Nicotiana Roots Recruit Rare Rhizosphere Taxa as Major Root-Inhabiting Microbes

Saleem, Muhammad; Law, Audrey D.; Moe, Luke A.

doi:10.1007/s00248-015-0672-x

Cited by 70 publications

(48 citation statements)

References 24 publications

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“…Here, we report the impacts of phyllosphere–bacterial interactions on plant performance, determined here from assessments of the plant–microbe interaction across the plant life cycle. The phyllosphere supported a relatively greater abundance of beneficial rather than pathogenic bacteria under our common garden conditions that included the presence of fungus gnat herbivory ( Figures 1A,B and 4 ), which is consistent with the view that hosts recruit beneficial microbes in relatively greater numbers under stressed and normal conditions to obtain the maximum mutualistic benefits (Vorholt, 2012; Ortega et al, 2016; Saleem et al, 2016b). The Bacillus species group is ubiquitously abundant in soil and plant environments with multiple plant beneficial (anti-insect/pathogen) properties.…”

Section: Discussionsupporting

confidence: 83%

Microbial Interactions in the Phyllosphere Increase Plant Performance under Herbivore Biotic Stress

et al. 2017

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The phyllosphere supports a tremendous diversity of microbes and other organisms. However, little is known about the colonization and survival of pathogenic and beneficial bacteria alone or together in the phyllosphere across the whole plant life-cycle under herbivory, which hinders our ability to understand the role of phyllosphere bacteria on plant performance. We addressed these questions in experiments using four genetically and biogeographically diverse accessions of Arabidopsis thaliana, three ecologically important bacterial strains (Pseudomonas syringae DC3000, Xanthomonas campestris, both pathogens, and Bacillus cereus, plant beneficial) under common garden conditions that included fungus gnats (Bradysia spp.). Plants supported greater abundance of B. cereus over either pathogenic strain in the phyllosphere under such greenhouse conditions. However, the Arabidopsis accessions performed much better (i.e., early flowering, biomass, siliques, and seeds per plant) in the presence of pathogenic bacteria rather than in the presence of the plant beneficial B. cereus. As a group, the plants inoculated with any of the three bacteria (Pst DC3000, Xanthomonas, or Bacillus) all had a higher fitness than uninoculated controls under these conditions. These results suggest that the plants grown under the pressure of different natural enemies, such as pathogens and an herbivore together perform relatively better, probably because natural enemies induce host defense against each other. However, in general, a positive impact of Bacillus on plant performance under herbivory may be due to its plant-beneficial properties. In contrast, bacterial species in the mixture (all three together) performed poorer than as monocultures in their total abundance and host plant growth promotion, possibly due to negative interspecific interactions among the bacteria. However, bacterial species richness linearly promoted seed production in the host plants under these conditions, suggesting that natural enemies diversity may be beneficial from the host perspective. Collectively, these results highlight the importance of bacterial community composition on plant performance and bacterial abundance in the phyllosphere.

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Section: Discussionsupporting

confidence: 83%

Microbial Interactions in the Phyllosphere Increase Plant Performance under Herbivore Biotic Stress

et al. 2017

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“…Therefore, all of our RSA traits are based on growth in sterile media. There is no doubt that microbial communities are important for root growth (Rolli et al ., ; Saleem et al ., ). Indeed, anecdotally, we observed that plants heavily contaminated by microbial growth (and therefore not imaged for this study) had visibly different growth patterns.…”

Section: Discussionmentioning

confidence: 97%

Convergent evolution of root system architecture in two independently evolved lineages of weedy rice

