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      Genome-wide transcriptional adaptation to salt stress in Populus

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          Abstract

          Background

          Adaptation to abiotic stresses is crucial for the survival of perennial plants in a natural environment. However, very little is known about the underlying mechanisms. Here, we adopted a liquid culture system to investigate plant adaptation to repeated salt stress in Populus trees.

          Results

          We first evaluated phenotypic responses and found that plants exhibit better stress tolerance after pre-treatment of salt stress. Time-course RNA sequencing (RNA-seq) was then performed to profile changes in gene expression over 12 h of salt treatments. Analysis of differentially expressed genes (DEGs) indicated that significant transcriptional reprogramming and adaptation to repeated salt treatment occurred. Clustering analysis identified two modules of co-expressed genes that were potentially critical for repeated salt stress adaptation, and one key module for salt stress response in general. Gene Ontology (GO) enrichment analysis identified pathways including hormone signaling, cell wall biosynthesis and modification, negative regulation of growth, and epigenetic regulation to be highly enriched in these gene modules.

          Conclusions

          This study illustrates phenotypic and transcriptional adaptation of Populus trees to salt stress, revealing novel gene modules which are potentially critical for responding and adapting to salt stress.

          Electronic supplementary material

          The online version of this article (10.1186/s12870-019-1952-2) contains supplementary material, which is available to authorized users.

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          Most cited references53

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          Plant hormone-mediated regulation of stress responses

          Background Being sessile organisms, plants are often exposed to a wide array of abiotic and biotic stresses. Abiotic stress conditions include drought, heat, cold and salinity, whereas biotic stress arises mainly from bacteria, fungi, viruses, nematodes and insects. To adapt to such adverse situations, plants have evolved well-developed mechanisms that help to perceive the stress signal and enable optimal growth response. Phytohormones play critical roles in helping the plants to adapt to adverse environmental conditions. The elaborate hormone signaling networks and their ability to crosstalk make them ideal candidates for mediating defense responses. Results Recent research findings have helped to clarify the elaborate signaling networks and the sophisticated crosstalk occurring among the different hormone signaling pathways. In this review, we summarize the roles of the major plant hormones in regulating abiotic and biotic stress responses with special focus on the significance of crosstalk between different hormones in generating a sophisticated and efficient stress response. We divided the discussion into the roles of ABA, salicylic acid, jasmonates and ethylene separately at the start of the review. Subsequently, we have discussed the crosstalk among them, followed by crosstalk with growth promoting hormones (gibberellins, auxins and cytokinins). These have been illustrated with examples drawn from selected abiotic and biotic stress responses. The discussion on seed dormancy and germination serves to illustrate the fine balance that can be enforced by the two key hormones ABA and GA in regulating plant responses to environmental signals. Conclusions The intricate web of crosstalk among the often redundant multitudes of signaling intermediates is just beginning to be understood. Future research employing genome-scale systems biology approaches to solve problems of such magnitude will undoubtedly lead to a better understanding of plant development. Therefore, discovering additional crosstalk mechanisms among various hormones in coordinating growth under stress will be an important theme in the field of abiotic stress research. Such efforts will help to reveal important points of genetic control that can be useful to engineer stress tolerant crops.
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            Epigenetic regulation of stress responses in plants.

            Gene expression driven by developmental and stress cues often depends on nucleosome histone post-translational modifications and sometimes on DNA methylation. A number of studies have shown that these DNA and histone modifications play a key role in gene expression and plant development under stress. Most of these stress-induced modifications are reset to the basal level once the stress is relieved, while some of the modifications may be stable, that is, may be carried forward as 'stress memory' and may be inherited across mitotic or even meiotic cell divisions. Epigenetic stress memory may help plants more effectively cope with subsequent stresses. Comparative studies on stress-responsive epigenomes and transcriptomes will enhance our understanding of stress adaptation of plants.
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              The role of gibberellin signalling in plant responses to abiotic stress.

              Plant hormones are small molecules that regulate plant growth and development, as well as responses to changing environmental conditions. By modifying the production, distribution or signal transduction of these hormones, plants are able to regulate and coordinate both growth and/or stress tolerance to promote survival or escape from environmental stress. A central role for the gibberellin (GA) class of growth hormones in the response to abiotic stress is becoming increasingly evident. Reduction of GA levels and signalling has been shown to contribute to plant growth restriction on exposure to several stresses, including cold, salt and osmotic stress. Conversely, increased GA biosynthesis and signalling promote growth in plant escape responses to shading and submergence. In several cases, GA signalling has also been linked to stress tolerance. The transcriptional regulation of GA metabolism appears to be a major point of regulation of the GA pathway, while emerging evidence for interaction of the GA-signalling molecule DELLA with components of the signalling pathway for the stress hormone jasmonic acid suggests additional mechanisms by which GA signalling may integrate multiple hormone signalling pathways in the response to stress. Here, we review the evidence for the role of GA in these processes, and the regulation of the GA signalling pathway on exposure to abiotic stress. The potential mechanisms by which GA signalling modulates stress tolerance are also discussed.
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                Author and article information

                Contributors
                liujingui2016@163.com
                hanx2017@zafu.edu.cn
                ytong0112@163.com
                whcui2018@163.com
                wuaimin@scau.edu.cn
                fucx@qibebt.ac.cn
                wangbc@ibcas.ac.cn
                +86 538 824 2118 , lijunliu@sdau.edu.cn
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                20 August 2019
                20 August 2019
                2019
                : 19
                : 367
                Affiliations
                [1 ]State Forestry and Grassland Administration Key Laboratory of Silviculture in downstream areas of the Yellow River, College of Forestry, Shandong Agriculture University, Taian, 271018 Shandong China
                [2 ]ISNI 0000 0000 9152 7385, GRID grid.443483.c, State Key Laboratory of Subtropical Silviculture, College of Forestry and Biotechnology, , Zhejiang A&F University, ; Lin’an, Hangzhou, 311300 China
                [3 ]ISNI 0000 0000 9546 5767, GRID grid.20561.30, Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, College of Forestry and Landscape Architecture, , South China Agricultural University, ; Guangzhou, 510642 China
                [4 ]ISNI 0000 0004 1806 7609, GRID grid.458500.c, Key Laboratory of Biofuels, Qingdao Engineering Research Center of Biomass Resources and Environment, , Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of Sciences, ; Qingdao, 266101 Shandong China
                [5 ]ISNI 0000 0004 0596 3367, GRID grid.435133.3, Photosynthesis Research Center, Key Laboratory of Photobiology, , Institute of Botany, Chinese Academy of Sciences, ; Beijing, 100093 China
                Author information
                http://orcid.org/0000-0002-4728-7841
                Article
                1952
                10.1186/s12870-019-1952-2
                6701017
                31429697
                53fa9009-c4fa-48d5-8adc-11752a8aeff2
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 31 March 2019
                : 29 July 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31700583
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Plant science & Botany
                abiotic stress,adaptation,perennial plants,populus,gene module
                Plant science & Botany
                abiotic stress, adaptation, perennial plants, populus, gene module

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