non-imbibed seeds of Goodyera pubescens.. 23 Figure 2-3. Autoradiogram of test of AFLP-DD using roots of Epidendrum radicans 24 Figure 2-4. Autoradiogram of AFLP-DD using roots of Cypripedium parviflorum grown in the presence or absence of Thanatephorus pennatus Figure 2-5. Reamplification of differentially expressed genes..26 Figure 2-6. Confirmation of differential expression of Tps and NuBP.. 28 Figure 2-7. Analysis of mycorrhizal formation between Cypipedium parviflorum and Thanatephorus pennatus 29 Figure 3-1. RACE PCR to clone 3' ends of NuBP and Tps...41 Figure 3-2. RACE PCR to clone 5' end of NuBP and Tps Figure 3-3. Nucleotide and deduced amino acid sequence of NuBP.43 Figure 3-4. Protein sequence alignment of NuBP.43 Figure 3-5. Nucleotide and deduced amino acid sequence of Tps Figure 3-6. Protein sequence alignment of Tps. 43 Figure 3-7. Analysis of tissue level expression of NuBP and Tps...48 Figure 3-8. Expression of Tps and NuBP in roots of Cypripedium parviflorum in response to exposure to Thanatephorus pennatus...49 Figure 3-9. Expression of NuBP and Tps in response to Ceratorhiza goodyera-repentis...50 Figure Expression of Tps and NuBP in response to various sugars and fungi...51 Figure Model of trehalose as a sugar signal in carbon partitioning.52 x

11 Figure 4-1. Schematic diagram of promoter:gus constructs in pbi 121 derived binary vector that were used to visualize expression of genes identified in Cypripedium parviflorum in Arabidopsis Figure 4-2. Confirmation of AtTps promoter:gus fusion in E. coli Figure 4-3. Confirmation of AtNuBP promoter:gus fusion in E. coli.64 Figure 4-4. Confirmation of AtTps promoter:gus fusion transgene in Arabidopsis plants using PCR.65 Figure 4-5. AtTps promoter driven GUS expression in Arabidopsis seedlings and plants..66 Figure 4-6. Wound induced expression of AtTps promoter driven GUS in leaves of Arabidopsis...67 Figure 4-7. AtTps promoter driven GUS expression in Arabidopsis flowers and fruits..68 Figure 4-8. Expression of AtTps promoter driven GUS in roots of Arabidopsis grown with various sugars and a fungus (Thanatephorus pennatus)..69 Figure 4-9. AtNuBP promoter driven GUS expression in Arabidopsis flowers...70 xi

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