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      Research priorities for harnessing plant microbiomes in sustainable agriculture

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          Abstract

          Feeding a growing world population amidst climate change requires optimizing the reliability, resource use, and environmental impacts of food production. One way to assist in achieving these goals is to integrate beneficial plant microbiomes—i.e., those enhancing plant growth, nutrient use efficiency, abiotic stress tolerance, and disease resistance—into agricultural production. This integration will require a large-scale effort among academic researchers, industry researchers, and farmers to understand and manage plant-microbiome interactions in the context of modern agricultural systems. Here, we identify priorities for research in this area: (1) develop model host–microbiome systems for crop plants and non-crop plants with associated microbial culture collections and reference genomes, (2) define core microbiomes and metagenomes in these model systems, (3) elucidate the rules of synthetic, functionally programmable microbiome assembly, (4) determine functional mechanisms of plant-microbiome interactions, and (5) characterize and refine plant genotype-by-environment-by-microbiome-by-management interactions. Meeting these goals should accelerate our ability to design and implement effective agricultural microbiome manipulations and management strategies, which, in turn, will pay dividends for both the consumers and producers of the world food supply.

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          Most cited references72

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          Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems.

          The cycles of the key nutrient elements nitrogen (N) and phosphorus (P) have been massively altered by anthropogenic activities. Thus, it is essential to understand how photosynthetic production across diverse ecosystems is, or is not, limited by N and P. Via a large-scale meta-analysis of experimental enrichments, we show that P limitation is equally strong across these major habitats and that N and P limitation are equivalent within both terrestrial and freshwater systems. Furthermore, simultaneous N and P enrichment produces strongly positive synergistic responses in all three environments. Thus, contrary to some prevailing paradigms, freshwater, marine and terrestrial ecosystems are surprisingly similar in terms of N and P limitation.
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            Patterns and processes of microbial community assembly.

            Recent research has expanded our understanding of microbial community assembly. However, the field of community ecology is inaccessible to many microbial ecologists because of inconsistent and often confusing terminology as well as unnecessarily polarizing debates. Thus, we review recent literature on microbial community assembly, using the framework of Vellend (Q. Rev. Biol. 85:183-206, 2010) in an effort to synthesize and unify these contributions. We begin by discussing patterns in microbial biogeography and then describe four basic processes (diversification, dispersal, selection, and drift) that contribute to community assembly. We also discuss different combinations of these processes and where and when they may be most important for shaping microbial communities. The spatial and temporal scales of microbial community assembly are also discussed in relation to assembly processes. Throughout this review paper, we highlight differences between microbes and macroorganisms and generate hypotheses describing how these differences may be important for community assembly. We end by discussing the implications of microbial assembly processes for ecosystem function and biodiversity.
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              Stress tolerance in plants via habitat-adapted symbiosis.

              We demonstrate that native grass species from coastal and geothermal habitats require symbiotic fungal endophytes for salt and heat tolerance, respectively. Symbiotically conferred stress tolerance is a habitat-specific phenomenon with geothermal endophytes conferring heat but not salt tolerance, and coastal endophytes conferring salt but not heat tolerance. The same fungal species isolated from plants in habitats devoid of salt or heat stress did not confer these stress tolerances. Moreover, fungal endophytes from agricultural crops conferred disease resistance and not salt or heat tolerance. We define habitat-specific, symbiotically-conferred stress tolerance as habitat-adapted symbiosis and hypothesize that it is responsible for the establishment of plants in high-stress habitats. The agricultural, coastal and geothermal plant endophytes also colonized tomato (a model eudicot) and conferred disease, salt and heat tolerance, respectively. In addition, the coastal plant endophyte colonized rice (a model monocot) and conferred salt tolerance. These endophytes have a broad host range encompassing both monocots and eudicots. Interestingly, the endophytes also conferred drought tolerance to plants regardless of the habitat of origin. Abiotic stress tolerance correlated either with a decrease in water consumption or reactive oxygen sensitivity/generation but not to increased osmolyte production. The ability of fungal endophytes to confer stress tolerance to plants may provide a novel strategy for mitigating the impacts of global climate change on agricultural and native plant communities.
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                Author and article information

                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                28 March 2017
                March 2017
                28 March 2017
                : 15
                : 3
                : e2001793
                Affiliations
                [1 ]Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America
                [2 ]Department of Natural Resources and Environmental Sciences, University of Illinois at Urbana Champaign, Urbana, Illinois, United States of America
                [3 ]Department of Plant Pathology, North Carolina State University, Raleigh, North Carolina, United States of America
                [4 ]Department of Plant Biology, Michigan State University, East Lansing, Michigan, United States of America
                [5 ]Program in Ecology, Evolutionary Biology and Behavior, Michigan State University, East Lansing, Michigan, United States of America
                [6 ]MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, Michigan, United States of America
                [7 ]The James Hutton Institute, Invergowrie, Dundee, Scotland
                [8 ]College of Natural Sciences and Mathematics, University of West Alabama, Livingston, Alabama, United States of America
                [9 ]Genome Center, University of California, Davis, California, United States of America
                [10 ]Bioagricultural Sciences and Pest Management, Colorado State University, Ft Collins, Colorado, United States of America
                [11 ]Howard Hughes Medical Institute, Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-2837-9820
                Article
                pbio.2001793
                10.1371/journal.pbio.2001793
                5370116
                28350798
                a5678f2a-4488-408f-b974-392a794a4372
                © 2017 Busby et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Page count
                Figures: 2, Tables: 0, Pages: 14
                Funding
                National Science Foundation www.nsf.org (grant number 1519383).Received by PEB and CS. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. National Science Foundation www.nsf.org (grant number 1314095).Received by PEB. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Perspective
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbiome
                Biology and Life Sciences
                Genetics
                Genomics
                Microbial Genomics
                Microbiome
                Biology and Life Sciences
                Microbiology
                Microbial Genomics
                Microbiome
                Biology and Life Sciences
                Ecology
                Microbial Ecology
                Ecology and Environmental Sciences
                Ecology
                Microbial Ecology
                Biology and Life Sciences
                Microbiology
                Microbial Ecology
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogenesis
                Host-Pathogen Interactions
                Biology and Life Sciences
                Ecology
                Community Ecology
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Biology and Life Sciences
                Agriculture
                People and Places
                Population Groupings
                Professions
                Agricultural Workers
                Biology and Life Sciences
                Organisms
                Plants
                Flowering Plants
                Biology and Life Sciences
                Ecology
                Plant Ecology
                Plant-Microbial Interactions
                Ecology and Environmental Sciences
                Ecology
                Plant Ecology
                Plant-Microbial Interactions
                Biology and Life Sciences
                Plant Science
                Plant Ecology
                Plant-Microbial Interactions

                Life sciences
                Life sciences

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