Factors Influencing Susceptibility to Viral Diseases in Plants and Pollinators and the Effects of Plant Virus Infection on Bee Attraction and Nutritional Resources
Open Access
- Author:
- Hinshaw, Chauncy
- Graduate Program:
- Plant Pathology
- Degree:
- Doctor of Philosophy
- Document Type:
- Dissertation
- Date of Defense:
- May 31, 2023
- Committee Members:
- Matthew Ferrari, Outside Unit & Field Member
Cristina Rosa, Co-Chair & Dissertation Advisor
Margarita Lopez-Uribe, Co-Chair & Dissertation Advisor
Beth Gugino, Major Field Member
Kevin Hockett, Major Field Member
Maria Del Mar Jimenez Gasco, Program Head/Chair - Keywords:
- Virology
Honey Bees
Plant Viruses
Domestication
Plant-Pollinator Interactions - Abstract:
- All types of organisms are susceptible to virus infections. However, many organisms have developed responses to virus infections that allow them to coexist with their parasites. Ultimately, host susceptibility is a result of underlying genetic factors controlling immune responses which lead to different infection outcomes even between closely related hosts. Through genetic bottlenecks and tradeoffs between immunity and traits desirable to humans, artificial selection can have consequences for disease susceptibility. A major goal of this research was to determine how domestication processes can alter host immunity by introducing selection pressures that change host responses and infection outcomes. To address these questions, this research focused on two systems that have long, complex histories of domestication and globalization: the honey bee (Apis mellifera) and squash plants in the genus Cucurbita. This research leveraged multi-year field experiments to characterize host fitness in natural settings and used molecular techniques to quantify immune responses. The results of this work show virus tolerance—defined as reductions in disease while allowing for pathogen replication,—is common in plant and pollinator systems. Additionally, to provide deeper insight into host responses to virus infection in squash plants, RNA sequencing was performed to identify specific transcriptional responses involved with differences in host immunity. Because domestication of honey bees may result in strong selection pressures that are different than the selection pressures faced by unmanaged bees in the wild (feral), we hypothesized that feral bees would have higher disease burdens but also higher levels of immune gene expression. Honey bees from 25 pairs of unmanaged (feral) and managed colonies were collected over two years and assessed for pathogen levels, host immune gene expression, and colony survival. We found that feral bees exhibited higher levels of one of the three pathogens tested and this was associated with increased immune gene expression. We also showed that feral colonies had similar levels of overwintering survival even with higher pathogen burdens, suggesting increased virus tolerance compared to managed honey bees. This work also identified immune genes that were associated with increased overwintering survival in both feral and managed honey bee colonies, providing insight into host-parasite ecology. As host defenses evolve over time, closely related hosts may share defenses contributing to similar levels of disease susceptibility. Thus, in addition to domestication status, host phylogenetic relatedness may also be an important predictor of host susceptibility to viral disease. The second research aim of this dissertation was to determine if either domestication status or host phylogenetic relatedness contribute to differences in susceptibility between squash plant hosts. We used three pairs of domesticated and wild plants in the genus Cucurbita to characterize host phenotypes throughout an entire field season. Plants were inoculated with a combination of zucchini yellow mosaic virus (ZYMV) and squash mosaic virus (SqMV). This study was conducted over three years resulting in a robust dataset with over 15 recorded variables related to plant health. Results indicate that domestication is not a driver of susceptibility in this system, but host phylogenetic relatedness is predictive of infection outcomes for many of the traits measured. Also, it was found that virus infection alters the behavior of a specialist pollinator but not a generalist pollinator in this system. Surprisingly, virus infection also decreased pollen production and nectar sugar concentration which has implications for pollinator nutrition. Furthermore, we found that although infection outcomes differed greatly between hosts, viral load did not, providing support for the importance of tolerance in this system. This study also provides evidence that tolerant plant hosts can maintain nearly all measures of fitness in the field, demonstrating that tolerance deserves further consideration as a disease management strategy in agriculture. After thorough characterization of susceptibility of different plant hosts in the field, species with low, medium, and high levels of disease susceptibility were chosen to investigate molecular mechanisms underlying reduced disease susceptibility. We exposed plants to mixed infection of ZYMV and SqMV, a mock-inoculation, or no treatment at three different time points under controlled conditions in a grow room. Tissue from these 81 plants was then sent for RNA sequencing. Results showed that less susceptible hosts had reduced responses in the total number of differentially expressed genes and in the number of defense-related genes. Responses in the least susceptible host also subsided more quickly compared to more susceptible hosts and were effective at reducing the accumulation of ZYMV, while SqMV levels were similar between all hosts. This research suggests that reduced disease susceptibility is characterized by delayed or lower magnitude of responses, which may deprive viruses of necessary factors for replication, and ultimately may limit virus-induced damage. Our results also highlight the importance of early host responses before symptom development for infection outcomes. This dataset provides a valuable resource for further investigating the molecular mechanisms of virus susceptibility in plants, which are largely unknown.