As a microbiome ecologist, I use community ecology theory to move beyond simple characterization of host-associated microbial communities to understand their role in the health and physiology of their hosts. My research has primarily focused on plants and foliar endophytic fungi, functionally dominant members of the plant leaf microbiome. I integrate cutting-edge molecular and stable isotope techniques, traditional culture-based approaches, and manipulative greenhouse and field experiments to answer questions about the assembly, maintenance, and function of microbial symbioses.
Harnessing aboveground-belowground microbial interactions for soybean health and productivity
In a changing world, it has become critical that we design sustainable systems for food, bioenergy, and industrial feedstock production that minimize inputs such as water, energy, pesticides, and fertilizer. Recently, there has been growing interest in integrating beneficial microbiota into agriculture to alleviate these problems. Plant-associated microorganisms can affect hosts in ways that are relevant to agricultural production, such as increasing growth, nutrient acquisition and uptake, enemy defense, and drought tolerance. In fact, the metagenomic potential of plant-associated microbiomes has been proposed to surpass the genomic abilities of plants, and represents an extensive and untapped reservoir for improving agriculturally important traits. To successfully integrate microbial symbioses into agriculture, we need to understand how complex and interacting suites of microbes interact with plants to alter key host traits.
To date, most work investigating effects of microbiota on their host plants has focused on inoculating plants with a single microbe and documenting its effects. While informative to basic science, this one-plant-one-microbe construct is an artifact of the laboratory and of questionable value for real-world systems. In nature, as well as in agriculture, co-infection of host tissues by microorganisms is the norm, yet we know almost nothing about how aboveground and belowground microbial colonizers interact to affect host plant health and productivity. This is despite recognition of co-colonization of the vast majority of land plants by above- and belowground microbes, and aboveground plant signaling affecting belowground responses and vice versa (though primarily in response to herbivores). I am currently investigating how selection for increased yield and disease resistance has altered soybean’s association with above- and belowground microbiota, and will capitalize on interactions between different soybean symbionts to optimize host yield and resistance. This work is in collaboration with Katy Heath (University of Illinois) and Posy Busby (Oregon State University) and is funded by a USDA AFRI ELI Postdoctoral Fellowship.
To date, most work investigating effects of microbiota on their host plants has focused on inoculating plants with a single microbe and documenting its effects. While informative to basic science, this one-plant-one-microbe construct is an artifact of the laboratory and of questionable value for real-world systems. In nature, as well as in agriculture, co-infection of host tissues by microorganisms is the norm, yet we know almost nothing about how aboveground and belowground microbial colonizers interact to affect host plant health and productivity. This is despite recognition of co-colonization of the vast majority of land plants by above- and belowground microbes, and aboveground plant signaling affecting belowground responses and vice versa (though primarily in response to herbivores). I am currently investigating how selection for increased yield and disease resistance has altered soybean’s association with above- and belowground microbiota, and will capitalize on interactions between different soybean symbionts to optimize host yield and resistance. This work is in collaboration with Katy Heath (University of Illinois) and Posy Busby (Oregon State University) and is funded by a USDA AFRI ELI Postdoctoral Fellowship.
Assembly and maintenance of foliar endophyte communities
Foliar endophytic fungi are environmentally-acquired symbionts, whose diverse communities reside cryptically within the healthy photosynthetic tissue of all plant species sampled to date. Endophyte colonization can benefit host plants by enhancing defense against pathogens and herbivores, but with demonstrated costs including latent pathogenicity and lowered host photosynthetic rate. A critical question in both endophyte ecology and broader ecological theory is to what extent do abiotic and biotic factors affect community composition? Moreover, does community assembly of endophytes carry functional consequences for plant hosts?
In collaboration with Allen Herre and Luis Mejia at the Smithsonian Tropical Research Institute (STRI) in Panama, I manipulated local environmental factors and show that leaf litter exposure and vertical stratification have dramatic effects on cacao’s microbiome. Remarkably, exposure to litter from cacao adults significantly reduced pathogen damage on conspecific seedlings – an effect attributable to microbiota transferred from litter that enriched the seedling microbiome with fungal species that enhanced pathogen resistance. Analogous ideas of “seeding” a healthy microbiome into hosts have been documented in human microbiome studies, including fecal transplants and maternal transmission of a healthy microbiome to infants. Read more about this work in the Proceedings of the Royal Society B and its coverage by Scientific American, and check out my interview with Quirks and Quarks on CBC Radio. I am currently using RNA-seq to more rigorously define how host and microbial gene expression drive patterns of community assembly and plant pathogen resistance.
