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The Pennsylvania State University The Pennsylvania State University The Graduate School PLANTS AS ILLEGITIMATE RECEIVERS OF INSECT SIGNALS: INSIGHT FROM MAIZE AND TEOSINTE A Thesis in Entomology by Julianne Golinski © 2020 Julianne Golinski Submitted in Partial Fulfillment of the Requirements for the Degree of Master of Science August 2020 ii The thesis of Julianne Golinski was reviewed and approved by the following: John F. Tooker Professor of Entomology and Extension Specialist Thesis Advisor Jared G. Ali Assistant Professor of Entomology Ben McGraw Associate Professor of Turfgrass Science Gary W. Felton Professor of Entomology Head of Department of Entomology iii ABSTRACT Plants have evolved to be sensitive to a range of insect-associated cues to detect the presence of herbivorous species and mount effective defense responses against future attack. Insect pheromones have recently been added to this library of cues as some plant species can act as “illegitimate receivers” that eavesdrop on the pheromones of insect herbivores, which act as reliable indicators of future larval damage. My thesis begins with a review that explores the perceptive capabilities of plants and how the ability to eavesdrop on insect pheromone cues may have evolved. I also cover the three known examples of plant illegitimate receivers and use shared traits in these systems to build criteria for finding other host plant species that may also utilize this strategy; native host plants species with (1) native, co-evolved insect herbivore species (2) that release abundant amounts of chemicals on or near the host plant, and (3) substantially reduce host plant fitness. My second chapter highlights two agriculturally relevant plant species that fit the criteria, maize (Zea mays ssp. mays; variety B73) and Balsas teosinte (Zea mays ssp. parviglumis). I investigated whether maize and its progenitor, teosinte, can detect the pheromone cues of a native co-evolved herbivore and important pest species, fall armyworm (FAW), and prime their defenses against future attack. To determine if maize or teosinte cue into FAW pheromone emissions, I exposed plants to FAW pheromones or the pheromones of sunflower head moth (SHM), an unassociated lepidopteran that acted as a chemical control. Following pheromone exposure, I allowed FAW caterpillars to feed on the plants. I found that feeding damage was reduced on maize plants that were exposed to FAW and SHM pheromone emissions and teosinte plants that were exposed to only FAW pheromone emissions. The levels of jasmonic acid in the leaves indicated that defenses were induced after feeding by FAW, but they were highly variable and did not predictably align with the expectation that FAW pheromone-exposed plants would have iv stronger, primed defense responses compared to controls. These results suggest that B73 line maize appears to respond to a broad spectrum of volatile chemicals and Balsas teosinte may have more targeted responses to FAW pheromones. v TABLE OF CONTENTS LIST OF FIGURES ................................................................................................................. vi LIST OF TABLES ................................................................................................................... viii ACKNOWLEDGEMENTS ..................................................................................................... ix Chapter 1 Plants as illegitimate receivers: how did it evolve and how common is it? ........... 1 Perceptive Abilities of Plants ........................................................................................... 2 Plant Detection of Volatiles ............................................................................................. 5 Plant Detection of Airborne Insect Cues .......................................................................... 7 Pheromones Derived from Plants ..................................................................................... 9 Criteria for Finding Other Examples of Plant Illegitimate Receivers .............................. 10 Known Examples of Plants as Illegitimate Receivers of Insect Pheromones .................. 12 Benefits of Understanding this Phenomenon ................................................................... 13 Conclusion ....................................................................................................................... 13 References ................................................................................................................................ 15 Chapter 2 The effects of fall armyworm sex pheromones on defenses in maize and its wild ancestor teosinte ....................................................................................................... 23 Introduction ...................................................................................................................... 23 Materials and Methods ..................................................................................................... 29 Plants and Insects ........................................................................................................ 29 Pheromone Lures ........................................................................................................ 30 Pheromone Lure Emissions ........................................................................................ 31 Experimental Setup ..................................................................................................... 31 Pheromone Exposure .................................................................................................. 32 Herbivore Feeding Assays .......................................................................................... 33 Measuring Leaf Damage Area .................................................................................... 34 Phytohormone Extractions .......................................................................................... 34 Quantification of Jasmonic Acid ................................................................................ 35 Statistical Analyses ..................................................................................................... 36 Results .............................................................................................................................. 37 Pheromone Lure Emissions ........................................................................................ 37 Fall Armyworm Feeding Damage and Weight Gain .................................................. 39 Phytohormone Analyses ............................................................................................. 42 Discussion ........................................................................................................................ 47 Conclusion ....................................................................................................................... 54 References ................................................................................................................................ 56 vi LIST OF FIGURES Figure 1-1: Criteria for finding host plants with the capacity to eavesdrop on insect- produced volatile compounds: (1) native, co-evolved insect herbivore species (2) that release abundant amounts of chemicals on or near the host plant, and (3) substantially reduce host plant fitness .. ........................................................................... 11 Figure 2-1: Images of leaf damage after 48 h of feeding by second instar fall armyworm larvae (A) before and (B) after editing. Damage area was colored in to properly process leaf damage area in ImageJ ................................................................................. 34 Figure 2-2: Linear regression of mass gain of fall armyworm larvae that fed on maize and teosinte in relation to damage area (Mass Gain = 2.016 + 2.329*damage area, R2 = 0.58) ................................................................................................................................. 37 Figure 2-3: Weight gain of fall armyworm larvae that fed on maize plants exposed to low or high doses of fall armyworm pheromones, sunflower head moth pheromones, or no pheromones (Tukey’s HSD P < 0.05). The bars shown are standard error bars and groups with different letters are statistically different ............................................... 40 Figure 2-4: Leaf damage area caused by fall armyworm larvae that fed for 48 h on maize plants exposed to low or high doses of fall armyworm pheromones, sunflower head moth pheromones, or no pheromones (Tukey’s HSD P < 0.05). The bars shown are standard error bars and groups with different letters are statistically different. The data shown are not transformed, but statistical analyses were carried out on square root-transformed data ....................................................................................................... 40 Figure 2-5: Weight gain of fall armyworm larvae that fed on teosinte plants exposed to low or high doses of fall armyworm pheromones, sunflower head moth pheromones, or no pheromones (Tukey’s HSD P < 0.05). The bars shown are standard error bars and groups with different letters are statistically different ............................................... 41 Figure 2-6: Leaf damage area caused by fall armyworm larvae that fed for 48 h on teosinte plants exposed to low or high doses of fall armyworm pheromones, sunflower head moth pheromones, or no pheromones (Tukey’s HSD P < 0.05). The bars shown
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