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      Drought-Tolerance of Wheat Improved by Rhizosphere Bacteria from Harsh Environments: Enhanced Biomass Production and Reduced Emissions of Stress Volatiles

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          Abstract

          Water is the key resource limiting world agricultural production. Although an impressive number of research reports have been published on plant drought tolerance enhancement via genetic modifications during the last few years, progress has been slower than expected. We suggest a feasible alternative strategy by application of rhizospheric bacteria coevolved with plant roots in harsh environments over millions of years, and harboring adaptive traits improving plant fitness under biotic and abiotic stresses. We show the effect of bacterial priming on wheat drought stress tolerance enhancement, resulting in up to 78% greater plant biomass and five-fold higher survivorship under severe drought. We monitored emissions of seven stress-related volatiles from bacterially-primed drought-stressed wheat seedlings, and demonstrated that three of these volatiles are likely promising candidates for a rapid non-invasive technique to assess crop drought stress and its mitigation in early phases of stress development. We conclude that gauging stress by elicited volatiles provides an effectual platform for rapid screening of potent bacterial strains and that priming with isolates of rhizospheric bacteria from harsh environments is a promising, novel way to improve plant water use efficiency. These new advancements importantly contribute towards solving food security issues in changing climates.

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          Most cited references30

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          Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance.

          Abiotic stresses, such as drought, salinity, extreme temperatures, chemical toxicity and oxidative stress are serious threats to agriculture and the natural status of the environment. Increased salinization of arable land is expected to have devastating global effects, resulting in 30% land loss within the next 25 years, and up to 50% by the year 2050. Therefore, breeding for drought and salinity stress tolerance in crop plants (for food supply) and in forest trees (a central component of the global ecosystem) should be given high research priority in plant biotechnology programs. Molecular control mechanisms for abiotic stress tolerance are based on the activation and regulation of specific stress-related genes. These genes are involved in the whole sequence of stress responses, such as signaling, transcriptional control, protection of membranes and proteins, and free-radical and toxic-compound scavenging. Recently, research into the molecular mechanisms of stress responses has started to bear fruit and, in parallel, genetic modification of stress tolerance has also shown promising results that may ultimately apply to agriculturally and ecologically important plants. The present review summarizes the recent advances in elucidating stress-response mechanisms and their biotechnological applications. Emphasis is placed on transgenic plants that have been engineered based on different stress-response mechanisms. The review examines the following aspects: regulatory controls, metabolite engineering, ion transport, antioxidants and detoxification, late embryogenesis abundant (LEA) and heat-shock proteins.
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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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              Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited.

              J Flexas (2002)
              There is a long-standing controversy as to whether drought limits photosynthetic CO2 assimilation through stomatal closure or by metabolic impairment in C3 plants. Comparing results from different studies is difficult due to interspecific differences in the response of photosynthesis to leaf water potential and/or relative water content (RWC), the most commonly used parameters to assess the severity of drought. Therefore, we have used stomatal conductance (g) as a basis for comparison of metabolic processes in different studies. The logic is that, as there is a strong link between g and photosynthesis (perhaps co-regulation between them), so different relationships between RWC or water potential and photosynthetic rate and changes in metabolism in different species and studies may be 'normalized' by relating them to g. Re-analysing data from the literature using light-saturated g as a parameter indicative of water deficits in plants shows that there is good correspondence between the onset of drought-induced inhibition of different photosynthetic sub-processes and g. Contents of ribulose bisphosphate (RuBP) and adenosine triphosphate (ATP) decrease early in drought development, at still relatively high g (higher than 150 mmol H20 m(-2) s(-1)). This suggests that RuBP regeneration and ATP synthesis are impaired. Decreased photochemistry and Rubisco activity typically occur at lower g (<100 mmol H20 m(-2) s(-1)), whereas permanent photoinhibition is only occasional, occurring at very low g (<50 mmol H20 m(-2) s(-1)). Sub-stomatal CO2 concentration decreases as g becomes smaller, but increases again at small g. The analysis suggests that stomatal closure is the earliest response to drought and the dominant limitation to photosynthesis at mild to moderate drought. However, in parallel, progressive down-regulation or inhibition of metabolic processes leads to decreased RuBP content, which becomes the dominant limitation at severe drought, and thereby inhibits photosynthetic CO2 assimilation.
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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
                8 May 2014
                : 9
                : 5
                : e96086
                Affiliations
                [1 ]Dept. of Forest Mycology and Plant Pathology, Uppsala BioCenter, SLU, Uppsala, Sweden
                [2 ]Dept. of Plant Physiology, Estonian University of Life Sciences, Tartu, Estonia
                [3 ]Institute of Evolution, The University of Haifa, Haifa, Israel
                [4 ]Dept. of Chemistry and Biotechnology, Uppsala BioCenter, SLU, Uppsala, Sweden
                [5 ]Estonian Academy of Sciences, Tallinn, Estonia
                University of Delhi South Campus, India
                Author notes

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

                Conceived and designed the experiments: ST ÜN LB IED LC GS. Performed the experiments: ST IED LC TT GS. Analyzed the data: ST ÜN IED LB LC AK GS ES. Contributed reagents/materials/analysis tools: ST ÜN LB EN GS. Wrote the paper: ST ÜN LB IED LC.

                Article
                PONE-D-13-47632
                10.1371/journal.pone.0096086
                4014485
                24811199
                8c8a679d-528b-453f-b362-cf42e43e97d4
                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
                : 12 November 2013
                : 2 April 2014
                Page count
                Pages: 13
                Funding
                Financial support for the study was provided by the European Commission through European Regional Fund (the Centre of Excellence in Environmental Adaptation), and the European Research Council (advanced grant 322603, SIP-VOL+), European Union FP7:247669, the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning 2009-243, Carl Tryggers Stiftelse for vetenskaplig forskning CTS09:385, Stiftelsen Oscar och Lili Lamms Minne DO2009-0052, and by the Estonian Ministry of Science and Education (institutional grant IUT-8-3). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Biochemistry
                Chemical Biology
                Biotechnology
                Plant Biotechnology
                Developmental Biology
                Plant Growth and Development
                Ecology
                Plant Ecology
                Plant-Environment Interactions
                Microbiology
                Plant Microbiology
                Plant Science
                Ecology and Environmental Sciences
                Physical Sciences
                Chemistry

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                Uncategorized

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