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      Multilevel Regulation of Abiotic Stress Responses in Plants

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          Abstract

          The sessile lifestyle of plants requires them to cope with stresses in situ. Plants overcome abiotic stresses by altering structure/morphology, and in some extreme conditions, by compressing the life cycle to survive the stresses in the form of seeds. Genetic and molecular studies have uncovered complex regulatory processes that coordinate stress adaptation and tolerance in plants, which are integrated at various levels. Investigating natural variation in stress responses has provided important insights into the evolutionary processes that shape the integrated regulation of adaptation and tolerance. This review primarily focuses on the current understanding of how transcriptional, post-transcriptional, post-translational, and epigenetic processes along with genetic variation orchestrate stress responses in plants. We also discuss the current and future development of computational tools to identify biologically meaningful factors from high dimensional, genome-scale data and construct the signaling networks consisting of these components.

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          Most cited references225

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          ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis.

          Cold temperatures trigger the expression of the CBF family of transcription factors, which in turn activate many downstream genes that confer chilling and freezing tolerance to plants. We report here the identification of ICE1 (inducer of CBF expression 1), an upstream transcription factor that regulates the transcription of CBF genes in the cold. An Arabidopsis ice1 mutant was isolated in a screen for mutations that impair cold-induced transcription of a CBF3 promoter-luciferase reporter gene. The ice1 mutation blocks the expression of CBF3 and decreases the expression of many genes downstream of CBFs, which leads to a significant reduction in plant chilling and freezing tolerance. ICE1 encodes a MYC-like bHLH transcriptional activator. ICE1 binds specifically to the MYC recognition sequences in the CBF3 promoter. ICE1 is expressed constitutively, and its overexpression in wild-type plants enhances the expression of the CBF regulon in the cold and improves freezing tolerance of the transgenic plants.
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            The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter.

            In Arabidopsis thaliana, the SOS1 (Salt Overly Sensitive 1) locus is essential for Na(+) and K(+) homeostasis, and sos1 mutations render plants more sensitive to growth inhibition by high Na(+) and low K(+) environments. SOS1 is cloned and predicted to encode a 127-kDa protein with 12 transmembrane domains in the N-terminal part and a long hydrophilic cytoplasmic tail in the C-terminal part. The transmembrane region of SOS1 has significant sequence similarities to plasma membrane Na(+)/H(+) antiporters from bacteria and fungi. Sequence analysis of various sos1 mutant alleles reveals several residues and regions in the transmembrane as well as the tail parts that are critical for SOS1 function in plant salt tolerance. SOS1 gene expression in plants is up-regulated in response to NaCl stress. This up-regulation is abated in sos3 or sos2 mutant plants, suggesting that it is controlled by the SOS3/SOS2 regulatory pathway.
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              CHL1 functions as a nitrate sensor in plants.

              Ions serve as essential nutrients in higher plants and can also act as signaling molecules. Little is known about how plants sense changes in soil nutrient concentrations. Previous studies showed that T101-phosphorylated CHL1 is a high-affinity nitrate transporter, whereas T101-dephosphorylated CHL1 is a low-affinity transporter. In this study, analysis of an uptake- and sensing-decoupled mutant showed that the nitrate transporter CHL1 functions as a nitrate sensor. Primary nitrate responses in CHL1T101D and CHLT101A transgenic plants showed that phosphorylated and dephosphorylated CHL1 lead to a low- and high-level response, respectively. In vitro and in vivo studies showed that, in response to low nitrate concentrations, protein kinase CIPK23 can phosphorylate T101 of CHL1 to maintain a low-level primary response. Thus, CHL1 uses dual-affinity binding and a phosphorylation switch to sense a wide range of nitrate concentrations in the soil, thereby functioning as an ion sensor in higher plants. For a video summary of this article, see the PaperFlick file with the Supplemental Data available online.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                20 September 2017
                2017
                : 8
                : 1564
                Affiliations
                [1] 1Department of Plant Pathology, Physiology, and Weed Science, Virginia Tech, Blacksburg VA, United States
                [2] 2Department of Crop and Soil Environmental Sciences, Virginia Tech, Blacksburg VA, United States
                [3] 3Department of Environmental and Plant Biology, Interdisciplinary Program in Molecular and Cellular Biology, Ohio University, Athens OH, United States
                [4] 4Institut für Botanik, Heinrich-Heine-Universität Düsseldorf Düsseldorf, Germany
                [5] 5Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow Glasgow, United Kingdom
                Author notes

                Edited by: Paul E. Verslues, Academia Sinica, Taiwan

                Reviewed by: Kazuo Nakashima, Japan International Research Center for Agricultural Sciences, Japan; Giorgia Batelli, Consiglio Nazionale Delle Ricerche (CNR), Italy

                *Correspondence: Ruth Grene, grene@ 123456vt.edu

                This article was submitted to Plant Abiotic Stress, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2017.01564
                5627039
                29033955
                df5ec480-16ca-4508-abc7-42554f9228db
                Copyright © 2017 Haak, Fukao, Grene, Hua, Ivanov, Perrella and Li.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 05 April 2017
                : 28 August 2017
                Page count
                Figures: 5, Tables: 0, Equations: 0, References: 274, Pages: 24, Words: 0
                Funding
                Funded by: National Science Foundation 10.13039/100000001
                Award ID: DBI-1062472
                Award ID: MCB-1052145
                Categories
                Plant Science
                Review

                Plant science & Botany
                abiotic stress,alternative splicing,protein modification,ion transport,chromatin modification,transcriptional and post-transcriptional regulation,data-driven modeling,network modeling

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