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      Specialized core bacteria associate with plants adapted to adverse environment with high calcium contents

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          Abstract

          Karst topography is formed from the dissolution of soluble rocks, such as limestone and dolomite. In soils of such a landform, excessive contents of exchangeable calcium seriously limit the growth of vegetations. Researches have proved that rhizosphere microorganisms and endophytes help host plants to adapt to various adverse environments. The adaptive capacity of plants that grow in adverse environment with salt, drought, thermal and heavy metal stresses partially or completely comes from symbiotic microorganisms. By using the high-throughput amplicon sequencing, the bacterial community structures in soil with high calcium contents and roots and leaves of Cochlearia henryi that is commonly seen in karst area were analyzed. The bacteria community structures in these three compartments showed obvious differences. This indicates that C. henryi, which is adaptive to high calcium stress, selectively co-exists with specific bacteria. Although the bacteria community structures in these three compartments differed significantly, there were 73 operational taxonomic units (OTUs) shared by karst soils as well as roots and leaves of C. henryi. The phylogenetic diversity of these 73 OTUs differed significantly from that of overall OTUs detected. There were also obvious differences in KEGG (Kyoto Encyclopedia of Genes and Genomes) pathways and abundance values between the 73 OTUs and overall bacterial communities. A large number of OTUs shared by the karst soils, roots and leaves of C. henryi had close genetic relationship with known stress-resistant bacterial strains. Our results showed that the functional bacteria can be predicted by exploring core bacteria, bacteria shared by soils, adaptable plant roots and leaves. This information will potentially accelerate studies on natural microbial communities which can promote the adaptive capacity of host plants to high calcium stress, and will be valuable for finding microbial strains for field application in karst topography.

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          Most cited references17

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          Calcium in plants.

          Calcium is an essential plant nutrient. It is required for various structural roles in the cell wall and membranes, it is a counter-cation for inorganic and organic anions in the vacuole, and the cytosolic Ca2+ concentration ([Ca2+]cyt) is an obligate intracellular messenger coordinating responses to numerous developmental cues and environmental challenges. This article provides an overview of the nutritional requirements of different plants for Ca, and how this impacts on natural flora and the Ca content of crops. It also reviews recent work on (a) the mechanisms of Ca2+ transport across cellular membranes, (b) understanding the origins and specificity of [Ca2+]cyt signals and (c) characterizing the cellular [Ca2+]cyt-sensors (such as calmodulin, calcineurin B-like proteins and calcium-dependent protein kinases) that allow plant cells to respond appropriately to [Ca2+]cyt signals.
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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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              Rapid responses of soil microorganisms improve plant fitness in novel environments.

              Global change is challenging plant and animal populations with novel environmental conditions, including increased atmospheric CO(2) concentrations, warmer temperatures, and altered precipitation regimes. In some cases, contemporary or "rapid" evolution can ameliorate the effects of global change. However, the direction and magnitude of evolutionary responses may be contingent upon interactions with other community members that also are experiencing novel environmental conditions. Here, we examine plant adaptation to drought stress in a multigeneration experiment that manipulated aboveground-belowground feedbacks between plants and soil microbial communities. Although drought stress reduced plant growth and accelerated plant phenologies, surprisingly, plant evolutionary responses to drought were relatively weak. In contrast, plant fitness in both drought and nondrought environments was linked strongly to the rapid responses of soil microbial community structure to moisture manipulations. Specifically, plants were most fit when their contemporary environmental conditions (wet vs. dry soil) matched the historical environmental conditions (wet vs. dry soil) of their associated microbial community. Together, our findings suggest that, when faced with environmental change, plants may not be limited to "adapt or migrate" strategies; instead, they also may benefit from association with interacting species, especially diverse soil microbial communities, that respond rapidly to environmental change.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: MethodologyRole: SoftwareRole: Validation
                Role: MethodologyRole: Resources
                Role: InvestigationRole: Resources
                Role: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                8 March 2018
                2018
                : 13
                : 3
                : e0194080
                Affiliations
                [001]Key Laboratory of Plant Physiology and Developmental Regulation, School of Life Sciences, Guizhou Normal University, Guiyang, Guizhou, China
                Estacion Experimental del Zaidin, SPAIN
                Author notes

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

                Author information
                http://orcid.org/0000-0002-1107-7375
                Article
                PONE-D-17-28527
                10.1371/journal.pone.0194080
                5843345
                29518143
                3fcfed14-2657-422a-a5f4-6fc76c2c518d
                © 2018 Li 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
                : 1 August 2017
                : 23 February 2018
                Page count
                Figures: 6, Tables: 1, Pages: 15
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: Grant No. 31760138
                Award Recipient :
                Funded by: Natural Science Foundation of Guizhou Province
                Award ID: Qian scientific contract No. [2016]7212
                Award Recipient :
                This work was supported by Natural Science Foundation of Guizhou Province; Award Number: [2016]7212 | http://kjt.gzst.gov.cn/, Guizhou Normal University Foundation for Ph.D Scholars http://www.gznu.edu.cn/. 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
                Organisms
                Bacteria
                Biology and Life Sciences
                Ecology
                Community Ecology
                Community Structure
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Community Structure
                Biology and Life Sciences
                Agriculture
                Agricultural Soil Science
                Ecology and Environmental Sciences
                Soil Science
                Agricultural Soil Science
                Earth Sciences
                Geography
                Physical Geography
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Systematics
                Phylogenetics
                Biology and Life Sciences
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Computer and Information Sciences
                Data Management
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Leaves
                Research and Analysis Methods
                Database and Informatics Methods
                Biological Databases
                Sequence Databases
                Research and Analysis Methods
                Database and Informatics Methods
                Bioinformatics
                Sequence Analysis
                Sequence Databases
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Custom metadata
                All relevant data are available within the paper, its Supporting Information files, and at GenBank ( https://www.ncbi.nlm.nih.gov/popset) under the accession numbers MF114128-MF114200.

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