There is increasing interest in the plant microbiome as it relates to both plant health and agricultural sustainability. One key unanswered question is whether we can select for a plant microbiome that is robust after colonization of target hosts. We used a successive passaging experiment to address this question by selecting upon the tomato phyllosphere microbiome. Beginning with a diverse microbial community generated from field-grown tomato plants, we inoculated replicate plants across 5 plant genotypes for 4 45-d passages, sequencing the microbial community at each passage. We observed consistent shifts in both the bacterial (16S amplicon sequencing) and fungal (internal transcribed spacer region amplicon sequencing) communities across replicate lines over time, as well as a general loss of diversity over the course of the experiment, suggesting that much of the naturally observed microbial community in the phyllosphere is likely transient or poorly adapted within the experimental setting. We found that both host genotype and environment shape microbial composition, but the relative importance of genotype declines through time. Furthermore, using a community coalescence experiment, we found that the bacterial community from the end of the experiment was robust to invasion by the starting bacterial community. These results highlight that selecting for a stable microbiome that is well adapted to a particular host environment is indeed possible, emphasizing the great potential of this approach in agriculture and beyond. In light of the consistent response of the microbiome to selection in the absence of reciprocal host evolution (coevolution) described here, future studies should address how such adaptation influences host health.
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Plant neighborhood shapes diversity and reduces interspecific variation of the phyllosphere microbiome
Microbial communities associated with plant leaf surfaces (i.e., the phyllosphere) are increasingly recognized for their role in plant health. While accumulating evidence suggests a role for host filtering of its microbiota, far less is known about how community composition is shaped by dispersal, including from neighboring plants. We experimentally manipulated the local plant neighborhood within which tomato, pepper, or bean plants were grown in a 3-month field trial. Focal plants were grown in the presence of con- or hetero-specific neighbors (or no neighbors) in a fully factorial combination. At 30-day intervals, focal plants were harvested and replaced with a new age- and species-matched cohort while allowing neighborhood plants to continue growing. Bacterial community profiling revealed that the strength of host filtering effects (i.e., interspecific differences in composition) decreased over time. In contrast, the strength of neighborhood effects increased over time, suggesting dispersal from neighboring plants becomes more important as neighboring plant biomass increases. We next implemented a cross-inoculation study in the greenhouse using inoculum generated from the field plants to directly test host filtering of microbiomes while controlling for directionality and source of dispersal. This experiment further demonstrated that focal host species, the host from which the microbiome came, and in one case the donor hosts’ neighbors, contribute to variation in phyllosphere bacterial composition. Overall, our results suggest that local dispersal is a key factor in phyllosphere assembly, and that demographic factors such as nearby neighbor identity and biomass or age are important determinants of phyllosphere microbiome diversity.
more » « less- NSF-PAR ID:
- 10485283
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- The ISME Journal
- Volume:
- 16
- Issue:
- 5
- ISSN:
- 1751-7362
- Format(s):
- Medium: X Size: p. 1376-1387
- Size(s):
- ["p. 1376-1387"]
- Sponsoring Org:
- National Science Foundation
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Summary Epiphytic microbes frequently affect plant phenotype and fitness, but their effects depend on microbe abundance and community composition. Filtering by plant traits and deterministic dispersal‐mediated processes can affect microbiome assembly, yet their relative contribution to predictable variation in microbiome is poorly understood.
We compared the effects of host‐plant filtering and dispersal on nectar microbiome presence, abundance, and composition. We inoculated representative bacteria and yeast into 30 plants across four phenotypically distinct cultivars of
Epilobium canum . We compared the growth of inoculated communities to openly visited flowers from a subset of the same plants.There was clear evidence of host selection when we inoculated flowers with synthetic communities. However, plants with the highest microbial densities when inoculated did not have the highest microbial densities when openly visited. Instead, plants predictably varied in the presence of bacteria, which was correlated with pollen receipt and floral traits, suggesting a role for deterministic dispersal.
These findings suggest that host filtering could drive plant microbiome assembly in tissues where species pools are large and dispersal is high. However, deterministic differences in microbial dispersal to hosts may be equally or more important when microbes rely on an animal vector, dispersal is low, or arrival order is important.
