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      Building the crops of tomorrow: advantages of symbiont-based approaches to improving abiotic stress tolerance

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          Abstract

          The exponential growth in world population is feeding a steadily increasing global need for arable farmland, a resource that is already in high demand. This trend has led to increased farming on subprime arid and semi-arid lands, where limited availability of water and a host of environmental stresses often severely reduce crop productivity. The conventional approach to mitigating the abiotic stresses associated with arid climes is to breed for stress-tolerant cultivars, a time and labor intensive venture that often neglects the complex ecological context of the soil environment in which the crop is grown. In recent years, studies have attempted to identify microbial symbionts capable of conferring the same stress-tolerance to their plant hosts, and new developments in genomic technologies have greatly facilitated such research. Here, we highlight many of the advantages of these symbiont-based approaches and argue in favor of the broader recognition of crop species as ecological niches for a diverse community of microorganisms that function in concert with their plant hosts and each other to thrive under fluctuating environmental conditions.

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          Most cited references46

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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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            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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              A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance.

              A mutualistic association between a fungal endophyte and a tropical panic grass allows both organisms to grow at high soil temperatures. We characterized a virus from this fungus that is involved in the mutualistic interaction. Fungal isolates cured of the virus are unable to confer heat tolerance, but heat tolerance is restored after the virus is reintroduced. The virus-infected fungus confers heat tolerance not only to its native monocot host but also to a eudicot host, which suggests that the underlying mechanism involves pathways conserved between these two groups of plants.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                09 May 2014
                06 June 2014
                2014
                : 5
                : 283
                Affiliations
                Joint Genome Institute, Walnut Creek CA, USA
                Author notes

                Edited by: Monica Medina, Pennsylvania State University, USA

                Reviewed by: Gabriele Berg, Graz University of Technology, Austria; Oded Yarden, The Hebrew University of Jerusalem, Israel

                *Correspondence: Susannah G. Tringe, Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598, USA e-mail: sgtringe@ 123456lbl.gov

                This article was submitted to Microbial Symbioses, a section of the journal Frontiers in Microbiology.

                Article
                10.3389/fmicb.2014.00283
                4047557
                24936202
                f67628da-eabf-4850-a05f-4009ad81ce18
                Copyright © 2014 Coleman-Derr and Tringe.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 11 April 2014
                : 22 May 2014
                Page count
                Figures: 1, Tables: 0, Equations: 0, References: 59, Pages: 6, Words: 0
                Categories
                Microbiology
                Perspective Article

                Microbiology & Virology
                symbiosis,abiotic stress,agriculture,plant growth promotion,plant–microbe interactions,drought

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