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Characterization and Gene Expression Analysis of Kazal-Type Serine Protease Inhibitors of Globisporangium Ultimum

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Characterization and Gene Expression Analysis of Kazal-Type Serine Protease Inhibitors of Globisporangium Ultimum CHARACTERIZATION AND GENE EXPRESSION ANALYSIS OF KAZAL-TYPE SERINE PROTEASE INHIBITORS OF GLOBISPORANGIUM ULTIMUM Ashok Maharjan A Thesis Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE August 2021 Committee: Vipaporn Phuntumart, Advisor Raymond Larsen Paul Morris © 2021 Ashok Maharjan All Rights Reserved iii ABSTRACT Vipaporn Phuntumart, Advisor An oomycete pathogen, Globisporangium ultimum (also known as Pythium ultimum), causes damping-off on a wide range of hosts. This disease is one of the major constraints on soybean production. Although fungicide seed treatments are often used to combat the disease, significant losses occur in cool and moist conditions. In addition, the emergence of fungicide- resistant isolates, the lack of resistant cultivars, and the ineffectiveness of crop rotations pose further challenges in managing the disease. Hence, new molecular targets are needed to control G. ultimum. In this study, G. ultimum and G. sylvaticum were isolated from the soybean fields (Bowling Green, Ohio). Pathogenicity assays were evaluated on two soybean cultivars: William and William 82. The seed-and seedling rot assays determined that both the isolates were pathogenic to both the seeds and seedlings of soybeans. Globisporangium ultimum showed a 100% disease severity index (DSI) on both cultivars, while G. sylvaticum had a DSI of 73.1% and 93% on William and William 82, respectively. The seedling root rot assay showed a similar rate of infection in both cultivars, based on the root surface area compared to the control (healthy plant). Kazal-type serine protease inhibitors (KPIs) are produced and secreted by many pathogens, including G. ultimum. They neutralize plant defense proteins in the protease family, allowing pathogens to colonize the hostile apoplast. In silico analysis via FungiDB showed that G. ultimum genome encodes 13 putative secreted KPIs. Four genes: PYU1_1G000142, PYU1_G009682, PYU1_G013310, and PYU1_G002778 were selected for gene expression iv analysis during infection using qPCR. Results showed that PYU1_1G000142 and PYU1_G009682 showed the highest expression at 48 hours post inoculation (hpi), indicating that they were associated with late infection in both soybean cultivars. In contrast, PYU1_G013310 showed highest expression at 6 hpi in William and at 24 hpi in William 82, indicating that it was associated with early and mid-infections. However, the transcripts of PYU1_G002778 could not be detected in this study, suggesting that the gene might be a pseudogene. While the specificity of these KPIs will require further experiments, nevertheless, they could be considered potential targets to control G. ultimum. v To my mother, Krishna Devi Maharjan vi ACKNOWLEDGMENTS First, I would like to remember my school, Siddhartha Secondary School (Sunakothi, Lalitpur, Nepal), where I got my schooling, and I would like to thank all my schoolteachers. I would like to thank my mother Krishna Devi Maharjan who knows the importance of education though she never got a chance to go to school. I am really honored to be a member of Dr. Phuntumart’s Lab and I am thankful to Dr. Vipaporn Phuntumart. I have learned many new techniques during my stay in the lab. Besides, I learned to develop scientific enquiries from her. Her caring and compassionate nature are always worth emulating. I am thankful to the Bowling Green State University and Dr. Zhaohui Xu for providing me an opportunity to be a part of Bowling Green State University. I would also like to express my sincere gratitude to Dr. Paul Morris and Dr. Raymond Larsen for their support and their depth of knowledge. It is always exciting to talk to them. I am thankful to my fellow lab members: Sudan Pacchain, Sarah Wagner, and Ebuka Onyenobi, and Gayathri Beligala for their suggestions and friendship. I am also thankful to Sayantan Roy Choudhury, Jyotshana Gautam, Kumud Joshi, and Carren Burkey for their help. Especially, I am grateful to Sarah Wagner for her care and support. I would like to thank my family, including Nanda Bahadur Maharjan, Singha Man Maharjan, Suroj Maharjan, and Nitesh Maharjan. vii TABLE OF CONTENTS Page CHAPTER 1. INTRODUCTION ............................................................................................ 1 1.1 Oomycetes ............................................................................................................. 1 1.1.1 Diversity and Pathology .......................................................................... 2 1.1.2 Evolution and Phylogeny ........................................................................ 