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null (Ed.)Plant leaves harbor complex microbial communities that influence plant health and productivity. Nevertheless, a detailed understanding of phyllosphere community assembly and drivers is needed, particularly for phyllosphere fungi. Here, we investigated seasonal dynamics of epiphytic phyllosphere fungal communities in switchgrass (Panicum virgatum L.), a focal bioenergy crop. We also leverage previously published data on switchgrass phyllosphere bacterial communities from the same experimental plants, allowing us to compare fungal and bacterial dynamics and explore interdomain network associations in the switchgrass phyllosphere. Overall, we found a strong impact of sampling date on fungal community composition, with multiple taxonomic levels exhibiting clear temporal patterns in relative abundance. In addition, leaf nitrogen concentration, leaf dry matter content, plant height, and minimum daily air temperature explained significant variation in phyllosphere fungal communities, likely due to their correlation with sampling date. Finally, among the core taxa, fungi–bacteria network associations were much more common than bacteria–bacteria associations, suggesting the importance of interdomain phylogenetic diversity in microbiome assembly. Although our findings highlight the complexity of phyllosphere microbiome assembly, the clear temporal patterns in lineage-specific fungal abundances give promise to the potential for accurately predicting shifts in fungal phyllosphere communities throughout the growing season, a key research priority for sustainable agriculture. [Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .more » « less
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Abstract Associational effects—in which the vulnerability of a plant to herbivores is influenced by its neighbors—have been widely implicated in mediating plant–herbivore interactions. Studies of associational effects typically focus on interspecific interactions or pest–crop dynamics. However, associational effects may also be important for species with intraspecific variation in defensive traits. In this study, we observed hundreds of
Datura wrightii —which exhibits dimorphism in its trichome phenotype—from over 30 dimorphic populations across California. Our aim was to determine whether a relationship existed between the trichome phenotype of neighboring conspecifics and the likelihood of being damaged by four species of herbivorous insects. We visited plants at three timepoints to assess how these effects vary both within and between growing seasons. We hypothesized that the pattern of associational effects would provide rare morphs (i.e., focal plants that are a different morph than their neighbors) with an advantage in the form of reduced herbivory, thereby contributing to the negative frequency‐dependent selection previously documented in this system. We found the best predictor of herbivory/herbivore presence on focal plants was the phenotype of the focal plant. However, we also found some important neighborhood effects. The total number of plants near a focal individual predicted the likelihood and/or magnitude of herbivory byTupiochoris notatus ,Lema daturaphila , andManduca sexta . We also found that velvety focal plants with primarily sticky neighbors are more susceptible to infestation byTupiochoris notatus andLema daturaphila . This does not align with the hypothesis that associational effects at the near‐neighbor scale contribute to a rare‐morph advantage in this system. Overall, the results of our study show that the number and trichome‐morph composition of neighboring conspecifics impact interactions betweenD. wrightii and insect herbivores. -
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Abstract Metacommunity theory predicts that the composition and diversity of a site depend on its characteristics and those of its neighborhood. Dispersal between plots in a field experiment could link responses observed in a focal plot to both its treatment and those of its neighbors. However, the diversity, composition, and treatments of neighboring plots are rarely included in analyses of experimental treatments. We analyzed a spatially gridded grassland nitrogen addition experiment and found that plant species richness and the composition of focal plots were influenced not just by their nitrogen treatment but also by the number of species in neighboring plots and their abundances. For each additional species in a focal plot's neighborhood, the species richness of the focal plot increased by 0.30 species. Control plots had a significant loss of species, at a rate of ~0.23 species per year during the 23‐year experiment, but only when their neighborhoods had low species richness. Changes in the abundance of the three dominant species depended both on the nitrogen treatment of a focal plot and on their abundance in adjacent plots. Our analyses suggested that both the experimental nitrogen treatments and metacommunity processes codetermined plant species richness and plant species’ abundances. Our findings suggested that analyzing many traditional field experiments with a metacommunity perspective may reveal a confounding of experimental treatments and provide empirical data to test metacommunity theory.
