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      Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots

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          Abstract

          Root-associated microbes play a key role in plant performance and productivity, making them important players in agroecosystems. So far, very few studies have assessed the impact of different farming systems on the root microbiota and it is still unclear whether agricultural intensification influences the structure and complexity of microbial communities. We investigated the impact of conventional, no-till and organic farming on wheat root fungal communities using PacBio SMRT sequencing on samples collected from 60 farmlands in Switzerland. Organic farming harboured a much more complex fungal network with significantly higher connectivity than conventional and no-till farming systems. The abundance of keystone taxa was the highest under organic farming where agricultural intensification was the lowest. We also found a strong negative association (R 2=0.366; P<0.0001) between agricultural intensification and root fungal network connectivity. The occurrence of keystone taxa was best explained by soil phosphorus levels, bulk density, pH and mycorrhizal colonization. The majority of keystone taxa are known to form arbuscular mycorrhizal associations with plants and belong to the orders Glomerales, Paraglomerales, and Diversisporales. Supporting this, the abundance of mycorrhizal fungi in roots and soils was also significantly higher under organic farming. To our knowledge, this is the first study to report mycorrhizal keystone taxa for agroecosystems, and we demonstrate that agricultural intensification reduces network complexity and the abundance of keystone taxa in the root microbiome.

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          Most cited references64

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            Emergence of scaling in random networks

            Systems as diverse as genetic networks or the World Wide Web are best described as networks with complex topology. A common property of many large networks is that the vertex connectivities follow a scale-free power-law distribution. This feature was found to be a consequence of two generic mechanisms: (i) networks expand continuously by the addition of new vertices, and (ii) new vertices attach preferentially to sites that are already well connected. A model based on these two ingredients reproduces the observed stationary scale-free distributions, which indicates that the development of large networks is governed by robust self-organizing phenomena that go beyond the particulars of the individual systems.
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              Feed Your Friends: Do Plant Exudates Shape the Root Microbiome?

              Plant health in natural environments depends on interactions with complex and dynamic communities comprising macro- and microorganisms. While many studies have provided insights into the composition of rhizosphere microbiomes (rhizobiomes), little is known about whether plants shape their rhizobiomes. Here, we discuss physiological factors of plants that may govern plant-microbe interactions, focusing on root physiology and the role of root exudates. Given that only a few plant transport proteins are known to be involved in root metabolite export, we suggest novel families putatively involved in this process. Finally, building off of the features discussed in this review, and in analogy to well-known symbioses, we elaborate on a possible sequence of events governing rhizobiome assembly.
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                Author and article information

                Journal
                101301086
                ISME J
                ISME J
                The ISME journal
                1751-7362
                1751-7370
                25 February 2019
                08 March 2019
                July 2019
                08 September 2019
                : 13
                : 7
                : 1722-1736
                Affiliations
                [1 ]Agroscope, Department of Agroecology & Environment, Reckenholzstrasse 191, 8046 Zürich, Switzerland
                [2 ]Agroscope, Plant Production Systems, Route de Duillier 50, 1260 Nyon, Switzerland
                [3 ]Natural Resources Institute, University of Greenwich, United Kingdom
                [4 ]Research Institute of Organic Agriculture FiBL, 5070 Frick, Switzerland Switzerland
                [5 ]Justus-Liebig University Giessen, Organic Farming with focus on Sustainable Soil Use, Karl-Glöckner-Str. 21 C, 35394 Giessen, Germany
                [6 ]Swedish University of Agricultural Sciences, Department of Soil & Environment, Box 7014, 75007 Uppsala, Sweden
                [7 ]Research Institute of Organic Agriculture FiBL, Jordils 3, 1001 Lausanne, Switzerland
                [8 ]Department of Plant and Microbial Biology, University of Zürich, Zürich 8008, Switzerland
                Author notes
                Article
                EMS81878
                10.1038/s41396-019-0383-2
                6591126
                30850707
                23189544-f7ed-47de-8110-4f568427faea

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                Microbiology & Virology
                Microbiology & Virology

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