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      Symbiotic Root-Endophytic Soil Microbes Improve Crop Productivity and Provide Environmental Benefits

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      Scientifica
      Hindawi

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          Abstract

          Plants should not be regarded as entities unto themselves, but as the visible part of plant-microbe complexes which are best understood as “holobiomes.” Some microorganisms when given the opportunity to inhabit plant roots become root symbionts. Such root colonization by symbiotic microbes can raise crop yields by promoting the growth of both shoots and roots, by enhancing uptake, fixation, and/or more efficient use of nutrients, by improving plants' resistance to pests, diseases, and abiotic stresses that include drought, salt, and other environmental conditions, and by enhancing plants' capacity for photosynthesis. We refer plant-microbe associations with these capabilities that have been purposefully established as enhanced plant holobiomes (EPHs). Here, we consider four groups of phylogenetically distinct and distant symbiotic endophytes: (1) Rhizobiaceae bacteria; (2) plant-obligate arbuscular mycorrhizal fungi (AMF); (3) selected endophytic strains of fungi in the genus Trichoderma; and (4) fungi in the Sebicales order, specifically Piriformospora indica. Although these exhibit quite different “lifestyles” when inhabiting plants, all induce beneficial systemic changes in plants' gene expression that are surprisingly similar. For example, all induce gene expression that produces proteins which detoxify reactive oxygen species (ROS). ROS are increased by environmental stresses on plants or by overexcitation of photosynthetic pigments. Gene overexpression results in a cellular environment where ROS levels are controlled and made more compatible with plants' metabolic processes. EPHs also frequently exhibit increased rates of photosynthesis that contribute to greater plant growth and other capabilities. Soil organic matter (SOM) is augmented when plant root growth is increased and roots remain in the soil. The combination of enhanced photosynthesis, increasing sequestration of CO 2 from the air, and elevation of SOM removes C from the atmosphere and stores it in the soil. Reductions in global greenhouse gas levels can be accelerated by incentives for carbon farming and carbon cap-and-trade programs that reward such climate-friendly agriculture. The development and spread of EPHs as part of such initiatives has potential both to enhance farm productivity and incomes and to decelerate global warming.

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          Induced systemic resistance by beneficial microbes.

          Beneficial microbes in the microbiome of plant roots improve plant health. Induced systemic resistance (ISR) emerged as an important mechanism by which selected plant growth-promoting bacteria and fungi in the rhizosphere prime the whole plant body for enhanced defense against a broad range of pathogens and insect herbivores. A wide variety of root-associated mutualists, including Pseudomonas, Bacillus, Trichoderma, and mycorrhiza species sensitize the plant immune system for enhanced defense without directly activating costly defenses. This review focuses on molecular processes at the interface between plant roots and ISR-eliciting mutualists, and on the progress in our understanding of ISR signaling and systemic defense priming. The central role of the root-specific transcription factor MYB72 in the onset of ISR and the role of phytohormones and defense regulatory proteins in the expression of ISR in aboveground plant parts are highlighted. Finally, the ecological function of ISR-inducing microbes in the root microbiome is discussed.
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            Meeting the global food demand of the future by engineering crop photosynthesis and yield potential.

            Increase in demand for our primary foodstuffs is outstripping increase in yields, an expanding gap that indicates large potential food shortages by mid-century. This comes at a time when yield improvements are slowing or stagnating as the approaches of the Green Revolution reach their biological limits. Photosynthesis, which has been improved little in crops and falls far short of its biological limit, emerges as the key remaining route to increase the genetic yield potential of our major crops. Thus, there is a timely need to accelerate our understanding of the photosynthetic process in crops to allow informed and guided improvements via in-silico-assisted genetic engineering. Potential and emerging approaches to improving crop photosynthetic efficiency are discussed, and the new tools needed to realize these changes are presented.
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              Redesigning photosynthesis to sustainably meet global food and bioenergy demand.

              The world's crop productivity is stagnating whereas population growth, rising affluence, and mandates for biofuels put increasing demands on agriculture. Meanwhile, demand for increasing cropland competes with equally crucial global sustainability and environmental protection needs. Addressing this looming agricultural crisis will be one of our greatest scientific challenges in the coming decades, and success will require substantial improvements at many levels. We assert that increasing the efficiency and productivity of photosynthesis in crop plants will be essential if this grand challenge is to be met. Here, we explore an array of prospective redesigns of plant systems at various scales, all aimed at increasing crop yields through improved photosynthetic efficiency and performance. Prospects range from straightforward alterations, already supported by preliminary evidence of feasibility, to substantial redesigns that are currently only conceptual, but that may be enabled by new developments in synthetic biology. Although some proposed redesigns are certain to face obstacles that will require alternate routes, the efforts should lead to new discoveries and technical advances with important impacts on the global problem of crop productivity and bioenergy production.
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                Author and article information

                Contributors
                Journal
                Scientifica (Cairo)
                Scientifica (Cairo)
                SCIENTIFICA
                Scientifica
                Hindawi
                2090-908X
                2019
                2 April 2019
                : 2019
                : 9106395
                Affiliations
                Cornell University, Ithaca, NY, USA
                Author notes

                Academic Editor: Luca Sebastiani

                Author information
                http://orcid.org/0000-0001-8154-5659
                Article
                10.1155/2019/9106395
                6466867
                31065398
                3d2b8243-c0ed-4cf1-8f3a-460b6952b23c
                Copyright © 2019 Gary E. Harman and Norman Uphoff.

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

                History
                : 10 December 2018
                : 5 February 2019
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