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      Disease-induced assemblage of a plant-beneficial bacterial consortium

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          Abstract

          Disease suppressive soils typically develop after a disease outbreak due to the subsequent assembly of protective microbiota in the rhizosphere. The role of the plant immune system in the assemblage of a protective rhizosphere microbiome is largely unknown. In this study, we demonstrate that Arabidopsis thaliana specifically promotes three bacterial species in the rhizosphere upon foliar defense activation by the downy mildew pathogen Hyaloperonospora arabidopsidis. The promoted bacteria were isolated and found to interact synergistically in biofilm formation in vitro. Although separately these bacteria did not affect the plant significantly, together they induced systemic resistance against downy mildew and promoted growth of the plant. Moreover, we show that the soil-mediated legacy of a primary population of downy mildew infected plants confers enhanced protection against this pathogen in a second population of plants growing in the same soil. Together our results indicate that plants can adjust their root microbiome upon pathogen infection and specifically recruit a group of disease resistance-inducing and growth-promoting beneficial microbes, therewith potentially maximizing the chance of survival of their offspring that will grow in the same soil.

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          Most cited references30

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          Induced systemic resistance by beneficial microbes.

          Beneficial microbes in the microbiome of plant roots improve plant health. Induced systemic resistance (ISR) emerged as an important mechanism by which selected plant growth-promoting bacteria and fungi in the rhizosphere prime the whole plant body for enhanced defense against a broad range of pathogens and insect herbivores. A wide variety of root-associated mutualists, including Pseudomonas, Bacillus, Trichoderma, and mycorrhiza species sensitize the plant immune system for enhanced defense without directly activating costly defenses. This review focuses on molecular processes at the interface between plant roots and ISR-eliciting mutualists, and on the progress in our understanding of ISR signaling and systemic defense priming. The central role of the root-specific transcription factor MYB72 in the onset of ISR and the role of phytohormones and defense regulatory proteins in the expression of ISR in aboveground plant parts are highlighted. Finally, the ecological function of ISR-inducing microbes in the root microbiome is discussed.
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            A5-miseq: an updated pipeline to assemble microbial genomes from Illumina MiSeq data.

            Open-source bacterial genome assembly remains inaccessible to many biologists because of its complexity. Few software solutions exist that are capable of automating all steps in the process of de novo genome assembly from Illumina data.
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              Roots shaping their microbiome: global hotspots for microbial activity.

              Land plants interact with microbes primarily at roots. Despite the importance of root microbial communities for health and nutrient uptake, the current understanding of the complex plant-microbe interactions in the rhizosphere is still in its infancy. Roots provide different microhabitats at the soil-root interface: rhizosphere soil, rhizoplane, and endorhizosphere. We discuss technical aspects of their differentiation that are relevant for the functional analysis of their different microbiomes, and we assess PCR (polymerase chain reaction)-based methods to analyze plant-associated bacterial communities. Development of novel primers will allow a less biased and more quantitative view of these global hotspots of microbial activity. Based on comparison of microbiome data for the different root-soil compartments and on knowledge of bacterial functions, a three-step enrichment model for shifts in community structure from bulk soil toward roots is presented. To unravel how plants shape their microbiome, a major research field is likely to be the coupling of reductionist and molecular ecological approaches, particularly for specific plant genotypes and mutants, to clarify causal relationships in complex root communities.
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                Author and article information

                Contributors
                +31302536860 , r.l.berendsen@uu.nl
                Journal
                ISME J
                ISME J
                The ISME Journal
                Nature Publishing Group UK (London )
                1751-7362
                1751-7370
                8 March 2018
                8 March 2018
                June 2018
                : 12
                : 6
                : 1496-1507
                Affiliations
                [1 ]ISNI 0000000120346234, GRID grid.5477.1, Plant-Microbe Interactions, Institute of Environmental Biology, , Utrecht University, ; Padualaan 8, 3584 CH Utrecht, The Netherlands
                [2 ]ISNI 0000 0000 9750 7019, GRID grid.27871.3b, Jiangsu Provincial Coordinated Research Center for Organic Solid Waste Utilization, , Nanjing Agricultural University, ; Nanjing, 210095 People’s Republic of China
                [3 ]ISNI 0000 0001 2069 7798, GRID grid.5342.0, Department of Plant Biotechnology and Bioinformatics, , Ghent University, ; Technologiepark 927, 9052 Ghent, Belgium
                [4 ]ISNI 0000000104788040, GRID grid.11486.3a, VIB Center for Plant Systems Biology, ; Technologiepark 927, 9052 Ghent, Belgium
                [5 ]ISNI 0000 0001 0674 042X, GRID grid.5254.6, Section of Microbiology, Department of Biology, , University of Copenhagen, ; Universitetsparken 15, 2100 København, Denmark
                Author information
                http://orcid.org/0000-0003-1870-632X
                http://orcid.org/0000-0002-5473-4646
                Article
                93
                10.1038/s41396-018-0093-1
                5956071
                29520025
                4e92f973-2a6d-40e9-8e74-551958e391f8
                © International Society for Microbial Ecology 2018

                Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License, which permits any non-commercial use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. If you remix, transform, or build upon this article or a part thereof, you must distribute your contributions under the same license as the original. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/4.0/.

                History
                : 22 June 2017
                : 3 January 2018
                : 10 January 2018
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                © International Society for Microbial Ecology 2018

                Microbiology & Virology
                Microbiology & Virology

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