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The spermosphere represents a short-lived, rapidly changing, and microbiologically dynamic zone of soil surrounding a germinating seed. It is analogous to the rhizosphere, being established largely by the carbon compounds released into the soil once the seed begins to hydrate. These seed exudations drive the microbial activities that take place in the spermosphere, many of which can have long-lasting impacts on plant growth and development as well as on plant health. In this review, I discuss the nature of the spermosphere habitat and the factors that give rise to its character, with emphasis on the types of microbial activities in the spermosphere that have important implications for disease development and biological disease control. This review, which represents the first comprehensive synthesis of the literature on spermosphere biology, is meant to illustrate the unique nature of the spermosphere and how studies of interactions in this habitat may serve as useful experimental models for testing hypotheses about plant-microbe associations and microbial ecology.

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Leaf composts were studied for their suppressive effects on Pythium ultimum sporangium germination, cottonseed colonization, and the severity of Pythium damping-off of cotton. A focus of the work was to assess the role of fatty-acid-metabolizing microbial communities in disease suppression. Suppressiveness was expressed within the first few hours of seed germination as revealed by reduced P. ultimum sporangium germination, reduced seed colonization, and reduced damping-off in transplant experiments. These reductions were not observed when cottonseeds were sown in a conducive leaf compost. Microbial consortia recovered from the surface of cottonseeds during the first few hours of germination in suppressive compost (suppressive consortia) induced significant levels of damping-off suppression, whereas no suppression was induced by microbial consortia recovered from cottonseeds germinated in conducive compost (conducive consortia). Suppressive consortia rapidly metabolized linoleic acid, whereas conducive consortia did not. Furthermore, populations of fatty-acidmetabolizing bacteria and actinobacteria were higher in suppressive consortia than in conducive consortia. Individual bacterial isolates varied in their ability to metabolize linoleic acid and protect seedlings from damping-off. Results indicate that communities of compost-inhabiting microorganisms colonizing cottonseeds within the first few hours after sowing in a Pythium-suppressive compost play a major role in the suppression of P. ultimum sporangium germination, seed colonization, and damping-off. Results further indicate that fatty acid metabolism by these seed-colonizing bacterial consortia can explain the Pythium suppression observed.

Soil pathogens are believed to be major contributors to negative plant–soil feedbacks that regulate plant community dynamics and plant invasions. While the theoretical basis for pathogen regulation of plant communities is well established within the plant–soil feedback framework, direct experimental evidence for pathogen community responses to plants has been limited, often relying largely on indirect evidence based on above-ground plant responses. As a result, specific soil pathogen responses accompanying above-ground plant community dynamics are largely unknown. Here, we examine the oomycete pathogens in soils conditioned by established populations of native noninvasive and non-native invasive haplotypes of Phragmites australis (European common reed). Our aim was to assess whether populations of invasive plants harbor unique communities of pathogens that differ from those associated with noninvasive populations and whether the distribution of taxa within these communities may help to explain invasive success. We compared the composition and abundance of pathogenic and saprobic oomycete species over a 2-year period. Despite a diversity of oomycete taxa detected in soils from both native and non-native populations, pathogen communities from both invaded and noninvaded soils were dominated by species of Pythium. Pathogen species that contributed the most to the differences observed between invaded and noninvaded soils were distributed between invaded and noninvaded soils. However, the specific taxa in invaded soils responsible for community differences were distinct from those in noninvaded soils that contributed to community differences. Our results indicate that, despite the phylogenetic relatedness of native and non-native P. australis haplotypes, pathogen communities associated with the dominant non-native haplotype are distinct from those of the rare native haplotype. Pathogen taxa that dominate either noninvaded or invaded soils suggest different potential mechanisms of invasion facilitation. These findings are consistent with the hypothesis that non-native plant species that dominate landscapes may “cultivate” a different soil pathogen community to their rhizosphere than those of rarer native species.

A growing body of literature supports microbial symbiosis as a foundational principle for the competitive success of invasive plant species. Further exploration of the relationships between invasive species and their associated microbiomes, as well as the interactions with the microbiomes of native species, can lead to key new insights into invasive success and potentially new and effective control approaches. In this manuscript, we review microbial relationships with plants, outline steps necessary to develop invasive species control strategies that are based on those relationships, and use the invasive plant species Phragmites australis (common reed) as an example of how development of microbial-based control strategies can be enhanced using a collective impact approach. The proposed science agenda, developed by the Collaborative for Microbial Symbiosis and Phragmites Management, contains a foundation of sequential steps and mutually-reinforcing tasks to guide the development of microbial-based control strategies for Phragmites and other invasive species. Just as the science of plant-microbial symbiosis can be transferred for use in other invasive species, so too can the model of collective impact be applied to other avenues of research and management.

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