Source: UNIVERSITY OF FLORIDA submitted to
INVASIVE SPECIES AS CONDUITS FOR PATHOGEN SPILLOVER BETWEEN NATURAL AND AGRICULTURAL SYSTEMS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
ACTIVE
Funding Source
Reporting Frequency
Annual
Accession No.
1031035
Grant No.
2023-67015-40544
Cumulative Award Amt.
$2,500,000.00
Proposal No.
2023-04655
Multistate No.
(N/A)
Project Start Date
Sep 1, 2023
Project End Date
Aug 31, 2027
Grant Year
2023
Program Code
[A1222]- Ecology and Evolution of Infectious Diseases
Project Director
Goss, E.
Recipient Organization
UNIVERSITY OF FLORIDA
G022 MCCARTY HALL
GAINESVILLE,FL 32611
Performing Department
(N/A)
Non Technical Summary
Movement of pathogens between ecosystems is a major driver of pathogen emergence in humans, animals, agricultural crops, and natural ecosystems. Invasive plants span natural, disturbed, and agricultural systems, provide a novel, abundant hostfor novel groups of microbes, and can have an outsized role in pathogen transmission because invasive plants occur in high density and create conducive environments for disease. This research will examine the role of invasive plants in the eco-evolutionary dynamics of transmission across ecosystems boundaries and crop disease emergence, and capture initial epidemic dynamics of an emerging pathogen on a novel host in real time. The sharp contrasts between agricultural and wild hosts in spatial and community structure, phenology, individual heterogeneity, and microbiomes provide an ideal model system for empirical and theoretical investigation of the interplay of these factors on ecological and evolutionary dynamics of infectious diseases at and across ecosystem boundaries. Our results will advance understanding of ecological and evolutionary drivers of pathogen spillover and adaptation to a novel host, inform more general theory in infectious disease ecology, and ultimately improve prediction and management of emerging diseases.
Animal Health Component
10%
Research Effort Categories
Basic
90%
Applied
10%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2121730110260%
2122300107040%
Goals / Objectives
The overarching goal of this project is to elucidate the process of disease emergence via spillover between plant species and ecosystems. We will investigate the unique role of invasive plants, with their large populations at ecosystem boundaries, as a conduit for spillover of microbes between hosts in natural areas and agroecosystems. Specifically, we will examine the rapid emergence of Bipolaris gigantea, a fungal pathogen of grasses, on industrial hemp (Cannabis sativa containing less than 0.3% THC) that we hypothesize was transmitted from leaf spot epidemics on the invasive grass Microstegium vimineum in natural ecosystems in the same region. Our objectives are to: (1) Quantify ecological drivers of pathogen transmission between species and ecosystems; (2) Determine role of pathogen evolution in disease emergence on a novel host; and (3) Develop eco-evolutionary infectious disease models for coupled natural-agricultural systems. We will address these objectives with field surveys, field and greenhouse experiments, pathogen population genomics, reciprocal host infection and co-infection experiments, and mathematical and computational modeling informed by results of the empirical work.
Project Methods
The proposed research will measure real time pathogen transmission and evolution in coupled natural and agroecosystems and develop novel models of disease dynamics.Objective 1. Quantify ecological drivers of pathogen transmission between ecosystems.To assess the role of invasive plants, and their litter, in pathogen transmission from natural areas to agricultural crops, we will use field surveys and field and greenhouse experiments. We will examine major factors likely to mediate disease on hemp, including distance from diseased invasive plants and their litter, hemp genotype and microbiome, nutrient availability, and abiotic conditions. Specifically, we will carry out extensive field surveys (Year 1), then introduce experimental hemp plants (Years 2, 3) to sites identified during the pathogen survey, manipulate invader litter, nutrients, microbiomes, and hemp genetics, and conduct greenhouse experiments on abiotic factors hypothesized to regulate disease.Objective 2. Determine role of pathogen evolution in disease emergence on a novel host.Hemp has been a host of B. gigantea populations for only a few years, providing a unique opportunity to study the evolution of a fungal pathogen on a novel host. Natural selection and/or reduced gene flow between hosts or ecosystems may result in host or ecosystem-specialized populations. We will examine the role of pathogen evolution on disease emergence, and the roles that movement between hosts and mixed reproduction may play in pathogen evolution. We will test the hypothesis that the pathogen is undergoing evolution in adaptation to hemp. To test this hypothesis, we will sample B. gigantea from hemp and grasses in adjacent ecosystems, estimate gene flow between hosts and ecosystems and the frequency of sexual reproduction, and measure components of pathogen fitness among hosts in growth chamber experiments.Objective 3. Develop eco-evolutionary infectious disease models for coupled natural-agricultural systems.Infectious disease dynamics reflect the interplay of pathogen dynamics within individual hosts, growing-season transmission of infectious propagules among hosts, demographic impacts upon hosts, and pathogen persistence among years in dormant stages or reservoir hosts. It also reflects pathogen adaptation to different hosts and local environmental conditions, spatial (e.g., patchiness) and temporal (e.g., phenology) heterogeneities within and among host populations, and interactions with the microbiome. We will develop mathematical and computational models to explore how these processes influence cross-system spillover, and the potential for emergence of pathogen strains specialized to the novel hemp host (or generalized to both). Our multi-level framework will be used to addressthesekey theoretical questionsin infectious disease, transcendingdetails of our empirical system, and allow interrogation of the key processes that affect pathogen spillover events.We will develop models tailored to the specific empirical system (using data from Obj. 1 and 2), and also general theoretical models to illuminate emergence in multi-host systems more broadly. We will then use these ecological models as a springboard to examine evolutionary dynamics of fungal strains adapting to hemp.We will embed pathogen dynamics into a flexible model of individual plant growth, that accommodates multiple levels of investigation, thereby elucidating mechanisms of plant-pathogen transmission between ecosystems.

