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      Burkholderia ambifaria and B. caribensis Promote Growth and Increase Yield in Grain Amaranth ( Amaranthus cruentus and A. hypochondriacus) by Improving Plant Nitrogen Uptake

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          Abstract

          Grain amaranth is an emerging crop that produces seeds having high quality protein with balanced amino-acid content. However, production is restricted by agronomic limitations that result in yields that are lower than those normally produced by cereals. In this work, the use of five different rhizobacteria were explored as a strategy to promote growth and yields in Amaranthus hypochondriacus cv. Nutrisol and A. cruentus cv. Candil, two commercially important grain amaranth cultivars. The plants were grown in a rich substrate, high in organic matter, nitrogen (N), and phosphorus (P) and under greenhouse conditions. Burkholderia ambifaria Mex-5 and B. caribensis XV proved to be the most efficient strains and significantly promoted growth in both grain amaranth species tested. Increased grain yield and harvest index occurred in combination with chemical fertilization when tested in A. cruentus. Growth-promotion and improved yields correlated with increased N content in all tissues examined. Positive effects on growth also occurred in A. cruentus plants grown in a poor soil, even after N and P fertilization. No correlation between non-structural carbohydrate levels in roots of inoculated plants and growth promotion was observed. Conversely, gene expression assays performed at 3-, 5- and 7-weeks after seed inoculation in plants inoculated with B. caribensis XV identified a tissue-specific induction of several genes involved in photosynthesis, sugar- and N- metabolism and transport. It is concluded that strains of Burkholderia effectively promote growth and increase seed yields in grain amaranth. Growth promotion was particularly noticeable in plants grown in an infertile soil but also occurred in a well fertilized rich substrate. The positive effects observed may be attributed to a bio-fertilization effect that led to increased N levels in roots and shoots. The latter effect correlated with the differential induction of several genes involved in carbon and N metabolism and transport.

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          Most cited references27

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          Plant nitrogen assimilation and use efficiency.

          Crop productivity relies heavily on nitrogen (N) fertilization. Production and application of N fertilizers consume huge amounts of energy, and excess is detrimental to the environment; therefore, increasing plant N use efficiency (NUE) is essential for the development of sustainable agriculture. Plant NUE is inherently complex, as each step-including N uptake, translocation, assimilation, and remobilization-is governed by multiple interacting genetic and environmental factors. The limiting factors in plant metabolism for maximizing NUE are different at high and low N supplies, indicating great potential for improving the NUE of current cultivars, which were bred in well-fertilized soil. Decreasing environmental losses and increasing the productivity of crop-acquired N requires the coordination of carbohydrate and N metabolism to give high yields. Increasing both the grain and N harvest index to drive N acquisition and utilization are important approaches for breeding future high-NUE cultivars.
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            Sugar transporters for intercellular exchange and nutrition of pathogens.

            Sugar efflux transporters are essential for the maintenance of animal blood glucose levels, plant nectar production, and plant seed and pollen development. Despite broad biological importance, the identity of sugar efflux transporters has remained elusive. Using optical glucose sensors, we identified a new class of sugar transporters, named SWEETs, and show that at least six out of seventeen Arabidopsis, two out of over twenty rice and two out of seven homologues in Caenorhabditis elegans, and the single copy human protein, mediate glucose transport. Arabidopsis SWEET8 is essential for pollen viability, and the rice homologues SWEET11 and SWEET14 are specifically exploited by bacterial pathogens for virulence by means of direct binding of a bacterial effector to the SWEET promoter. Bacterial symbionts and fungal and bacterial pathogens induce the expression of different SWEET genes, indicating that the sugar efflux function of SWEET transporters is probably targeted by pathogens and symbionts for nutritional gain. The metazoan homologues may be involved in sugar efflux from intestinal, liver, epididymis and mammary cells.
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              Applications of free living plant growth-promoting rhizobacteria.

              Free-living plant growth-promoting rhizobacteria (PGPR) can be used in a variety of ways when plant growth enhancements are required. The most intensively researched use of PGPR has been in agriculture and horticulture. Several PGPR formulations are currently available as commercial products for agricultural production. Recently developing areas of PGPR usage include forest regeneration and phytoremediation of contaminated soils. As the mechanisms of plant growth promotion by these bacteria are unravelled, the possibility of more efficient plant-bacteria pairings for novel and practical uses will follow. The progress to date in using PGPR in a variety of applications with different plants is summarized and discussed here.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                12 February 2014
                : 9
                : 2
                : e88094
                Affiliations
                [1 ]Centro de Investigación y de Estudios Avanzados-Unidad Irapuato, Irapuato, Guanajuato, México
                [2 ]Departamento de Ciencias del Agua y del Medio Ambiente, Instituto Tecnológico de Sonora, Ciudad Obregón, Sonora, México
                University of Illinois at Chicago College of Medicine, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: JPDF FIPC. Performed the experiments: FIPC NAMG. Analyzed the data: JPDF FIPC SSV JJPC. Contributed reagents/materials/analysis tools: SSV JJPC. Wrote the paper: JPDF FIPC.

                Article
                PONE-D-13-47986
                10.1371/journal.pone.0088094
                3922803
                24533068
                bf719b91-9270-474c-9c39-04cff7d4f4cd
                Copyright @ 2014

                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
                : 14 November 2013
                : 6 January 2014
                Page count
                Pages: 14
                Funding
                This work was largely supported financially by the European Commission 6th Framework Programme, AMARANTH: FUTURE-FOOD, Contract No. 032263. Financial support was provided by México Tierra de Amaranto A. C. and The Deborah Presser-Velder Foundation. FIPC and SSV were supported by postgraduate scholarships (codes 10506 and 10512, respectively) granted by The National Council for Science and Technology (CONACyT, México). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Agriculture
                Agricultural Biotechnology
                Agricultural Production
                Crops
                Cereals
                Sustainable Agriculture
                Biology
                Biochemistry
                Metabolism
                Nitrogen Metabolism
                Ecology
                Plant Ecology
                Plant-Environment Interactions
                Genomics
                Microbiology
                Molecular Cell Biology
                Gene Expression
                Plant Science
                Agronomy
                Plant Biochemistry
                Plant Growth and Development

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