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      Initial soil microbiome composition and functioning predetermine future plant health

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          Abstract

          Soil microbiome composition and functioning determine the outcome of plant-pathogen interactions under natural field conditions.

          Abstract

          Plant-pathogen interactions are shaped by multiple environmental factors, making it difficult to predict disease dynamics even in relatively simple agricultural monocultures. Here, we explored how variation in the initial soil microbiome predicts future disease outcomes at the level of individual plants. We found that the composition and functioning of the initial soil microbiome predetermined whether the plants survived or succumbed to disease. Surviving plant microbiomes were associated with specific rare taxa, highly pathogen-suppressing Pseudomonas and Bacillus bacteria, and high abundance of genes encoding antimicrobial compounds. Microbiome-mediated plant protection could subsequently be transferred to the next plant generation via soil transplantation. Together, our results suggest that small initial variation in soil microbiome composition and functioning can determine the outcomes of plant-pathogen interactions under natural field conditions.

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          Most cited references37

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          Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays.

          Here we describe a quantitative PCR-based approach to estimating the relative abundances of major taxonomic groups of bacteria and fungi in soil. Primers were thoroughly tested for specificity, and the method was applied to three distinct soils. The technique provides a rapid and robust index of microbial community structure.
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            Root microbiota drive direct integration of phosphate stress and immunity

            Plants live in biogeochemically diverse soils that harbor extraordinarily diverse microbiota. Plant organs associate intimately with a subset of these microbes; this community’s structure can be altered by soil nutrient content. Plant-associated microbes can compete with the plant and with each other for nutrients; they can also provide traits that increase plant productivity. It is unknown how the plant immune system coordinates microbial recognition with nutritional cues during microbiome assembly. We establish that a genetic network controlling phosphate stress response influences root microbiome community structure, even under non-stress phosphate conditions. We define a molecular mechanism regulating coordination between nutrition and defense in the presence of a synthetic bacterial community. We demonstrate that the master transcriptional regulators of phosphate stress response in Arabidopsis also directly repress defense, consistent with plant prioritization of nutritional stress over defense. Our work will impact efforts to define and deploy useful microbes to enhance plant performance.
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              Core microbiomes for sustainable agroecosystems

              In an era of ecosystem degradation and climate change, maximizing microbial functions in agroecosystems has become a prerequisite for the future of global agriculture. However, managing species-rich communities of plant-associated microbiomes remains a major challenge. Here, we propose interdisciplinary research strategies to optimize microbiome functions in agroecosystems. Informatics now allows us to identify members and characteristics of 'core microbiomes', which may be deployed to organize otherwise uncontrollable dynamics of resident microbiomes. Integration of microfluidics, robotics and machine learning provides novel ways to capitalize on core microbiomes for increasing resource-efficiency and stress-resistance of agroecosystems.
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                Author and article information

                Journal
                Sci Adv
                Sci Adv
                SciAdv
                advances
                Science Advances
                American Association for the Advancement of Science
                2375-2548
                September 2019
                25 September 2019
                : 5
                : 9
                : eaaw0759
                Affiliations
                [1 ]Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Weigang 1, Nanjing, 210095, P.R. China.
                [2 ]Jiangsu Key Laboratory for Eco-Agricultural Biotechnology around Hongze Lake, Jiangsu Collaborative Innovation Center of Regional Modern Agriculture & Environmental Protection, Huaiyin Normal University, Huaian, 223300, P.R. China.
                [3 ]Department of Biology, University of York, York, UK.
                [4 ]Institute for Environmental Biology, Ecology and Biodiversity, Utrecht University, Utrecht, Netherlands.
                Author notes
                [*]

                These authors contributed equally to this work.

                []Corresponding author. Email: shenqirong@ 123456njau.edu.cn (Q.S.); ycxu@ 123456njau.edu.cn (Y.X.)
                Author information
                http://orcid.org/0000-0002-7967-4897
                http://orcid.org/0000-0002-3011-3685
                http://orcid.org/0000-0002-1592-157X
                http://orcid.org/0000-0002-4939-2506
                Article
                aaw0759
                10.1126/sciadv.aaw0759
                6760924
                31579818
                b36542de-7ce0-45b9-a9cc-5f2ee6447989
                Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

                History
                : 15 November 2018
                : 27 August 2019
                Funding
                Funded by: doi http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31801952, 41471213, BK20181068, BK20170085
                Funded by: doi http://dx.doi.org/10.13039/501100013290, National Key Research and Development Program of China Stem Cell and Translational Research;
                Award ID: 2018YFD1000800
                Funded by: National Key Basic Research Program of China;
                Award ID: 2015CB150503
                Categories
                Research Article
                Research Articles
                SciAdv r-articles
                Plant Sciences
                Custom metadata
                Sam Ardiente

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