Common garden studies in collaboration with Briana Whitaker, Chai Qing, and Keith Clay at Indiana University (IU), as well as with Allen Herre and Luis Mejia at STRI in Panama, have independently shown that endophyte communities exhibit some degree of host-specificity, even when microclimate and local spore sources are largely the same for all plants. However, despite a growing number of studies characterizing endophyte community composition and function, the mechanisms by which plant hosts select and maintain mutually beneficial horizontally-transmitted symbioses with leaf microbiota remain largely unknown. These processes may potentially be informed by theoretical and empirical work conducted on interactions with root symbionts and plant pollinators, where preferential allocation of resources to more beneficial partners has been shown to promote mutualism stability. We tested for analogous patterns of preferential allocation in foliar endophytes of cacao by inoculating leaves with four common symbionts that range in their effect from protective to pathogenic. We then traced Nitrogen-15 uptake and its subsequent allocation to whole plants and individual leaves. While we found mixed support for preferential allocation to more beneficial foliar endosymbionts, our results indicate that that colonization by foliar endophytes has major effects on nitrogen uptake and alters its distribution within plant hosts in ways that appear to be context-dependent on other microbiome components. Read more about this work in New Phytologist.
In collaboration with Allen Herre and Luis Mejia at the Smithsonian Tropical Research Institute (STRI) in Panama, I manipulated local environmental factors and show that leaf litter exposure and vertical stratification have dramatic effects on cacao’s microbiome. Remarkably, exposure to litter from cacao adults significantly reduced pathogen damage on conspecific seedlings – an effect attributable to microbiota transferred from litter that enriched the seedling microbiome with fungal species that enhanced pathogen resistance. Analogous ideas of “seeding” a healthy microbiome into hosts have been documented in human microbiome studies, including fecal transplants and maternal transmission of a healthy microbiome to infants. Read more about this work in the Proceedings of the Royal Society B and its coverage by Scientific American, and check out my interview with Quirks and Quarks on CBC Radio. I am currently using RNA-seq to more rigorously define how host and microbial gene expression drive patterns of community assembly and plant pathogen resistance.
Common garden studies in collaboration with Briana Whitaker, Chai Qing, and Keith Clay at Indiana University (IU), as well as with Allen Herre and Luis Mejia at STRI in Panama, have independently shown that endophyte communities exhibit some degree of host-specificity, even when microclimate and local spore sources are largely the same for all plants. However, despite a growing number of studies characterizing endophyte community composition and function, the mechanisms by which plant hosts select and maintain mutually beneficial horizontally-transmitted symbioses with leaf microbiota remain largely unknown. These processes may potentially be informed by theoretical and empirical work conducted on interactions with root symbionts and plant pollinators, where preferential allocation of resources to more beneficial partners has been shown to promote mutualism stability. We tested for analogous patterns of preferential allocation in foliar endophytes of cacao by inoculating leaves with four common symbionts that range in their effect from protective to pathogenic. We then traced Nitrogen-15 uptake and its subsequent allocation to whole plants and individual leaves. While we found mixed support for preferential allocation to more beneficial foliar endosymbionts, our results indicate that that colonization by foliar endophytes has major effects on nitrogen uptake and alters its distribution within plant hosts in ways that appear to be context-dependent on other microbiome components. Read more about this work in New Phytologist.
