Dataset Information

Elevated Ozone Concentration and Nitrogen Addition Increase Poplar Rust Severity by Shifting the Phyllosphere Microbial Community.

ABSTRACT: Tropospheric ozone and nitrogen deposition are two major environmental pollutants. A great deal of research has focused on the negative impacts of elevated O₃ and the complementary effect of soil N addition on the physiological properties of trees. However, it has been overlooked how elevated O₃ and N addition affect tree immunity in face of pathogen infection, as well as of the important roles of phyllosphere microbiome community in host-pathogen-environment interplay. Here, we examined the effects of elevated O₃ and soil N addition on poplar leaf rust [Melampsora larici-populina] severity of two susceptible hybrid poplars [clone '107': Populus euramericana cv. '74/76'; clone '546': P. deltoides Í P. cathayana] in Free-Air-Controlled-Environment plots, in addition, the link between Mlp-susceptibility and changes in microbial community was determined using Miseq amplicon sequencing. Rust severity of clone '107' significantly increased under elevated O₃ or N addition only; however, the negative impact of elevated O₃ could be significantly mitigated when accompanied by N addition, likewise, this trade-off was reflected in its phyllosphere microbial α-diversity responding to elevated O₃ and N addition. However, rust severity of clone '546' did not differ significantly in the cases of elevated O₃ and N addition. Mlp infection altered microbial community composition and increased its sensitivity to elevated O₃, as determined by the markedly different abundance of taxa. Elevated O₃ and N addition reduced the complexity of microbial community, which may explain the increased severity of poplar rust. These findings suggest that poplars require a changing phyllosphere microbial associations to optimize plant immunity in response to environmental changes.

SUBMITTER: Tao S

PROVIDER: S-EPMC9148057 | biostudies-literature | 2022 May

REPOSITORIES: biostudies-literature

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Publications

Elevated Ozone Concentration and Nitrogen Addition Increase Poplar Rust Severity by Shifting the Phyllosphere Microbial Community.

Tao Siqi S Zhang Yunxia Y Tian Chengming C Duplessis Sébastien S Zhang Naili N

Journal of fungi (Basel, Switzerland) 20220518 5

Tropospheric ozone and nitrogen deposition are two major environmental pollutants. A great deal of research has focused on the negative impacts of elevated O<sub>3</sub> and the complementary effect of soil N addition on the physiological properties of trees. However, it has been overlooked how elevated O<sub>3</sub> and N addition affect tree immunity in face of pathogen infection, as well as of the important roles of phyllosphere microbiome community in host-pathogen-environment interplay. Her ...[more]

PMID: 35628778

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Project description:Microbes constitute a vital part of the plant holobiont. They establish plant-microbe or microbe-microbe associations, forming a unique microbiota with each plant species and under different environmental conditions. These microbial communities have to adapt to diverse environmental conditions, such as geographical location, climate conditions and soil types, and are subjected to changes in their surrounding environment. Elevated ozone concentration is one of the most important aspects of global change, but its effect on microbial communities living on plant surfaces has barely been investigated. In the current study, we aimed at elucidating the potential effect of elevated ozone concentrations on the phyllosphere (aerial part of the plant) and rhizoplane (surface of the root) microbiota by adopting next-generation 16S rRNA amplicon sequencing. A standard japonica rice cultivar Nipponbare and an ozone-tolerant breeding line L81 (Nipponbare background) were pre-grown in a greenhouse for 10 weeks and then exposed to ozone at 85 ppb for 7 h daily for 30 days in open top chambers. Microbial cells were collected from the phyllosphere and rhizoplane separately. The treatment or different genotypes did not affect various diversity indices. On the other hand, the relative abundance of some bacterial taxa were significantly affected in the rhizoplane community of ozone-treated plants. A significant effect of ozone was detected by homogeneity of molecular variance analysis in the phyllosphere, meaning that the community from ozone-treated phyllosphere samples was more variable than those from control plants. In addition, a weak treatment effect was observed by clustering samples based on the Yue and Clayton and weighted UniFrac distance matrices among samples. We therefore conclude that the elevated ozone concentrations affected the bacterial community structure of the phyllosphere and the rhizosplane as a whole, even though this effect was rather weak and did not lead to changes of the function of the communities.

