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Structure, variation, and assembly of the root-associated microbiomes of rice

Joseph Edwards, Cameron Johnson, Christian Santos-Medellín, Eugene Lurie, Natraj Kumar Podishetty, Srijak Bhatnagar, Jonathan A. Eisen, and Venkatesan Sundaresan
PNAS February 24, 2015 112 (8) E911-E920; published ahead of print January 20, 2015 https://doi.org/10.1073/pnas.1414592112
Joseph Edwards
Departments of aPlant Biology,
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Cameron Johnson
Departments of aPlant Biology,
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Christian Santos-Medellín
Departments of aPlant Biology,
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Eugene Lurie
Departments of aPlant Biology,
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Natraj Kumar Podishetty
bPlant Sciences, and
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Srijak Bhatnagar
cMedical Microbiology and Immunology, University of California, Davis, CA 95616
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Jonathan A. Eisen
cMedical Microbiology and Immunology, University of California, Davis, CA 95616
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Venkatesan Sundaresan
Departments of aPlant Biology,bPlant Sciences, and
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  • For correspondence: sundar@ucdavis.edu
  1. Edited by Jeffery L. Dangl, Howard Hughes Medical Institute and The University of North Carolina at Chapel Hill, Chapel Hill, NC, and approved December 22, 2014 (received for review July 31, 2014)

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  • Fig. 1.
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    Fig. 1.

    Root-associated microbial communities are separable by rhizocompartment and soil type. (A) A representation of a rice root cross-section depicting the locations of the microbial communities sampled. (B) Within-sample diversity (α-diversity) measurements between rhizospheric compartments indicate a decreasing gradient in microbial diversity from the rhizosphere to the endosphere independent of soil type. Estimated species richness was calculated as eShannon_entropy. The horizontal bars within boxes represent median. The tops and bottoms of boxes represent 75th and 25th quartiles, respectively. The upper and lower whiskers extend 1.5× the interquartile range from the upper edge and lower edge of the box, respectively. All outliers are plotted as individual points. (C) PCoA using the WUF metric indicates that the largest separation between microbial communities is spatial proximity to the root (PCo 1) and the second largest source of variation is soil type (PCo 2). (D) Histograms of phyla abundances in each compartment and soil. B, bulk soil; E, endosphere; P, rhizoplane; S, rhizosphere; Sac, Sacramento.

  • Fig. 2.
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    Fig. 2.

    Rhizocompartments are enriched and depleted for certain OTUs. (A) Enrichment and depletion of the 27,147 OTUs included in the greenhouse experiment for each rhizospheric compartment compared with bulk soil controls as determined by differential abundance analysis. Each point represents an individual OTU, and the position along the y axis represents the abundance fold change compared with bulk soil. (B) Numbers of differentially enriched OTUs between each compartment compared with bulk soil. (C) Numbers of differentially depleted OTUs between each compartment.

  • Fig. 3.
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    Fig. 3.

    Host plant genotype significantly affects microbial communities in the rhizospheric compartments. (A) Ordination of CAP analysis using the WUF metric constrained to rice genotype. (B) Within-sample diversity measurements of rhizosphere samples of each cultivar grown in each soil. Estimated species richness was calculated as eShannon_entropy. The horizontal bars within boxes represent median. The tops and bottoms of boxes represent 75th and 25th quartiles, respectively. The upper and lower whiskers extend 1.5× the interquartile range from the upper edge and lower edge of the box, respectively. All outliers are plotted as individual points.

  • Fig. 4.
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    Fig. 4.

    Root-associated microbiomes from field-grown plants are separable by cultivation site, rhizospheric compartment, and cultivation practice. (A) Map depicting the locations of the field experiment collection sites across California’s Central Valley. Circles represent organic-cultivated sites whereas triangles represent ecofarm-cultivated sites. (Scale bar, 10 mi.) (B) PCoA using the WUF method colored to depict the various sample collection sites. (C) Same PCoA in B colored by rhizospheric compartment. (D) Same PCoA in B and C depicting second and third axes and colored by cultivation practice.

  • Fig. 5.
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    Fig. 5.

    OTU coabundance network reveals modules of OTUs associated with methane cycling. (A) Subset of the entire network corresponding to 11 modules with methane cycling potential. Each node represents one OTU and an edge is drawn between OTUs if they share a Pearson correlation of greater than or equal to 0.6. (B) Depiction of module 119 showing the relationship between methanogens, syntrophs, methanotrophs, and other methane cycling taxonomies. Each node represents one OTU and is labeled by the presumed function of that OTU’s taxonomy in methane cycling. An edge is drawn between two OTUs if they have a Pearson correlation of greater than or equal to 0.6. (C) Mean abundance profile for OTUs in module 119 across all rhizocompartments and field sites. The position along the x axis corresponds to a different field site. Error bars represent SE. The x and y axes represent no particular scale.

  • Fig. 6.
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    Fig. 6.

    Time-series analysis of root-associated microbial communities reveals distinct microbiome colonization patterns. (A) Ratios of microbial to organellar (plastidial and mitochondrial) 16S rRNA gene reads in the endosphere after transplantation into Davis soil. The 42-d time point corresponds to the earlier greenhouse experiment data (Fig. 1) subsetted to M104 in Davis soil. Mean percentages of the ratios are depicted with each bar. (B) PCoA of the time-series experiment and the greenhouse experiment subsetted to plants growing in Davis soil and colored by rhizospheric compartment. (C) The same PCoA as in B colored by collection day after transplantation into soil. (D) Average relative abundance for select phyla over the course of microbiome acquisition. (E) Average abundance profile of 53 out of the 92 core endosphere-enriched OTUs in each rhizospheric compartment. Error bars represent SE.

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Rice root-associated microbiomes
Joseph Edwards, Cameron Johnson, Christian Santos-Medellín, Eugene Lurie, Natraj Kumar Podishetty, Srijak Bhatnagar, Jonathan A. Eisen, Venkatesan Sundaresan
Proceedings of the National Academy of Sciences Feb 2015, 112 (8) E911-E920; DOI: 10.1073/pnas.1414592112

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Rice root-associated microbiomes
Joseph Edwards, Cameron Johnson, Christian Santos-Medellín, Eugene Lurie, Natraj Kumar Podishetty, Srijak Bhatnagar, Jonathan A. Eisen, Venkatesan Sundaresan
Proceedings of the National Academy of Sciences Feb 2015, 112 (8) E911-E920; DOI: 10.1073/pnas.1414592112
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