Microbial activity in drylands is mediated by the magnitude and frequency of growing season rain events that will shift as climate change progresses. Nitrogen is often co-limiting with water availability to dryland plants, and thus we investigated how microbes important to the nitrogen (N) cycle and soil N availability varied temporally and spatially in the context of a long-term rainfall variability experiment in the northern Chihuahuan Desert. Specifically, we assessed biological soil crust (biocrust) chlorophyll content, fungal abundance, and inorganic N in soils adjacent to individuals of the grassland foundation species, Bouteloua eriopoda, and in the unvegetated interspace at multiple time points associated with an experimental monsoon rain treatment. Treatments included small weekly (5 mm) or large monthly (20 mm) rain events, which had been applied during the summer monsoon for nine years prior to our sampling. Additionally, we evaluated target plant C:N ratios and added 15 N-glutamate to biocrusts to determine potential for nutrient transport to B. eriopoda. Biocrust chlorophyll was up to 67% higher in the small weekly or large monthly rainfall regimes compared to ambient controls. Fungal biomass was 57% lower in soil interspaces than adjacent to plants but did not respond to rainfall regime treatments. Ammonium and nitrate concentrations near plants declined through the sampling period but varied little in soil interspaces. There was limited movement of 15 N from interspace biocrusts to leaves but high 15 N retention in the soils even after additional ambient and experimental rain events. Plant C:N ratio was unaffected by rainfall treatments. The long-term alteration in rainfall regime in this experiment did not change how short-term microbial abundance or N availability responded to the magnitude or frequency of events, suggesting a limited response of N availability to future climate change.
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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
- NSF-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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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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Abstract Basic helix–loop–helix (bHLH) transcription factors constitute a superfamily in eukaryotes, but their roles in plant immunity remain largely uncharacterized. We found that the transcript abundance in tomato (Solanum lycopersicum) leaves of one bHLH transcription factor-encoding gene, negative regulator of resistance to DC3000 1 (Nrd1), increased significantly after treatment with the immunity-inducing flgII-28 peptide. Plants carrying a loss-of-function mutation in Nrd1 (Δnrd1) showed enhanced resistance to Pseudomonas syringae pv. tomato (Pst) DC3000 although early pattern-triggered immunity responses, such as generation of reactive oxygen species and activation of mitogen-activated protein kinases after treatment with flagellin-derived flg22 and flgII-28 peptides, were unaltered compared to wild-type plants. RNA-sequencing (RNA-seq) analysis identified a gene, Arabinogalactan protein 1 (Agp1), whose expression is strongly suppressed in an Nrd1-dependent manner. Agp1 encodes an arabinogalactan protein, and overexpression of the Agp1 gene in Nicotiana benthamiana led to ∼10-fold less Pst growth compared to the control. These results suggest that the Nrd1 protein promotes tomato susceptibility to Pst by suppressing the defense gene Agp1. RNA-seq also revealed that the loss of Nrd1 function has no effect on the transcript abundance of immunity-associated genes, including AvrPtoB tomato-interacting 9 (Bti9), Cold-shock protein receptor (Core), Flagellin sensing 2 (Fls2), Flagellin sensing (Fls3), and Wall-associated kinase 1 (Wak1) upon Pst inoculation, suggesting that the enhanced immunity observed in the Δnrd1 mutants is due to the activation of key PRR signaling components as well as the loss of Nrd1-regulated suppression of Agp1.
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Summary Microbial communities will experience novel climates in the future. Dispersal is now recognized as a driver of microbial diversity and function, but our understanding of how dispersal influences responses to novel climates is limited. We experimentally tested how the exclusion of aerially dispersed fungi and bacteria altered the compositional and functional response of soil microbial communities to drought. We manipulated dispersal and drought by collecting aerially deposited microbes after precipitation events and subjecting soil mesocosms to either filter‐sterilized rain (no dispersal) or unfiltered rain (dispersal) and to either drought (25% ambient) or ambient rainfall for 6 months. We characterized community composition by sequencing 16S and ITS rRNA regions and function using community‐level physiological profiles. Treatments without dispersal had lower soil microbial biomass and metabolic diversity but higher bacterial and fungal species richness. Dispersal also altered soil community response to drought; drought had a stronger effect on bacterial (but not fungal) community composition, and induced greater functional loss, when dispersal was present. Surprisingly, neither immigrants nor drought‐tolerant taxa had higher abundance in dispersal treatments. We show experimentally that natural aerial dispersal rate alters soil microbial responses to disturbance. Changes in dispersal rates should be considered when predicting microbial responses to climate change.
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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
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1094/PBIOMES-04-21-0025-R
