STUDIES ON THE DEVELOPMENT AND MANAGEMENT OF POWDERY SCAB AND ROOT GALL FORMATION CAUSED BY SPONGOSPORA SUBTERRANEA ON POTATO (SOLANUM TUBEROSUM L.) A Dissertation Submitted to the Graduate Faculty of the North Dakota State University of Agriculture and Applied Science By Francisco Gabriel Bittara Molina In Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY Major Department: Plant Pathology November 2015 Fargo, North Dakota North Dakota State University Graduate School Title Studies on the development and management of powdery scab and root gall formation caused by Spongospora subterranea on potato (Solanum tuberosum L.) By Francisco Gabriel Bittara Molina The Supervisory Committee certifies that this disquisition complies with North Dakota State University’s regulations and meets the accepted standards for the degree of DOCTOR OF PHILOSOPHY SUPERVISORY COMMITTEE: Dr. Gary A. Secor Co-Chair Dr. Neil C. Gudmestad Co-Chair Dr. Asunta L. Thompson Dr. Luis E. del Rio Mendoza Approved: 11/02/2015 Dr. Jack B. Rasmussen Date Department Chair ABSTRACT The biotroph protozoan Spongospora subterranea causes root gall formation and powdery scab on potato. Symptoms on tubers affect directly the quality and marketability of the harvested product while infection in roots are associated with yield reductions. Moreover, S. subterranea is the vector of the Potato mop-top virus. The management of the disease is difficult due to the limited number of current control options and requires the integration of control measures among which host resistance represents the most economically and long-term approach. This dissertation focuses on the evaluation of management strategies for the control of powdery scab and root gall formation. In the first study, a total of 43 potato cultivars and 80 advanced clones representing a range of skin types were assessed for their response to powdery scab and root gall formation in five field experiments. High levels of resistance was observed among genotypes against the development of disease on tubers and roots which accounted for 32.5% of the evaluated population. Resistance to powdery scab and root gall formation was shown to follow a continuum from very susceptible to very resistant. In the second study, the effect of chloropicrin soil fumigation on the soil populations of S. subterranea and the concomitant development of disease in roots and tubers was investigated in seven field trials. Results indicated a reduction of pathogen soil inoculum, which in most cases was accompanied by an increase in yield and disease on tubers and roots. These results were confirmed in controlled condition experiments in which the amount of pathogen DNA detected in roots increased with the fumigant rate. In the third study, reciprocal grafts between ‘Shepody’ (susceptible to powdery scab and root gall formation) and ‘Dakota Trailblazer’ (resistant) were prepared in order to assess the effect of grafting on the translocation of susceptibility factors affecting the infection and development of root galls. The amount of pathogen DNA increased, iii as did the number of root galls, on graft combinations involving ‘Shepody’. The results presented in this dissertation highlight the importance of cultivar selection in the management of root gall formation and powdery scab on tubers. iv ACKNOWLEDGMENTS I would like to express my sincere gratitude to my advisers Dr. Gary Secor and Dr. Neil Gudmestad for their guidance, support and constructive criticism along the course of this research. I also appreciate their patience toward me and the opportunity offered to become a grad-student of the NDSU Plant Pathology Department. I want also to thank Dr. Asunta (Susie) Thompson and Dr. Julio Kalazich for their contribution in supplying the potato genotypes evaluated in this research and Dr. Luis del Río Mendoza for his support and advice in the statistical analysis of the experiments. I want to thank the funding sources made this project possible: The Northern Plans Potato Growers Association, US Potato Board and Minnesota Area II Potato Growers. I also want to show my gratitude to all the faculty members and grad-student in the department whom made easier my days in Fargo. Thanks to Viviana Rivera for her assistance and support, and also the interesting discussion of ideas developed in this dissertation. I am very thankful to Ipsita Mallik who helped and trained me in the molecular component of this research. I also want to include Dr. Julie Pasche for her support. I am very thankful to Dean Peterson and Russel Benz, as well as, all seasonal workers at potato storage for their contribution in all field experiments. I want to thank my wife, Lauren Sager-Bittara for her support and love in every single second since the moment we met. My appreciation to Dr. Dorian Rodriguez for his support and friendship in the good and bad moments whether in the US or Venezuela. I also want to include Prof. Maria Elena Sanabria, Dr. Alexander Hernandez and Mr. Michael Miller for their support throughout these years of research. To all of you and those I might forget, thanks a bunch! v DEDICATION To my family vi TABLE OF CONTENTS ABSTRACT ................................................................................................................................... iii ACKNOWLEDGMENTS .............................................................................................................. v DEDICATION ............................................................................................................................... vi LIST OF TABLES ......................................................................................................................... ix LIST OF FIGURES ........................................................................................................................ x LIST OF APPENDIX TABLES ................................................................................................... xii CHAPTER I. LITERATURE REVIEW ......................................................................................... 1 The Potato ............................................................................................................................1 The Disease ..........................................................................................................................4 Causal Organism ..................................................................................................................9 Environmental Conditions Conducive for Disease Development .....................................16 Management Approaches...................................................................................................22 Literature Cited ..................................................................................................................27 CHAPTER II. FIELD EVALUATION OF POTATO GENOTYPES FOR RESISTANCE TO POWDERY SCAB ON TUBERS AND ROOT GALL FORMATION CAUSED BY SPONGOSPORA SUBTERRANEA ............................................................................................... 38 Abstract ..............................................................................................................................38 Introduction ........................................................................................................................39 Materials and Methods .......................................................................................................42 Results ................................................................................................................................47 Discussion ..........................................................................................................................60 Literature Cited ..................................................................................................................63 vii CHAPTER III. INFLUENCE OF SPONGOSPORA SUBTERRANEA INOCULUM LEVELS ON THE DEVELOPMENT OF POWDERY SCAB AND ROOT GALL FORMATION AND THE POTENTIAL FOR REDUCTION OF SOIL INOCULUM USING CHLOROPICRIN ............................................................................................................ 69 Abstract ..............................................................................................................................69 Introduction ........................................................................................................................70 Materials and Methods .......................................................................................................73 Results ................................................................................................................................81 Discussion ..........................................................................................................................98 Literature Cited ................................................................................................................102 CHAPTER IV. EVALUATION OF THE EFFECT OF RECIPROCAL GRAFTING BETWEEN TWO POTATO CULTIVARS ON THE INFECTION AND DEVELOPMENT OF ROOT GALLS CAUSED BY SPONGOSPORA SUBTERRANEA ....... 109 Abstract ............................................................................................................................109 Introduction ......................................................................................................................110 Materials and Methods .....................................................................................................113