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      Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species

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          Summary

          • Desert plants are hypothesized to survive the environmental stress inherent to these regions in part thanks to symbioses with microorganisms, and yet these microbial species, the communities they form, and the forces that influence them are poorly understood.

          • Here we report the first comprehensive investigation of the microbial communities associated with species of Agave, which are native to semiarid and arid regions of Central and North America and are emerging as biofuel feedstocks. We examined prokaryotic and fungal communities in the rhizosphere, phyllosphere, leaf and root endosphere, as well as proximal and distal soil samples from cultivated and native agaves, through Illumina amplicon sequencing.

          • Phylogenetic profiling revealed that the composition of prokaryotic communities was primarily determined by the plant compartment, whereas the composition of fungal communities was mainly influenced by the biogeography of the host species. Cultivated A. tequilana exhibited lower levels of prokaryotic diversity compared with native agaves, although no differences in microbial diversity were found in the endosphere.

          • Agaves shared core prokaryotic and fungal taxa known to promote plant growth and confer tolerance to abiotic stress, which suggests common principles underpinning Agave–microbe interactions.

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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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            Feedstocks for lignocellulosic biofuels.

            In 2008, the world produced approximately 87 gigaliters of liquid biofuels, which is roughly equal to the volume of liquid fuel consumed by Germany that year. Essentially, all of this biofuel was produced from crops developed for food production, raising concerns about the net energy and greenhouse gas effects and potential competition between use of land for production of fuels, food, animal feed, fiber, and ecosystem services. The pending implementation of improved technologies to more effectively convert the nonedible parts of plants (lignocellulose) to liquid fuels opens diverse options to use biofuel feedstocks that reach beyond current crops and the land currently used for food and feed. However, there has been relatively little discussion of what types of plants may be useful as bioenergy crops.
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              A Drought Resistance-Promoting Microbiome Is Selected by Root System under Desert Farming

              Background Traditional agro-systems in arid areas are a bulwark for preserving soil stability and fertility, in the sight of “reverse desertification”. Nevertheless, the impact of desert farming practices on the diversity and abundance of the plant associated microbiome is poorly characterized, including its functional role in supporting plant development under drought stress. Methodology/Principal Findings We assessed the structure of the microbiome associated to the drought-sensitive pepper plant (Capsicum annuum L.) cultivated in a traditional Egyptian farm, focusing on microbe contribution to a crucial ecosystem service, i.e. plant growth under water deficit. The root system was dissected by sampling root/soil with a different degree of association to the plant: the endosphere, the rhizosphere and the root surrounding soil that were compared to the uncultivated soil. Bacterial community structure and diversity, determined by using Denaturing Gradient Gel Electrophoresis, differed according to the microhabitat, indicating a selective pressure determined by the plant activity. Similarly, culturable bacteria genera showed different distribution in the three root system fractions. Bacillus spp. (68% of the isolates) were mainly recovered from the endosphere, while rhizosphere and the root surrounding soil fractions were dominated by Klebsiella spp. (61% and 44% respectively). Most of the isolates (95%) presented in vitro multiple plant growth promoting (PGP) activities and stress resistance capabilities, but their distribution was different among the root system fractions analyzed, with enhanced abilities for Bacillus and the rhizobacteria strains. We show that the C. annuum rhizosphere under desert farming enriched populations of PGP bacteria capable of enhancing plant photosynthetic activity and biomass synthesis (up to 40%) under drought stress. Conclusions/Significance Crop cultivation provides critical ecosystem services in arid lands with the plant root system acting as a “resource island” able to attract and select microbial communities endowed with multiple PGP traits that sustain plant development under water limiting conditions.
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                Author and article information

                Journal
                New Phytol
                New Phytol
                10.1111/(ISSN)1469-8137
                NPH
                The New Phytologist
                John Wiley and Sons Inc. (Hoboken )
                0028-646X
                1469-8137
                January 2016
                15 October 2015
                : 209
                : 2 ( doiID: 10.1111/nph.2016.209.issue-2 )
                : 798-811
                Affiliations
                [ 1 ] Department of EnergyJoint Genome Institute Walnut Creek CA 94598USA
                [ 2 ] Genomics DivisionLawrence Berkeley National Laboratory Berkeley CA 94720USA
                [ 3 ] Plant Gene Expression CenterUSDA‐ARS Albany CA 94710USA
                [ 4 ] Departamento de Ingeniería GenéticaCentro de Investigación y de Estudios Avanzados Irapuato 36821Mexico
                [ 5 ] Department of BiologyOccidental College Los Angeles CA 90041USA
                [ 6 ] School of Natural SciencesUniversity of California Merced CA 95343USA
                Author notes
                [*] [* ] Authors for correspondence:

                Axel Visel

                Tel: +1 510 495 2301

                Email: avisel@ 123456lbl.gov

                Laila P. Partida‐Martinez

                Tel: +52 462 623 9658

                Email: laila.partida@ 123456ira.cinvestav.mx

                Susannah G. Tringe

                Tel: +1 925 296 5813

                Email: sgtringe@ 123456lbl.gov

                Author information
                http://orcid.org/0000-0001-8037-2856
                Article
                NPH13697 2015-20050
                10.1111/nph.13697
                5057366
                26467257
                f69a1456-5149-4e1e-a4ec-80931b621ace
                No claim to US Government works. New Phytologist © 2015 New Phytologist Trust

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 01 July 2015
                : 31 August 2015
                Page count
                Pages: 14
                Funding
                Funded by: JGI Community Science Program (CSP)
                Funded by: US Department of Energy Joint Genome Institute
                Funded by: DOE Office of Science User Facility
                Award ID: DE‐AC02‐05CH11231
                Funded by: Consejo Nacional de Ciencia y Tecnologia in Mexico (CONACyT)
                Award ID: CB‐2010‐01‐151007
                Award ID: INFR‐2012‐01‐197799
                Categories
                Full Paper
                Research
                Full Papers
                Custom metadata
                2.0
                nph13697
                January 2016
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.4 mode:remove_FC converted:12.10.2016

                Plant science & Botany
                agave,biogeography,cultivation,desert,itags,microbial diversity,plant microbiome,plant–microbe interactions

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