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      Plant root-microbe communication in shaping root microbiomes

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          Abstract

          A growing body of research is highlighting the impacts root-associated microbial communities can have on plant health and development. These impacts can include changes in yield quantity and quality, timing of key developmental stages and tolerance of biotic and abiotic stresses. With such a range of effects it is clear that understanding the factors that contribute to a plant-beneficial root microbiome may prove advantageous. Increasing demands for food by a growing human population increases the importance and urgency of understanding how microbiomes may be exploited to increase crop yields and reduce losses caused by disease. In addition, climate change effects may require novel approaches to overcoming abiotic stresses such as drought and salinity as well as new emerging diseases. This review discusses current knowledge on the formation and maintenance of root-associated microbial communities and plant–microbe interactions with a particular emphasis on the effect of microbe–microbe interactions on the shape of microbial communities at the root surface. Further, we discuss the potential for root microbiome modification to benefit agriculture and food production.

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          Most cited references110

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          Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi.

          Arbuscular mycorrhizal (AM) fungi form mutualistic, symbiotic associations with the roots of more than 80% of land plants. The fungi are incapable of completing their life cycle in the absence of a host root. Their spores can germinate and grow in the absence of a host, but their hyphal growth is very limited. Little is known about the molecular mechanisms that govern signalling and recognition between AM fungi and their host plants. In one of the first stages of host recognition, the hyphae of AM fungi show extensive branching in the vicinity of host roots before formation of the appressorium, the structure used to penetrate the plant root. Host roots are known to release signalling molecules that trigger hyphal branching, but these branching factors have not been isolated. Here we have isolated a branching factor from the root exudates of Lotus japonicus and used spectroscopic analysis and chemical synthesis to identify it as a strigolactone, 5-deoxy-strigol. Strigolactones are a group of sesquiterpene lactones, previously isolated as seed-germination stimulants for the parasitic weeds Striga and Orobanche. The natural strigolactones 5-deoxy-strigol, sorgolactone and strigol, and a synthetic analogue, GR24, induced extensive hyphal branching in germinating spores of the AM fungus Gigaspora margarita at very low concentrations.
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            Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants.

            Plants associate with a wide range of microorganisms, with both detrimental and beneficial outcomes. Central to plant survival is the ability to recognize invading microorganisms and either limit their intrusion, in the case of pathogens, or promote the association, in the case of symbionts. To aid in this recognition process, elaborate communication and counter-communication systems have been established that determine the degree of ingress of the microorganism into the host plant. In this Review, I describe the common signalling processes used by plants during mutualistic interactions with microorganisms as diverse as arbuscular mycorrhizal fungi and rhizobial bacteria.
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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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                Author and article information

                Contributors
                +44(0) 24 765 75244 , P.Schafer@warwick.ac.uk
                Journal
                Plant Mol Biol
                Plant Mol. Biol
                Plant Molecular Biology
                Springer Netherlands (Dordrecht )
                0167-4412
                1573-5028
                4 January 2016
                4 January 2016
                2016
                : 90
                : 575-587
                Affiliations
                [ ]School of Life Sciences, University of Warwick, Coventry, CV4 7AL UK
                [ ]Warwick Integrative Synthetic Biology Centre, University of Warwick, Coventry, CV4 7AL UK
                Article
                417
                10.1007/s11103-015-0417-8
                4819777
                26729479
                6ef4d3b1-d509-42f7-aecb-81f46d532682
                © The Author(s) 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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.

                History
                : 18 May 2015
                : 1 December 2015
                Funding
                Funded by: BBSRC/EPSRC
                Award ID: BB/M017982/1
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000270, Natural Environment Research Council;
                Categories
                Article
                Custom metadata
                © Springer Science+Business Media Dordrecht 2016

                Plant science & Botany
                rhizosphere,microbiome,microbial communication,plant root,soil
                Plant science & Botany
                rhizosphere, microbiome, microbial communication, plant root, soil

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