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      Ecophylogeny of the endospheric root fungal microbiome of co-occurring Agrostis stolonifera

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          Abstract

          Background

          Within the root endosphere, fungi are known to be important for plant nutrition and resistance to stresses. However, description and understanding of the rules governing community assembly in the fungal fraction of the plant microbiome remains scarce.

          Methods

          We used an innovative DNA- and RNA-based analysis of co-extracted nucleic acids to reveal the complexity of the fungal community colonizing the roots of an Agrostis stolonifera population. The normalized RNA/DNA ratio, designated the ‘mean expression ratio’, was used as a functional trait proxy. The link between this trait and phylogenetic relatedness was measured using the Blomberg’s K statistic.

          Results

          Fungal communities were highly diverse. Only ∼1.5% of the 635 OTUs detected were shared by all individuals, however these accounted for 33% of the sequence number. The endophytic fungal communities in plant roots exhibit phylogenetic clustering that can be explained by a plant host effect acting as environmental filter. The ‘ mean expression ratio’ displayed significant but divergent phylogenetic signals between fungal phyla.

          Discussion

          These results suggest that environmental filtering by the host plant favours the co-existence of related and similar OTUs within the Basidiomycota community assembly, whereas the Ascomycota and Glomeromycota communities seem to be impacted by competitive interactions which promote the co-existence of phylogenetically related but ecologically dissimilar OTUs.

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          Most cited references42

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          R: A language and environment for statistical computing

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            Testing for phylogenetic signal in comparative data: behavioral traits are more labile.

            The primary rationale for the use of phylogenetically based statistical methods is that phylogenetic signal, the tendency for related species to resemble each other, is ubiquitous. Whether this assertion is true for a given trait in a given lineage is an empirical question, but general tools for detecting and quantifying phylogenetic signal are inadequately developed. We present new methods for continuous-valued characters that can be implemented with either phylogenetically independent contrasts or generalized least-squares models. First, a simple randomization procedure allows one to test the null hypothesis of no pattern of similarity among relatives. The test demonstrates correct Type I error rate at a nominal alpha = 0.05 and good power (0.8) for simulated datasets with 20 or more species. Second, we derive a descriptive statistic, K, which allows valid comparisons of the amount of phylogenetic signal across traits and trees. Third, we provide two biologically motivated branch-length transformations, one based on the Ornstein-Uhlenbeck (OU) model of stabilizing selection, the other based on a new model in which character evolution can accelerate or decelerate (ACDC) in rate (e.g., as may occur during or after an adaptive radiation). Maximum likelihood estimation of the OU (d) and ACDC (g) parameters can serve as tests for phylogenetic signal because an estimate of d or g near zero implies that a phylogeny with little hierarchical structure (a star) offers a good fit to the data. Transformations that improve the fit of a tree to comparative data will increase power to detect phylogenetic signal and may also be preferable for further comparative analyses, such as of correlated character evolution. Application of the methods to data from the literature revealed that, for trees with 20 or more species, 92% of traits exhibited significant phylogenetic signal (randomization test), including behavioral and ecological ones that are thought to be relatively evolutionarily malleable (e.g., highly adaptive) and/or subject to relatively strong environmental (nongenetic) effects or high levels of measurement error. Irrespective of sample size, most traits (but not body size, on average) showed less signal than expected given the topology, branch lengths, and a Brownian motion model of evolution (i.e., K was less than one), which may be attributed to adaptation and/or measurement error in the broad sense (including errors in estimates of phenotypes, branch lengths, and topology). Analysis of variance of log K for all 121 traits (from 35 trees) indicated that behavioral traits exhibit lower signal than body size, morphological, life-history, or physiological traits. In addition, physiological traits (corrected for body size) showed less signal than did body size itself. For trees with 20 or more species, the estimated OU (25% of traits) and/or ACDC (40%) transformation parameter differed significantly from both zero and unity, indicating that a hierarchical tree with less (or occasionally more) structure than the original better fit the data and so could be preferred for comparative analyses.
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              Vive la différence: plant functional diversity matters to ecosystem processes

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                Author and article information

                Contributors
                Journal
                PeerJ
                PeerJ
                peerj
                peerj
                PeerJ
                PeerJ Inc. (San Francisco, USA )
                2167-8359
                8 June 2017
                2017
                : 5
                : e3454
                Affiliations
                [1 ]CNRS, UMR6553 Ecobio, Université de Rennes 1 , Rennes, France
                [2 ]Department of Biology, Stanford University , Stanford, CA, United States of America
                [3 ]CNRS, UMS3343 OSUR, Université de Rennes 1 , Rennes, France
                Article
                3454
                10.7717/peerj.3454
                5466812
                28607843
                85e38353-f86f-4c31-afb4-5cb98d21266d
                ©2017 Lê Van et al.

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

                History
                : 10 October 2016
                : 20 May 2017
                Funding
                Funded by: ‘l’Agence Nationale de la Recherche’
                Award ID: ANR-10-STRA-0002
                This work was supported by a grant from ‘l’Agence Nationale de la Recherche’ (ANR-10-STRA-0002). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Biodiversity
                Ecology
                Molecular Biology
                Mycology
                Plant Science

                agrostis stolonifera,ecophylogeny,phylogenetic signal,mean expression ratio,ssu rrna amplicons,root fungal microbiome,phylogenetic structure,plant microbiota

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