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      Assembly and ecological function of the root microbiome across angiosperm plant species

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          Abstract

          <p id="d7437981e250">Microbial communities living on and within plants and animals contribute to host function. How host evolution shapes associated microbial communities, and in turn, how these microbes affect the ecology of their hosts is relatively unknown. Here, we demonstrate that evolution occurring across plant species affects root microbial diversity and composition. Greater similarity in root microbiota among host plant species leads to reduced plant performance through negative soil feedbacks. Additionally, drought shifts the composition of root microbiomes, where changes in the relative abundance of specific bacterial taxa are associated with increased drought tolerance of plants. Our work highlights the potential role of host-associated microbial communities in mediating interactions between hosts and their biotic and abiotic environment. </p><p class="first" id="d7437981e253">Across plants and animals, host-associated microbial communities play fundamental roles in host nutrition, development, and immunity. The factors that shape host–microbiome interactions are poorly understood, yet essential for understanding the evolution and ecology of these symbioses. Plant roots assemble two distinct microbial compartments from surrounding soil: the rhizosphere (microbes surrounding roots) and the endosphere (microbes within roots). Root-associated microbes were key for the evolution of land plants and underlie fundamental ecosystem processes. However, it is largely unknown how plant evolution has shaped root microbial communities, and in turn, how these microbes affect plant ecology, such as the ability to mitigate biotic and abiotic stressors. Here we show that variation among 30 angiosperm species, which have diverged for up to 140 million years, affects root bacterial diversity and composition. Greater similarity in root microbiomes between hosts leads to negative effects on plant performance through soil feedback, with specific microbial taxa in the endosphere and rhizosphere potentially affecting competitive interactions among plant species. Drought also shifts the composition of root microbiomes, most notably by increasing the relative abundance of the Actinobacteria. However, this drought response varies across host plant species, and host-specific changes in the relative abundance of endosphere <i>Streptomyces</i> are associated with host drought tolerance. Our results emphasize the causes of variation in root microbiomes and their ecological importance for plant performance in response to biotic and abiotic stressors. </p>

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          Most cited references34

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          Gene networks involved in drought stress response and tolerance.

          Plants respond to survive under water-deficit conditions via a series of physiological, cellular, and molecular processes culminating in stress tolerance. Many drought-inducible genes with various functions have been identified by molecular and genomic analyses in Arabidopsis, rice, and other plants, including a number of transcription factors that regulate stress-inducible gene expression. The products of stress-inducible genes function both in the initial stress response and in establishing plant stress tolerance. In this short review, recent progress resulting from analysis of gene expression during the drought-stress response in plants as well as in elucidating the functions of genes implicated in the stress response and/or stress tolerance are summarized. A description is also provided of how various genes involved in stress tolerance were applied in genetic engineering of dehydration stress tolerance in transgenic Arabidopsis plants.
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            Rhizosphere bacteria help plants tolerate abiotic stress.

            Plant-growth-promoting rhizobacteria (PGPR) are associated with plant roots and augment plant productivity and immunity; however, recent work by several groups shows that PGPR also elicit so-called 'induced systemic tolerance' to salt and drought. As we discuss here, PGPR might also increase nutrient uptake from soils, thus reducing the need for fertilizers and preventing the accumulation of nitrates and phosphates in agricultural soils. A reduction in fertilizer use would lessen the effects of water contamination from fertilizer run-off and lead to savings for farmers.
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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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                Author and article information

                Journal
                Proceedings of the National Academy of Sciences
                Proc Natl Acad Sci USA
                Proceedings of the National Academy of Sciences
                0027-8424
                1091-6490
                February 06 2018
                February 06 2018
                : 115
                : 6
                : E1157-E1165
                Article
                10.1073/pnas.1717617115
                5819437
                29358405
                327a28f4-f878-4a04-8545-ceef03d7e5ba
                © 2018

                http://www.pnas.org/site/misc/userlicense.xhtml

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