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PLANT-NEMATODE INTERACTIONS AND THE APPLICATION OF RNA INTERFERENCE FOR CONTROLLING ROOT-KNOT NEMATODES By PHUONG THI YEN DINH A dissertation submitted in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY WASHINGTON STATE UNIVERSITY Department of Plant Pathology MAY 2015 © Copyright by PHUONG THI YEN DINH, 2015 All Rights Reserved © Copyright by PHUONG THI YEN DINH, 2015 All Rights Reserved To the Faculty of Washington State University: The members of the Committee appointed to examine the dissertation of PHUONG THI YEN DINH find it satisfactory and recommend that it be accepted. ___________________________________ Debra A. Inglis, Ph.D., Chair ___________________________________ Charles R. Brown, Ph.D. ___________________________________ Lori M. Carris, Ph.D. ___________________________________ Axel A. Elling, Ph.D. ___________________________________ Kiwamu Tanaka, Ph.D. ii ACKNOWLEDGMENTS I thank my parents, Nghia Dinh and Yen Nguyen, for their support, care and encouragement during my education. I especially want to express my deepest gratitude to Dr. Axel Elling, my major advisor for his incredible advice and persistent support. My sincere gratitude also goes to Dr. Debra Inglis, my committee member and my major advisor in the last year of my PhD program, for her encouragement, concern and guidance. I also am thankful to other committee members, Drs. Charles Brown, Lori Carris, Kiwamu Tanaka and Brenda Schroeder, for their suggestions about my research and reviews of my manuscripts and dissertation. I extend my appreciation to Dr. Michael Knoblauch for his guidance and support in microscopy techniques. I also express my gratitude to Professor Elizabeth Siler for her assistance with and proofreading of my dissertation. I thank the faculty, staff, and students in the Department of Plant Pathology, Franceschi Microscopy and Imaging Center as well as Plant Growth Facilities for their help, assistance, and friendship during my studies at Washington State University. I offer a warm thank-you to all members and undergraduate students, past and present, of Dr. Elling’s lab. It has been a great pleasure to work with these lab members. Thanks to all of my friends for their comfort. I am thankful to my colleagues in Southern Horticultural Research Institute, Vietnam for their encouragement during my studies. This project was funded by the Washington State Department of Agriculture, Washington State Potato Commission, Idaho Potato Commission, Northwest Potato Research Consortium, Washington Grain Commission, and United States Department of Agriculture, and I gratefully acknowledge the support. iii PLANT-NEMATODE INTERACTIONS AND THE APPLICATION OF RNA INTERFERENCE FOR CONTROLLING ROOT-KNOT NEMATODES Abstract by Phuong Thi Yen Dinh, Ph.D. Washington State University May 2015 Chair: Debra A. Inglis Plant parasitic nematodes are significant pests in major agricultural systems. Sedentary endoparasites like root knot nematodes (RKN; Meloidogyne sp.) obtain plant- derived nutrients from feeding sites formed in host roots thereby supporting nematode development. The formation of feeding sites is hypothesized to be mediated by nematode effectors, proteinaceous secretions from nematode esophageal gland cells. An inherent challenge in studying most plant-nematode interactions is the difficulty in directly observing nematodes within plant roots. Traditional microscopy techniques are unusable because developing nematodes are surrounded by layers of root cells. In this study, a novel, nondestructive technique was developed to observe the progression of nematode pathogenesis in planta. Pratylenchus penetrans, Heterodera schachtii and Meloidogyne chitwoodi were fluorescently labeled with the lipid specific stain PKH26 and inoculated onto Arabidopsis thaliana seedlings growing in microscopy rhizosphere chambers. The migration patterns and morphology of live nematodes then were observed using confocal microscopy during the parasitic life cycles. Host-nematode interactions were studied at the molecular level by characterizing the highly conserved RKN effector, 16D10. Overexpression of 16D10 in iv A. thaliana increased the transcript level of VND7, a xylem development marker, and metaxylem root cell numbers, thereby enhancing susceptibility of A. thaliana to M. incognita. Modifying xylem development by 16D10 possibly facilitates M. incognita feeding site formation. An ortholog of 16D10, Mc16D10L, was cloned from M. chitwoodi. Plant-mediated 16D10 RNA interference (RNAi) silenced Mc16D10L and significantly reduced M. chitwoodi race 1 reproduction by up to 71% in A. thaliana and potato (Solanum tuberosum cvs Russet Burbank and Désirée) plants. Introducing 16D10 RNAi into potato breeding line PA99N82-4 also decreased reproduction of M. chitwoodi pathotype Roza by 50%; this pathotype breaks RMc1(blb), a resistant gene of PA99N82-4. The RNAi effect of Mc16D10L was transmitted to M. chitwoodi offspring, and significantly reduced pathogenicity of nematode offspring on non-RNAi plants. The potato RNAi line, D21 further proved resistant to M. incognita, M. javanica, M. arenaria and M. hapla. Plant-mediated 16D10 RNAi offers a promising new tool for molecular breeding against RKN in potato. v TABLE OF CONTENTS Page ACKNOWLEDGEMENTS ................................................................................................ iii ABSTRACT ..................................................................................................................... iv LIST OF TABLES ............................................................................................................. x LIST OF FIGURES .......................................................................................................... xi CHAPTER 1: GENERAL INTRODUCTION ...................................................................... 1 1. 1. Plant parasitic nematodes ................................................................................... 1 1. 1. 1. Root-lesion nematodes .............................................................................. 2 1. 1. 2. Cyst nematodes ......................................................................................... 3 1. 1. 3. Root-knot nematodes ................................................................................ 6 1. 1. 4. Molecular plant-nematode interactions ...................................................... 8 1. 1. 5. Management ............................................................................................ 14 1. 2. Root-knot nematodes in potato ......................................................................... 23 1. 3. Research objectives and contributions ............................................................. 25 1. 4. Literature cited .................................................................................................. 30 CHAPTER 2: NONDESTRUCTIVE IMAGING OF PLANT-PARASITIC NEMATODE DEVELOPMENT AND HOST RESPONSE TO NEMATODE PATHOGENESIS ........... 62 2. 1. Abstract ............................................................................................................. 63 2. 2. Introduction ....................................................................................................... 64 2. 3. Materials and methods ...................................................................................... 66 2. 4. Results .............................................................................................................. 70 2. 5. Discussion ......................................................................................................... 74 vi 2. 6. Acknowledgments ............................................................................................. 79 2. 7. Literature cited .................................................................................................. 80 2. 8. Figures .............................................................................................................. 88 CHAPTER 3: MELOIDOGYNE INCOGNITA EFFECTOR 16D10 MODIFIES XYLEM DIFFERENTIATION IN ARABIDOPSIS THALIANA TO FACILITATE NEMATODE PARASITISM .................................................................................................................. 97 3. 1. Abstract ............................................................................................................. 98 3. 2. Introduction ....................................................................................................... 99 3. 3. Materials and methods .................................................................................... 102 3. 4. Results ............................................................................................................ 112 3. 5. Discussion ....................................................................................................... 117 3. 6. Acknowledgments ........................................................................................... 123 3. 7. Literature cited ................................................................................................ 124 3. 8. Figures ............................................................................................................ 134 3. 9. Supplement ..................................................................................................... 141 CHAPTER 4: RNA INTERFERENCE OF EFFECTOR GENE MC16D10L CONFERS RESISTANCE AGAINST MELOIDOGYNE CHITWOODI IN ARABIDOPSIS AND POTATO ......................................................................................................................
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