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      Legacy of land use history determines reprogramming of plant physiology by soil microbiome

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          Abstract

          Microorganisms associated with roots are thought to be part of the so-called extended plant phenotypes with roles in the acquisition of nutrients, production of growth hormones, and defense against diseases. Since the crops selectively enrich most rhizosphere microbes out of the bulk soil, we hypothesized that changes in the composition of bulk soil communities caused by agricultural management affect the extended plant phenotype. In the current study, we performed shotgun metagenome sequencing of the rhizosphere microbiome of the peanut ( Arachis hypogaea) and metatranscriptome analysis of the roots of peanut plants grown in the soil with different management histories, peanut monocropping and crop rotation. We found that the past planting record had a significant effect on the assembly of the microbial community in the peanut rhizosphere, indicating a soil memory effect. Monocropping resulted in a reduction of the rhizosphere microbial diversity, an enrichment of several rare species, and a reduced representation of traits related to plant performance, such as nutrients metabolism and phytohormone biosynthesis. Furthermore, peanut plants in monocropped soil exhibited a significant reduction in growth coinciding with a down-regulation of genes related to hormone production, mainly auxin and cytokinin, and up-regulation of genes related to the abscisic acid, salicylic acid, jasmonic acid, and ethylene pathways. These findings suggest that land use history affects crop rhizosphere microbiomes and plant physiology.

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          Most cited references 60

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          Indole-3-acetic acid in microbial and microorganism-plant signaling.

          Diverse bacterial species possess the ability to produce the auxin phytohormone indole-3-acetic acid (IAA). Different biosynthesis pathways have been identified and redundancy for IAA biosynthesis is widespread among plant-associated bacteria. Interactions between IAA-producing bacteria and plants lead to diverse outcomes on the plant side, varying from pathogenesis to phyto-stimulation. Reviewing the role of bacterial IAA in different microorganism-plant interactions highlights the fact that bacteria use this phytohormone to interact with plants as part of their colonization strategy, including phyto-stimulation and circumvention of basal plant defense mechanisms. Moreover, several recent reports indicate that IAA can also be a signaling molecule in bacteria and therefore can have a direct effect on bacterial physiology. This review discusses past and recent data, and emerging views on IAA, a well-known phytohormone, as a microbial metabolic and signaling molecule.
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            Rhizosphere microbiome assemblage is affected by plant development.

            There is a concerted understanding of the ability of root exudates to influence the structure of rhizosphere microbial communities. However, our knowledge of the connection between plant development, root exudation and microbiome assemblage is limited. Here, we analyzed the structure of the rhizospheric bacterial community associated with Arabidopsis at four time points corresponding to distinct stages of plant development: seedling, vegetative, bolting and flowering. Overall, there were no significant differences in bacterial community structure, but we observed that the microbial community at the seedling stage was distinct from the other developmental time points. At a closer level, phylum such as Acidobacteria, Actinobacteria, Bacteroidetes, Cyanobacteria and specific genera within those phyla followed distinct patterns associated with plant development and root exudation. These results suggested that the plant can select a subset of microbes at different stages of development, presumably for specific functions. Accordingly, metatranscriptomics analysis of the rhizosphere microbiome revealed that 81 unique transcripts were significantly (P<0.05) expressed at different stages of plant development. For instance, genes involved in streptomycin synthesis were significantly induced at bolting and flowering stages, presumably for disease suppression. We surmise that plants secrete blends of compounds and specific phytochemicals in the root exudates that are differentially produced at distinct stages of development to help orchestrate rhizosphere microbiome assemblage.
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              Manipulating the soil microbiome to increase soil health and plant fertility

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                Author and article information

                Contributors
                xxwang@issas.ac.cn , xgli@issas.ac.cn
                Journal
                ISME J
                ISME J
                The ISME Journal
                Nature Publishing Group UK (London )
                1751-7362
                1751-7370
                27 October 2018
                27 October 2018
                March 2019
                : 13
                : 3
                : 738-751
                Affiliations
                [1 ]ISNI 0000000119573309, GRID grid.9227.e, CAS Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, , Chinese Academy of Sciences, ; Nanjing, 210008 China
                [2 ]ISNI 0000 0001 1013 0288, GRID grid.418375.c, Department of Microbial Ecology, , Netherlands Institute of Ecology, NIOO-KNAW, ; Wageningen, 6708 PB The Netherlands
                [3 ]ISNI 0000000120346234, GRID grid.5477.1, Institute for Environmental Biology, Ecology & Biodiversity, , Utrecht University, ; Utrecht, 3584 CH The Netherlands
                [4 ]ISNI 0000 0001 0791 5666, GRID grid.4818.5, Soil Biology Group, , Wageningen University, ; Wageningen, 6708 PB The Netherlands
                [5 ]ISNI 0000000119573309, GRID grid.9227.e, Experimental Station of Red Soil, , Chinese Academy of Sciences, ; Yingtan, 335211 China
                Article
                300
                10.1038/s41396-018-0300-0
                6461838
                30368524
                af9ad79c-daf4-496e-95ca-497d7f272524
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits 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. 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/4.0/.

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                © International Society for Microbial Ecology 2019

                Microbiology & Virology

                microbial ecology, metagenomics

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