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.
Experimental Evidence Pointing to Rain as a Reservoir of Tomato Phyllosphere Microbiota
Plant microbiota play essential roles in plant health and crop productivity. Comparisons of community composition have suggested seed, soil, and the atmosphere as reservoirs of phyllosphere microbiota. After finding that leaves of tomato (Solanum lycopersicum) plants exposed to rain carried a higher microbial population size than leaves of tomato plants not exposed to rain, we experimentally tested the hypothesis that rain is a thus-far-neglected reservoir of phyllosphere microbiota. Therefore, rain microbiota were compared with phyllosphere microbiota of tomato plants either treated with concentrated rain microbiota, filter-sterilized rain, or sterile water. Based on 16S ribosomal RNA amplicon sequencing, 104 operational taxonomic units (OTUs) significantly increased in relative abundance after inoculation with concentrated rain microbiota but no OTU significantly increased after treatment with either sterile water or filter-sterilized rain. Some of the genera to which these 104 OTUs belonged were also found at higher relative abundance on tomato plants exposed to rain outdoors than on tomato plants grown protected from rain in a commercial greenhouse. Taken together, these results point to precipitation as a reservoir of phyllosphere microbiota and show the potential of controlled experiments to investigate the role of different reservoirs in the assembly of phyllosphere microbiota.
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- Award ID(s):
- 1754721
- PAR ID:
- 10321224
- Date Published:
- Journal Name:
- Phytobiomes Journal
- Volume:
- 5
- Issue:
- 4
- ISSN:
- 2471-2906
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
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Summary Water and nutrient acquisition are key drivers of plant health and ecosystem function. These factors impact plant physiology directly as well as indirectly through soil‐ and root‐associated microbial responses, but how they in turn affect aboveground plant–microbe interactions are not known.
Through experimental manipulations in the field and growth chamber, we examine the interacting effects of water stress, soil fertility, and arbuscular mycorrhizal fungi on bacterial and fungal communities of the tomato (
Solanum lycopersicum ) phyllosphere.Both water stress and mycorrhizal disruption reduced leaf bacterial richness, homogenized bacterial community composition among plants, and reduced the relative abundance of dominant fungal taxa. We observed striking parallelism in the individual microbial taxa in the phyllosphere affected by irrigation and mycorrhizal associations.
Our results show that soil conditions and belowground interactions can shape aboveground microbial communities, with important potential implications for plant health and sustainable agriculture.
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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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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.more » « less
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null (Ed.)Leaf fungal endophytes (LFEs) contribute to plant growth and responses to stress. Fungi colonize leaves through maternal transmission, e.g. via the seed, and through environmental transmission, e.g. via aerial dispersal. The relative importance of these two pathways in assembly and function of the LFE community is poorly understood. We used amplicon sequencing to track switchgrass ( Panicum virgatum ) LFEs in a greenhouse and field experiment as communities assembled from seed endophytes and rain fungi (integration of wet and dry aerial dispersal) in germinating seeds, seedlings, and adult plants. Rain fungi varied temporally and hosted a greater portion of switchgrass LFE richness (greater than 65%) than were found in seed endophytes (greater than 25%). Exposure of germinating seeds to rain inoculum increased dissimilarity between LFE communities and seed endophytes, increasing the abundance of rain-derived taxa, but did not change diversity. In the field, seedling LFE composition changed more over time, with a decline in seed-derived taxa and an increase in richness, in response to environmental transmission than LFEs of adult plants. We show that environmental transmission is an important driver of LFE assembly, and likely plant growth, but its influence depends on both the conditions at the time of colonization and plant life stage.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1094/PBIOMES-04-21-0025-R