Project description:Plant primary productivity and crop yields have been reduced due to the doubled level of global tropospheric ozone. Little is known about how elevated ozone affects soil microbial communities in the cropland ecosystem and whether such effects are sensitive to the nitrogen (N) supply. Here, we examined the responses of bacterial and fungal communities in maize soils to elevated ozone (+60 ppb ozone) across different levels of N fertilization (+60, +120, and +240 kg N ha-1yr-1). The fungal alpha diversity was decreased (P < 0.05), whereas the bacterial alpha diversity displayed no significant change under elevated ozone. Significant (P < 0.05) effects of N fertilization and elevated ozone on both the bacterial and fungal communities were observed. However, no interactive effects between N fertilization and elevated ozone were observed for bacterial and fungal communities (P > 0.1). The bacterial responses to N fertilization as well as the bacterial and fungal responses to elevated ozone were all phylogenetically conserved, showing universal homogeneous selection (homogeneous environmental conditions leading to more similar community structures). In detail, bacterial Alphaproteobacteria, Actinobacteria, and Chloroflexi, as well as fungal Ascomycota, were increased by elevated ozone, whereas bacterial Gammaproteobacteria, Bacteroidetes, and Elusimicrobia, as well as fungal Glomeromycota, were decreased by elevated ozone (P < 0.05). These ozone-responsive phyla were generally correlated (P < 0.05) with plant biomass, plant carbon (C) uptake, and soil dissolved organic C, demonstrating that elevated ozone affects plant-microbe interactions. Our study highlighted that microbial responses to elevated ozone display a phylogenetic clustering pattern, suggesting that response strategies to elevated ozone stress may be phylogenetically conserved ecological traits. IMPORTANCE The interactions of plant and soil microbial communities support plant growth and health. The increasing tropospheric ozone decreases crop biomass and also alters soil microbial communities, but the ways in which crops and their associated soil microbial communities respond to elevated tropospheric ozone are not clear, and it is also obscure whether the interactions between ozone and the commonly applied N fertilization exist. We showed that the microbial responses to both elevated ozone and N fertilization were phylogenetically conserved. However, the microbial communities that responded to N fertilization and elevated ozone were different, and this was further verified by the lack of an interactive effect between N fertilization and elevated ozone. Given that the global tropospheric ozone concentration will continue to increase in the coming decades, the decrease of specific microbial populations caused by elevated ozone would result in the extinction of certain microbial taxa. This ozone-induced effect will further harm crop production, and awareness is urgently needed.

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Project description:Plant-associated microbial communities play a central role in the plant response to biotic and abiotic stimuli, improving plant fitness under challenging growing conditions. Many studies have focused on the characterization of changes in abundance and composition of root-associated microbial communities as a consequence of the plant response to abiotic factors such as altered soil nutrients and drought. However, changes in composition in response to abiotic factors are still poorly understood concerning the endophytic community associated to the phyllosphere, the above-ground plant tissues. In the present study, we applied high-throughput 16S rDNA gene sequencing of the phyllosphere endophytic bacterial communities colonizing wild Populus trichocarpa (black cottonwood) plants growing in native, nutrient-limited environments characterized by hot-dry (xeric) riparian zones (Yakima River, WA), riparian zones with mid hot-dry (Tieton and Teanaway Rivers, WA) and moist (mesic) climates (Snoqualmie, Skykomish and Skagit Rivers, WA). From sequencing data, 587 Amplicon Sequence Variants (ASV) were identified. Surprisingly, our data show that a core microbiome could be found in phyllosphere-associated endophytic communities in trees growing on opposite sides of the Cascades Mountain Range. Considering only taxa appearing in at least 90% of all samples within each climatic zone, the core microbiome was dominated only by two ASVs affiliated Pseudomonadaceae and two ASVs of the Enterobacteriaceae family. Alpha-diversity measures indicated that plants colonizing hot-dry environments showed a lower diversity than those from mid hot-dry and moist climates. Beta-diversity measures showed that bacterial composition was significantly different across sampling sites. Accordingly, we found that specific ASV affiliated to Pseudomonadaceae and Enterobacteriaceae were significantly more abundant in the phyllosphere endophytic community colonizing plants adapted to the xeric environment. In summary, this study highlights that sampling site is the major driver of variation and that only a few ASV showed a distribution that significantly correlated to climate variables.

Dataset Information

Elevated Ozone Concentration and Nitrogen Addition Increase Poplar Rust Severity by Shifting the Phyllosphere Microbial Community.

Publications

Elevated Ozone Concentration and Nitrogen Addition Increase Poplar Rust Severity by Shifting the Phyllosphere Microbial Community.

Similar Datasets

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