Collaborative Research: Developing a new framework to understand the evolution of specialization in plant-endosymbiont response to varying environments

A stressful environment presents major challenges to organisms, including imposing new and potentially more requirements for them to survive. Partnerships between two different organisms, such as the mutualistic associations between a plant and soil fungi, can determine how they respond to, and thrive under the new environment. However, the status of these associations can change, for example, from beneficial (both partners exchange benefits) to neutral (no benefits or harm) or harmful (one partner may cause harm to the other), depending on the prevailing conditions. For coastal marshes facing new, stressful environments, these associations can be critical, but insights are limited. This project will evaluate the extent of mutual partnership between a saltmarsh grass and fungal partner along a natural stress gradient. It will also assess if, when and how these associations change when exposed to salinity stress. The outcomes of the project will include a publicly available database/collection of fungal beneficial partners that can aid management decisions geared towards conservation and restoration of coastal ecosystems under increasing environmental stress. The project will provide 3-year training of early-career Americans, who will receive cross-disciplinary education and training across different skillsets including fieldwork, greenhouse, microbial, genomic and analytical skills. Through partnerships will local communities, it will further benefit local high school students and biology teachers who will be given opportunities to conduct classroom research on saltmarsh and fungi as well as present their work and network with other students and researchers in a local symposium that the team will organize. Extreme environmental events can influence the evolutionary trajectories of host-endosymbiont associations. While several theoretical models predicting organismal responses exist, very few capture how host-endosymbiont relationships can evolve under extreme events. The proposed research will develop a framework that combines the stress gradient hypothesis and the geographic mosaic theory of coevolution to predict the evolution of specialized host-endosymbiont relationships in dynamic environments, and the adaptive benefits of such partnership in shaping host species resilience to extreme events. This framework will be tested using Spartina alterniflora, a dominant salt marsh grass, and its dark septate endophyte (DSE) fungal partners. The project will (Aim 1) evaluate levels of S. alterniflora population genomic variation and structure and levels of in situ DSE colonization along natural gradient of salinity. It will (Aim 2) characterize the DSE community, genotypic diversity and functional traits promoting salinity stress tolerance by conducting salinity assays to isolate, identify and determine fitness of DSE strains/genotypes associated with specific S. alterniflora genotypes. Finally, (Aim 3) the frequency, direction, dependency and specialization of the S. alterniflora-DSE relationship will be tested when exposed to different salinity regimes. A reciprocal-cross experiment will be conducted to determine the fitness outcomes and specialization among host-DSE pairings across the salinity gradient and when exposed to novel salinity conditions. These integrative experiments will enable us to achieve a holistic perspective on how evolution of specialized host-endosymbiont interactions can contribute to organism resilience in new and stressful environments. This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.