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Effects of Beneficial Microbes on Plant‐Virus‐Vector Interactions

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Effects of Beneficial Microbes on Plant‐Virus‐Vector Interactions The Pennsylvania State University The Graduate School Department of Biology EFFECTS OF BENEFICIAL MICROBES ON PLANT‐VIRUS‐VECTOR INTERACTIONS INVOLVING SOYBEAN A Dissertation in Biology by Hannier Pulido Barrios 2016 Hannier Pulido Barrios Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy December 2016 ii The dissertation of Hannier Pulido Barrios was reviewed and approved* by the following: Mark C. Mescher Adjunct Professor of Biology Dissertation Advisor Andrew G. Stephenson Distinguished Professor of Biology Associate Dean for Research Chair of Committee Consuelo M. de Moraes Adjunct Professor of Biology Naomi Altman Professor of Statistics Cristina Rosa Assistant Professor of Plant Pathology John Tooker Associate Professor of Entomology Tracy Langkilde Professor and Head of Biology *Signatures are on file in the Graduate School iii ABSTRACT Soil‐borne microorganisms can have significant effects on aboveground interactions between plants and other organisms. For example, association with some non‐pathogenic soil microbes stimulates plants and modify volatile emissions, defense capability, nutritional quality and host gene expression. Likewise, detrimental microorganisms like some plant viruses, can also change plant phenotype in ways that influence transmission. As a result, microbe‐plant associations may indirectly modify the interactions among plants, herbivorous insects and parasitoids. While the relevance of microorganisms on the ecology of plant mediated interactions has been widely studied, research that integrates ecological and molecular approaches involved in these multi‐trophic interactions are still limited. The general goal of this research is to understand how microbial associations influences plant‐pathogen and plant‐insect interactions in soybean. To achieve this goal, I use a combination of chemical analysis, gene transcriptomics and insect behavior linked with state‐of‐the‐art data mining techniques. We examined how two species of beneficial rhizobacteria—the plant growth promoter rhizobacteria (PGPR) species Delftia acidovorans, which lives in the rhizosphere in close association with root surfaces, and the nitrogen‐fixing Bradyrhizobium japonicum—influence the interactions of soybean plants (Glycine max cultivar Williams 82) with the herbivorous beetle Epilachna varivestis, which vectors an economically important pathogen of cultivated soybean, Bean pod mottle virus (BPMV) and with the parasitoid wasp Pediobius foveolatus. In a multi‐factorial experiment, we characterized the volatile organic compounds (VOC), the primary and secondary leaf metabolites and the transcriptome produced by soybean plants in the presence/absence of the two rhizobacteria and with or without infection by BPMV. Our results indicate that BPMV infection and inoculation with beneficial rhizobacteria cause dramatic changes in metabolites iv and genes related with plant nutrition and defense, with significant consequences for soybean interactions with an important herbivore and virus vector. v TABLE OF CONTENTS LIST OF FIGURES ....................................................................................................................... vii LIST OF TABLES ......................................................................................................................... ix ACKNOWLEDGEMENTS ............................................................................................................ x Introduction ............................................................................................................................. 1 Biology of Bean pod mottle virus (BPMV) and beetle vector ........................................... 2 Biology of soybean interactions with nitrogen‐fixing bacteria and PGPR ....................... 4 Overview of chapters ....................................................................................................... 5 References........................................................................................................................ 7 Parasitoid attraction to herbivore‐damaged soybean volatiles depends on the identity of rhizobacterial colonizers ................................................................................. 10 Abstract ............................................................................................................................ 10 Introduction ..................................................................................................................... 11 Materials and methods .................................................................................................... 16 RESULTS ............................................................................................................................ 23 Discussion ......................................................................................................................... 26 References........................................................................................................................ 33 Figures .............................................................................................................................. 39 Effect of beneficial rhizobacteria and a virus infection on soybean metabolomics with downstream consequences on beetle feeding preferences ............ 44 Abstract ............................................................................................................................ 44 Introduction ..................................................................................................................... 45 Materials and Methods .................................................................................................... 47 Results .............................................................................................................................. 55 Discussion ......................................................................................................................... 61 References........................................................................................................................ 67 Figures .............................................................................................................................. 71 Integration of transcriptomics and metabolomics reveals rhizobacteria and viral effects on soybean ................................................................................................... 79 Abstract ............................................................................................................................ 79 Introduction ..................................................................................................................... 80 Materials and Methods .................................................................................................... 83 Results .............................................................................................................................. 86 Discussion ......................................................................................................................... 90 References........................................................................................................................ 95 Figures .............................................................................................................................. 98 vi Conclusions .............................................................................................................................. 107 Appendix A. Components of the metabolite and behavioral bioassays .................................. 111 Appendix B. Bayesian anova results for the main factors and their interaction effects ......... 112 Appendix C. Random Forest and Bayesian Analysis main results ............................................ 113 Appendix D. Compounds emitted by damaged soybean plants under different rhizobacteria and virus treatments .................................................................................. 114 Appendix E. Dual choice feeding assay setup in a semi‐natural environment ........................ 115 Appendix F. Top 20 overrepresented KEGG pathways ............................................................ 116 vii LIST OF FIGURES Figure 1‐1. Total volatile emissions from damaged soybean plants under different rhizobacteria and virus treatments. ................................................................................. 39 Figure 1‐2. Heatmap depicting soybean volatile signatures associated with rhizobacteria and virus treatments. ....................................................................................................... 40 Figure 1‐3. Pasrasitoid preferences for odors of host‐damaged soybeans under different rhizobacteria and virus treatments. ................................................................................. 41 Figure 1‐4. Parasitism rates on larval hosts residing on soybeans with different rhizobacteria and virus treatments. ................................................................................. 42 Figure 1‐5. Key compounds discriminating blends from damaged soybeans under rhizobacteria and virus treatments. ................................................................................. 43 Figure 2‐1. Experimental design workflow. ............................................................................. 71 Figure 2‐2. Adult foraging behavior. .......................................................................................
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