Getting to the root of nematode chemotaxis: Manipulation of belowground plant-nematode interactions
Restricted (Penn State Only)
- Author:
- Zainuddin, Nursyafiqi
- Graduate Program:
- Entomology
- Degree:
- Doctor of Philosophy
- Document Type:
- Dissertation
- Date of Defense:
- December 09, 2021
- Committee Members:
- Jared Ali, Chair & Dissertation Advisor
Mary Barbercheck, Major Field Member
Wendy Hanna-Rose, Outside Unit & Field Member
Gary Felton, Program Head/Chair
Edwin Rajotte, Major Field Member
Jared Ali, Chair & Dissertation Advisor - Keywords:
- nematode
kinesis
taxis
volatile
exudate
chemotaxis
non-volatile
olfactometer
behavior
ecological niche
environmental context
phytochemical
plant-nematode
evolution
parasitism
plant defense
carbon dioxide - Abstract:
- Nematodes represent a diverse class of organisms contributing to a myriad of ecosystem services and disservices through their roles as nutrient cyclers, biological control agents and plant or animal parasites. Therefore, a deeper understanding of how nematodes interact with cues related to the other organisms they interact with will bring us closer to developing novel and sustainable approaches for their management and utilization. Another crucial element to investigate is a comparative understanding of how nematode species from various ecological niches respond to cues. In particular, the identification of significant relationships between plant root exudates and nematode orientation behavior has application in nematode biology, ecology, and agricultural pest management. My overarching goal is to evaluate how nematodes from three different ecological niches respond to various plant cues and test whether there are any points of convergence for nematode orientation behavior. In chapter 1, I review the foundational research on nematode plant-nematode orientation behavior dating back to the early 1920s. In doing so, I highlight reasons why plant-nematode orientation behavior studies have faced several challenges for over a century. In this review, I focus on agriculturally important taxa and detail how the more than 100 years of work have made few advances in utilizing phytochemical-based strategies to manipulate nematodes in applied systems. Such alternatives will be vital, in part due to continued restrictions of pesticides and the innovation of new biological control tactics. With bans on many nematicides and a need to improve the culture and application of entomopathogenic nematodes on a large scale as a biological control agent for insect pests, there is a need to better understand nematode chemical ecology and how plant-nematode orientation behavior can be understood and utilized. However, inconsistent nematode responses were observed for more than 100 years of work between nematode orientation behavior and plant root exudate components such as non-volatile exudates, carbon dioxide and volatile organic compounds, affect host selection and behavior of nematodes. To determine how nematodes from three different ecological niches behave in terms of either attractiveness or repellency of plant root exudates, I conducted multiple-choice plants assays described in Chapter 2 to address my hypothesis that all three nematode species used in this study will be attracted to the crops that produce the highest abundance of attractive root volatiles and release high concentrations of carbon dioxide. I compared nematode responses to various plant species and characterized root volatiles emitted from these plants. Moreover, I determined if nematode attraction was influenced by root volatile organic compounds (VOCs) based on quantitative or qualitative traits. I conducted belowground behavioral assays on nematodes from three ecological niches and compared attractiveness among various plant species. This design tested whether nematodes from three ecological niches preferred similar plants, thus examining the potential for a basal trait in chemical preference. In addition, carbon dioxide released from individual plant species was measured using an infrared gas analysis system to determine the rate of plant root respiration. However, this study suggests that plant roots with a high abundance of attractive volatile organic compounds and respiratory carbon dioxide were not necessarily promising cues for below-ground nematode orientation behavior. Therefore, more mechanistic studies to understand nematode orientation behavior and its relationships with different plant species is necessary for each specific system of interests. To assess the impact of chemotactic response in a semi-natural setting I assessed plant root VOCs emitted from the roots of four major crop species (Daucus carota var. Danvers, Solanum lycopersicum var. Better Boy, Solanum tuberosum var. Yukon Gold, Zea mays var. B73) compared to a plant species thought to be repellent (Tagetes erecta var. Cracker Jack) and a non-crop species (Dara Daucus carota, a close relative of domestic carrot) growing in three different locations (Chapter 3). This experiment addressed the importance of soil environment on plant root VOC profiles and nematode orientation behavior. I hypothesized that there is a significant overlap across plant species that influence nematode responses and the total abundance of root volatile emission among locations would differ significantly. To test this hypothesis, I assessed whether plants release the same VOCs across various soil types and geographic locations. Several factors were documented to affect indigenous populations of nematodes in the soil, such as host availability, aeration, temperature, pH, water availability, soil microorganisms, soil health, soil texture, soil quality and soil chemical composition including plant root volatiles. Our results suggest that each of the plant species that we tested have a different strategy in releasing root volatiles, which might affect the belowground nematode population even in the absence of the root herbivory. In chapter 4, I sought to disentangle the role of non-volatile plant root exudates and root volatile organic compound extracts as potential attractants or repellants for nematodes. It is extremely vital to identify which isolated root VOCs are the most attractive or repellent to these nematodes differing in ecological niche. All nematode species are economically significant in assessing agriculture soil quality. Plus, due to the increasing concern for finding sustainable approaches for pest suppression, identifying novel tactics is a goal of many agricultural research programs. I hypothesized that non-volatile and volatile organic compounds extracted from roots were equally attractive, repellent or neutral to nematode orientation behavior. With this research, the goal was to better understand how non-volatile and volatile organic compounds emitted from plant roots with either attractant or repellent properties could be used in concert to create a phytochemical based strategy to manipulate nematode host-seeking behavior in agricultural fields. However, this study found that root non-volatile and volatile organic compounds from the same plant could attract, repel or be neutral for nematode orientation behavior. Therefore, understanding what characteristics of non-volatile and volatiles make certain plant species more apparent to nematodes and some other plants less so are vital for future research on these organisms. Based on data collected in this study, in chapter 5, I performed an additional analysis to explain why the study of plant-nematode orientation behavior still has many challenges even after a century of research. Surprisingly, inconsistent findings were found throughout my research between nematode orientation behavior and plant root exudate components such as non-volatile exudates, carbon dioxide and volatile organic compounds. Nematode responses were decreased if non-volatile or volatile compounds from root extracts were applied in the assay without the entire plant's presence. Furthermore, the magnitude of nematode response was positively correlated with the total number of trapped nematodes which suggested that communication might also influence nematode orientation behavior in the assay. Overall, this study indicated that root non-volatiles or volatiles alone could have a different effect without the presence of cues from the entire plant.