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Effects of Anaerobic Soil Disinfestation Combined With EFFECTS OF ANAEROBIC SOIL DISINFESTATION COMBINED WITH BIOLOGICAL CONTROL ON ROOT-KNOT NEMATODE AND LETTUCE DROP THESIS Presented in Partial Fulfillment of the Requirements for the Degree Master of Science in the Graduate School of The Ohio State University By Andres D. Sanabria-Velazquez Plant Pathology Graduate Program The Ohio State University 2018 Dissertation Committee: Sally A. Miller, Advisor Christopher G. Taylor Pierce A. Paul Copyright by Andres D. Sanabria-Velazquez 2018 Abstract Lettuce is one of the most important leafy vegetables produced on muck soils in Ohio. The fungi Sclerotinia minor and Sclerotinia sclerotiorum cause lettuce drop, a disease that results in the complete wilting and death of the plants. These pathogens produce large overwintering structures called sclerotia that are resistant to environmental extremes such as cold and heat, and can persist in the soil for several years. Another soilborne pathogen that limits lettuce production is the root-knot nematode (Meloidogyne hapla). Vegetable growers require sustainable approaches to manage these soilborne pathogens. Moreover, anaerobic soil disinfestation (ASD) appears to be a very promising management technique for smallholder farmers in developing countries like Paraguay. We evaluated the effectiveness of biocontrol bacteria and anaerobic soil disinfestation (ASD) as management tools for these pathogens. This is the first study of the effect of these tactics on the survival of Sclerotinia’s resistant overwintering structures in Ohio and Paraguay. The potential of biocontrol bacteria to suppress the viability of the survival structures (sclerotia) of Sclerotinia sclerotiorum and Sclerotinia minor was evaluated during laboratory experiments. The antagonism of forty-five bacterial strains (one Streptomyces sp., two Bacillus spp., and forty-two Pseudomonas spp.) was tested using the dual culture and sclerotia germination inhibition methods. We also evaluated a new soil disinfestation technique called anaerobic soil disinfestation (ASD) and its efficacy in suppressing Sclerotinia and root-knot nematode in Ohio and Paraguay. This technique consisted of incorporating an organic amendment into the soil followed by saturation with water and covering with plastic mulch for four weeks. During this procedure, levels ii of oxygen decrease and complex microbial processes, including production of organic acids, reduce the viability of the pathogens. During growth chamber trials, muck soils containing sclerotia placed in mesh bags and root-knot nematode eggs were treated with ASD using one of four organic amendments (molasses, wheat bran, or mustard greens at 20.2 Mg/ha, or 2% ethanol). Organic acids produced during the disinfestation process were characterized. After four weeks, sclerotia were removed and tested for viability, and lettuce plants were grown in treated and control soils for five weeks to determine root- knot severity. Field trials were conducted in Ohio muck soils and Paraguay red (oxisols) soil as well. Plots were amended with wheat bran (20.2 Mg (metric tonne)/ha), molasses (10.1 Mg/ha), wheat bran (20.2 Mg/ha) plus molasses (10.1 Mg/ha) or maintained unamended (control). Sclerotia in mesh bags were buried in the plots, which were then saturated and covered. After four weeks, sclerotia of both fungal pathogens were recovered and their viability evaluated. Biocontrol bacteria including Pseudomonas and Bacillus strains reduced the viability of the survival structures (sclerotia) of the fungal pathogens >70% during in vitro trials. ASD reduced the viability of the sclerotia >80% obtaining similar results from field trials in Ohio muck soils and Paraguay red soils. Complete suppression of root-knot nematode was observed in soils treated with ASD, regardless of carbon source during growth chamber trials. Organic acids produced during ASD were deleterious to sclerotia viability. Concentrations of these organic acids varied depending on the carbon source employed for ASD. The carbon sources for ASD that allowed highest production of organic acids were molasses followed by wheat bran and ethanol, being mustard greens the least effective in regards of organic acids production. When P. chlororaphis iii 14B11R was applied and anaerobic soil disinfestation (ASD) was conducted in those soils, no bacterial growth was observed. On the contrary, populations of B. subtilis QST 713R did not differ from populations of B. subtilis QST 713R in the positive, non-ASD control, whether applied to the soil before or after ASD treatment. The combination of biocontrol agent (BCA) application with ASD soil treatment did not lead to a significantly higher reduction of sclerotia viability compared to ASD alone for both S. minor and