Disturbance in the plant microbiome
Little is known about how disturbances to plants affect their fungal symbiont communities. Together with Keith Clay and former IU undergraduate students Courtney Sullivan and Noelle Visser, I examined the tension between natural and anthropogenic disturbances and host identity and location, to ask if and how endophytic fungal communities are affected by perturbation. We conducted two experiments in order to test the effects of perturbation on endophyte communities in two different contexts: First, we examined endophyte response to a natural perturbation resulting from leaf mining insect activity. Second, we employed a manipulative study to test endophyte community response to an anthropogenic perturbation of fungicide application. We conducted both experiments using a perennial wildflower host native to the midwestern United States, Ageratina altissima (white snakeroot, Asteraceae). Although we hypothesized that both leaf mining and fungicide application would alter composition and diversity of the fungal microbiome, we found that endophyte communities are strongly buffered from perturbation, and that plant host individual and geographic location are instead the major determinants of endophyte community composition even in the face of these perturbations. Read more about this work in Microbial Ecology.Little is known about how disturbances to plants affect their fungal symbiont communities. Together with Keith Clay and former IU undergraduate students Courtney Sullivan and Noelle Visser, I examined the tension between natural and anthropogenic disturbances and host identity and location, to ask if and how endophytic fungal communities are affected by perturbation. We conducted two experiments in order to test the effects of perturbation on endophyte communities in two different contexts: First, we examined endophyte response to a natural perturbation resulting from leaf mining insect activity. Second, we employed a manipulative study to test endophyte community response to an anthropogenic perturbation of fungicide application. We conducted both experiments using a perennial wildflower host native to the midwestern United States, Ageratina altissima (white snakeroot, Asteraceae). Although we hypothesized that both leaf mining and fungicide application would alter composition and diversity of the fungal microbiome, we found that endophyte communities are strongly buffered from perturbation, and that plant host individual and geographic location are instead the major determinants of endophyte community composition even in the face of these perturbations. Read more about this work in Microbial Ecology.
Chemical ecology of plant microbiomes
An emerging question in the field of microbiome ecology is how colonization by microbiota alters the defensive chemical profiles of their hosts. Members of the plant microbiome have been shown to produce a myriad of secondary metabolites in culture, which may be responsible for suppressing disease or deterring herbivory. However, it is unclear if these compounds are also synthesized during symbiosis within the host plant, or if endophytes stimulate plant chemical responses, thus affecting how hosts interact with their enemies. Using the well-known toxic plant white snakeroot, preliminary results in collaboration with Noelle Visser show that plants treated with a dominant endophyte or a natural microbial spore source (rain water) produced a significantly larger breadth of chemical compounds, including the characteristic toxin tremetone, compared to uninoculated seedlings, although it is unclear if these chemicals were produced by endophytes, or by the plants themselves. Preliminary research from a collaboration with researchers at STRI (led by Brian Sedio) in a different host system (cacao) suggests the latter - that colonization by microbiota upregulates host chemical defense.
Competition between root mutualists
Plants engage in multiple root symbioses that offer varying degrees of benefit. In collaboration with Jim Bever at the University of Kansas, we are using theoretical approaches to understand how variation in partner quality persists. We considered the plant’s ability to preferentially allocate carbon to mutualists, and competition for plant carbon between mutualist and non-mutualist symbionts. We treated carbon as two nutritionally interchangeable, but temporally separated, resources – carbon allocated indiscriminately for the construction of the symbiosis, and carbon preferentially allocated to the mutualist after symbiosis establishment and assessment. This approach demonstrated that coexistence of mutualists and non-mutualists is possible when fidelity of the plant to the mutualist and the cost of mutualism mediate resource competition. Furthermore, it allows us to trace symbiont population dynamics given varying degrees of carbon allocation.
Along with Carli Gurholt, we are empirically testing how carbon allocation and competition affect population dynamics of arbuscular mycorrhizal fungi (AMF) using Allium vineale (wild onion) as our host plant. To do so, we are first developing new molecular techniques to quantify AMF in plant roots in collaboration with Tanya Cheek (Washington State University) and Ursel Shuette (University of Alaska Fairbanks).
Along with Carli Gurholt, we are empirically testing how carbon allocation and competition affect population dynamics of arbuscular mycorrhizal fungi (AMF) using Allium vineale (wild onion) as our host plant. To do so, we are first developing new molecular techniques to quantify AMF in plant roots in collaboration with Tanya Cheek (Washington State University) and Ursel Shuette (University of Alaska Fairbanks).