2019

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Summary Root system architecture (RSA) is a critical aspect of plant growth and competitive ability. Here we used two independently evolved strains of weedy rice, a de‐domesticated form of rice, to study the evolution of weed‐associated RSA traits and the extent to which they evolve through shared or different genetic mechanisms. We characterised 98 two‐dimensional and three‐dimensional RSA traits in 671 plants representing parents and descendants of two recombinant inbred line populations derived from two weed × crop crosses. A random forest machine learning model was used to assess the degree to which root traits can predict genotype and the most diagnostic traits for doing so. We used quantitative trait locus (QTL) mapping to compare genetic architecture between the weed strains. The two weeds were distinguishable from the crop in similar and predictable ways, suggesting independent evolution of a ‘weedy’ RSA phenotype. Notably, comparative QTL mapping revealed little evidence for shared underlying genetic mechanisms. Our findings suggest that despite the double bottlenecks of domestication and de‐domestication, weedy rice nonetheless shows genetic flexibility in the repeated evolution of weedy RSA traits. Whereas the root growth of cultivated rice may facilitate interactions among neighbouring plants, the weedy rice phenotype may minimise below‐ground contact as a competitive strategy.

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“…The majority of such studies used fingerprinting techniques, which allowed differentiation of abundant bacteria at low phylogenetic resolution. In our study, we expanded investigation of the root bacteriome to the large bacterial diversity represented by low-abundance bacteria (Dohrmann et al, 2013; Nuccio et al, 2016; Saleem et al, 2016; Shi et al, 2016) and analyzed how this rare biosphere shapes the plant species-specific root bacteriome.…”

Section: Discussionmentioning

confidence: 99%

“…However, only few studies extended this knowledge so far to a more complete census of the plant species-specific rhizosphere bacterial community using modern next-generation amplicon sequencing approaches that target the phylogenetic breadth of most bacteria at sufficient sampling depth (Rodríguez-Echeverría et al, 2013; Rosenzweig et al, 2013; Hortal et al, 2015). Furthermore, studies on the role of low-abundance bacterial populations in shaping the plant species-specific root bacteriome are still scarce (Dohrmann et al, 2013; Nuccio et al, 2016; Saleem et al, 2016; Shi et al, 2016). …”

Section: Introductionmentioning

confidence: 99%

A Small Number of Low-abundance Bacteria Dominate Plant Species-specific Responses during Rhizosphere Colonization

et al. 2017

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Plant growth can be affected by soil bacteria. In turn, plants are known to influence soil bacteria through rhizodeposits and changes in abiotic conditions. We aimed to quantify the phylotype richness and relative abundance of rhizosphere bacteria that are actually influenced in a plant species-specific manner and to determine the role of the disproportionately large diversity of low-abundance bacteria belonging to the rare biosphere (<0.1 relative abundance) in this process. In addition, we aimed to determine whether plant phylogeny has an influence on the plant species-specific rhizosphere bacterial community. For this purpose, 19 herbaceous plant species from five different plant orders were grown in a common soil substrate. Bacterial communities in the initial soil substrate and the established rhizosphere soils were compared by 16S rRNA gene amplicon sequencing. Only a small number of bacterial operational taxonomic units (OTUs, 97% sequence identity) responded either positively (ca. 1%) or negatively (ca. 1%) to a specific plant species. On average, 91% of plant-specific positive response OTUs comprised bacteria belonging to the rare biosphere, highlighting that low-abundance populations are metabolically active in the rhizosphere. In addition, low-abundance OTUs were in terms of their summed relative abundance major drivers of the bacterial phyla composition across the rhizosphere of all tested plant species. However, no effect of plant phylogeny could be observed on the established rhizosphere bacterial communities, neither when considering differences in the overall established rhizosphere communities nor when considering plant species-specific responders only. Our study provides a quantitative assessment of the effect of plants on their rhizosphere bacteria across multiple plant orders. Plant species-specific effects on soil bacterial communities involved only 18–111 bacterial OTUs out of several 1000s; this minority may potentially impact plant growth in plant–bacteria interactions.

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Nicotiana Roots Recruit Rare Rhizosphere Taxa as Major Root-Inhabiting Microbes

Cited by 70 publications

References 24 publications

Microbial Interactions in the Phyllosphere Increase Plant Performance under Herbivore Biotic Stress

Microbial Interactions in the Phyllosphere Increase Plant Performance under Herbivore Biotic Stress

Convergent evolution of root system architecture in two independently evolved lineages of weedy rice

A Small Number of Low-abundance Bacteria Dominate Plant Species-specific Responses during Rhizosphere Colonization

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