Progress 09/01/23 to 08/31/24

Outputs
Target Audience:We have worked closely with hemp growers in Kentucky during the first year of the project, including explaining the objectives of the work and providing information on the fungal pathogen we are studying. Changes/Problems:We did not face major problems, but the drought in Kentucky in August affected our field experiments and we are planning to use fewer sites and irrigation in Year 2. We were not able to recruit to oneof the University of Florida postdoc positions. We are readvertising the position to have a postdoc in place before summer 2025 and planning contingencies if we again face recruiting challenges. What opportunities for training and professional development has the project provided?Three graduate students were recruited to thethe project in year 1 for training inendophyte ecology and plant pathology.One undergraduate and one postdoc were trained in theoretical biology.Postdoc Simon received management training through KU (i.e., Managing Bias, Unpacking Whiteness in the Workplace, and Leadership Framework for Action on Equity and Inclusion). She has also participated in two data analysis workshops and honed communication skills by presenting a Rshiny app that was aproduct of a previous project. How have the results been disseminated to communities of interest?Undergraduate Pua presented modeling results at multiple conferences aimed at undergraduates and minorities in the sciences (see Products). What do you plan to do during the next reporting period to accomplish the goals?In Year 1, we collected critical baseline data. The Year 1 field experiments will form the basis of plans for the summer of Year 2, for endophyte analysis and subsequent experiments manipulating the endophytic community, and evolutionary and host range analyses of the pathogen. Similarly, we will continuing building complexity into our analytical models.

Impacts
What was accomplished under these goals? Objective 1. We conducted experiments at 6 locations to examine Microstegium as a conduit of the Bipolaris pathogen to hemp. We placed two varieties of hemp plants along six 5 meter transects per location. At one site, transects were extended to 10 and 20 meters. Disease data were collected in August and September, but limited by drought conditions in August. Plant samples were obtained for endophyte isolation and analysis. Objective 2. Samples were collected for pathogen isolation for population and evolutionary analyses. Objective 3. Two major theoretical projects have progressed. For the first, Postdoc Simon and PIs Orive and Holt developed an individual-based model of plant individuals in a landscape. Individuals engage in both resource competition (modeled using a "zone-of-influence" framework) and host-pathogen dynamics that assumes that presence of a fungal foliar disease that can transmit between individuals (via spore dispersal) and within individuals (via fungal hyphae growth). Currently, this model is being used to explore how disease alters a well-known empirical phenomenon that occurs under resource competition, but in the absence of disease called self-thinning. A manuscript related to this work is in preparation and will be submitted early in spring 2025. For the second project, Simon and Orive developed a model exploring the role of infected litter in disease establishment and persistence in a single host that can support disease both in its live plant tissue and shed litter (i.e., dead tissue). Analysis of this scenario will guide understanding of the modes of disease transmission in the hemp-Microstegium field system. In addition to these, Undergraduate Researcher Pua and PI Orive and collaborator F.B. Agusto have developed a compartmental epidemiological model for a two plant-host system with a shared fungal pathogen; Pua has presented this work at several local and national conferences and a manuscript is in preparation.

Publications

  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2024 Citation: Pua, S., F.B. Agusto, and M.E. Orive. Two plants hosts fungal pathogen model, KU Online Undergraduate Research Symposium, Lawrence KS, April 21-25, 2024.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2024 Citation: Pua, S., F.B. Agusto, and M.E. Orive. Model of a multiple plant host  fungal pathogen system (poster), KU-Haskell Indian Nations Undergraduate Research Symposium, Lawrence, KS, April 12, 2024.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2023 Citation: Pua, S., F.B. Agusto, and M.E. Orive. Model of a multiple plant host  fungal pathogen system (poster), Annual Biomedical Research Conference for Minoritized Scientists (ABRCMS), Phoenix, AZ, November 15-18, 2023.