S. sclerotiorum. Future work will focus on determining if the biocontrol bacteria will be similarly effective when inoculated into the soil and/or on the roots of the plants. These bacteria can reduce the number of sclerotia by producing fungal inhibiting compounds and growing in association with the plant roots. Anaerobic soil disinfestation is currently being adopted by farmers in Ohio and in Paraguay. Future research will focus on optimizing ASD for soilborne pathogen management in different soils and with additional readily available organic amendments. iv Dedication Dedicated to My Family v Acknowledgments I thank Almighty God for all the blessings He has given me, for all I have learned, for all the people I have known during this journey. I want to express my sincere thanks to my advisor, Dr. Sally A. Miller for her patience and guidance throughout my research. Thanks for encouraging me to be a better plant pathologist and researcher. I would like to thank the members of my student advisory committee, Dr. Christopher G. Taylor, and Dr. Pierce A. Paul for their helpful comments and support. I thank all the staff, professors and fellow students of the Department of Plant pathology. Thanks for the opportunity of being part of this amazing group of people. I thank all members of the Vegetable Lab. Thanks specially for the friendship (and patience!). Thanks to Angela Nanes, Cláudio Vrisman, Hellen Kanyagha, Ram Khadka, Francesca Rotondo, Nitika Khatri. My special thanks to Anna Testen, who I consider one of my best Plant pathology friends. Thanks so much for your friendship. I want to thank my dear Wooster friends who always supported me and shared unforgettable moments with me. Thanks to Luis Huezo, Kaylee South, Juan Quijia, Jhony Mera, Andika and Mao Gunadi, and Lucia Pisoni. I also want to express my thanks to my parents Antonia and Patricio, my sister Paola and my brother David, for their unconditional help. I want to thank my dear Yoli, for her support and patience during all this time. I thank the Fulbright Foreign Student Program for giving me financial support to pursue my Master’s degree in the United States of America. vi Vita 2014.................................................. BS Agronomy, National University of Asuncion- Paraguay 2014-2016.......................................... Research assistant, Paraguayan Institute of - Agricultural Technologies-Paraguay 2016 to present...................................Graduate Student, Department of Plan Pathology- The Ohio State University-USA 2016 to present................................... Fulbright International Fellow-USA Publications Sanabria, A.D. and Grabowski Ocampos, C.J., 2016. Biological control of Rosellinia sp. causing of the sudden death of the macadamia (Macadamia integrifolia) with isolates of Trichoderma spp. Investigación Agraria, 18(2), pp.77-86. Sanabria, A. D., Taylor, C. G., Miller, S. A. 2017. Antagonistic potential of biocontrol bacteria against Sclerotinia sclerotiorum causing lettuce drop. (Abstr.) Phytopathology 107:S5.1. https://doi.org/10.1094/PHYTO-107-12-S5.1 Villalba Silvero, F. A., Sanabria, A. D., Flores-Giubi , M. E., and Barua. J. E. 2017. Differential antibiosis of hydrolytic enzymes and metabolites by Paraguayan isolates of Trichoderma spp. against Macrophomina phaseolina. (Abstr.) Phytopathology 107:S5.1. https://doi.org/10.1094/PHYTO-107-12-S5.1 vii Miller, S.A., Vrisman, C.M., Sanabria, A., Mera, J.R., Hofelich, M., Bergefurd, B., Jasinski, J. and Harker, T. 2017. Bioassay for sensitivity of Podosphaera xanthii to fungicides in OH, 2017. Vegetable Disease Management Research Reports. Plant Pathology Series N°. 154. Miller, S.A., Vrisman, C.M., Sanabria, A., Mera, J.R., Hofelich, M., Bergefurd, B., Jasinski, J. and Harker, T. 2017. Bioassay of pumpkin cultivar resistance to powdery mildew in OH, 2017. Vegetable Disease Management Research Reports. Plant Pathology Series N°. 154. Major Field: Plant Pathology viii Table of Contents Abstract ….………….………….………….…….……………………………….. ii Dedication ...…………………..……….………….………….…........................... v Acknowledgements….….…….………….………….…………….....…...………. vi Vita………………………………………….………..….……..…….…………… vii Table of contents………….………….………….……………….......................... ix List of Tables..….….…….………….………….……………………………….... xii List of Figures………….………….………….…………………….…………...... xiv Chapter 1: Literature review ………………………………………....................... 1 References ….………………………............................................................. 29 Chapter 2: Effects of anaerobic soil disinfestation on Sclerotinia minor and S. sclerotiorum sclerotia viability and Meloidogyne hapla survival in muck soils……………………………………………………………………………...... 49 Abstract ….………………………................................................................
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