4 1.1.3 Oomycete Genome .................................................................................. 5 1.1.4 Oomycete Pathogenesis ........................................................................... 8 1.2 Globisporangium ultimum: Pathogenicity and Life Cycle........... .......................... 11 1.3 Protease Inhibitors..................................................... ............................................. 13 CHAPTER 2. AIM OF THE STUDY ..................................................................................... 16 CHAPTER 3. METHODS ....................................................................................................... 18 3.1 Isolation and Identification of Globisporangium Isolates and Examination of Their Pathogenicity on Soybean Cultivars ............................................................... 18 3.1.1 Isolation of Pathogens ............................................................................. 18 3.1.2 DNA Extraction ....................................................................................... 18 3.1.3 Polymerase Chain Reaction and Sequencing .......................................... 19 3.1.4 Seed Rot Assay ........................................................................................ 20 3.1.5 Seedling Root Rot Assay ......................................................................... 21 3.2 Identification and Characterization of Kazal-Type Serine Protease Inhibitor Domains of Oomycetes ................................................................................................ 21 3.3 Expression of Selected G. ultimum Kazal-Type Serine Protease Inhibitor Genes During Infection ........................................................................................................... 23 3.3.1 Experimental Treatments ......................................................................... 23 viii 3.3.2 RNA Extraction and cDNA Synthesis .................................................... 23 3.3.3 Primer Design .......................................................................................... 23 3.3.4 Quantitative Polymerase Chain Reaction (qPCR) ................................... 24 CHAPTER 4. RESULTS ......................................................................................................... 26 4.1 Isolation and Identification of Globisporangium Isolates and Examination of Their Pathogenicity on Soybean Cultivars ................................................................... 26 4.1.1 Isolation and Identification of Pathogens ................................................ 26 4.1.2 Seed Rot Assay ........................................................................................ 27 4.1.3 Seedling Root Rot Assay ......................................................................... 29 4.2 Identification and Characterization of Kazal-Type Serine Protease Inhibitor Domains of Oomycetes ................................................................................................ 32 4.3 Expression of Selected G. ultimum Kazal-Type Serine Protease Inhibitor Genes During Infection................................................................................................ 36 CHAPTER 5. DISCUSSION .................................................................................................. 40 REFERENCES ......................................................................................................................... 44 APPENDIX A. LIST OF KAZAL DOMAINS OF OOMYCETES ANNOTATED IN FUNGIDB ................................................................................................................................ 62 ix LIST OF FIGURES Figure Page 1 Phylogenetic Tree of Eukaryotes .................................................................................. 5 2 Secretion and Translocation of Effectors ..................................................................... 10 3 Life Cycle of Globisporangium ultimum ..................................................................... 13 4 Structure of KPI Domain .............................................................................................. 15 5 Agarose Gel Electrophoresis of Internal Transcribed Spacer (ITS) ............................. 27 6 Seedling Root Rot Assay on William Soybean Cultivar .............................................. 30 7 Seedling Root Rot Assay on William 82 Soybean Cultivar ......................................... 31 8 Multiple Sequence Alignment of G. ultimum KPI Domains ........................................ 34 9 The Consensus Sequence of G. ultimum Kazal Domains Using Weblogo .................. 35 10 P1 Residues Distribution .............................................................................................. 36 11 Expression of KPI Genes on Infected William
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