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      A member of wheat class III peroxidase gene family, TaPRX-2A, enhanced the tolerance of salt stress

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          Abstract

          Background

          Salt and drought are the main abiotic stresses that restrict the yield of crops. Peroxidases (PRXs) are involved in various abiotic stress responses. Furthermore, only few wheat PRXs have been characterized in the mechanism of the abiotic stress response.

          Results

          In this study, a novel wheat peroxidase (PRX) gene named TaPRX-2A, a member of wheat class III PRX gene family, was cloned and its response to salt stress was characterized. Based on the identification and evolutionary analysis of class III PRXs in 12 plants, we proposed an evolutionary model for TaPRX-2A, suggesting that occurrence of some exon fusion events during evolution. We also detected the positive selection of PRX domain in 13 PRXs involving our evolutionary model, and found 2 or 6 positively selected sites during TaPRX-2A evolution. Quantitative reverse transcription–polymerase chain reaction (qRT–PCR) results showed that TaPRX-2A exhibited relatively higher expression levels in root tissue than those exhibited in leaf and stem tissues. TaPRX-2A expression was also induced by abiotic stresses and hormone treatments such as polyethylene glycol 6000, NaCl, hydrogen peroxide (H 2O 2), salicylic acid (SA), methyljasmonic acid (MeJA) and abscisic acid (ABA). Transgenic wheat plants with overexpression of TaPRX-2A showed higher tolerance to salt stress than wild-type (WT) plants. Confocal microscopy revealed that TaPRX-2A-eGFP was mainly localized in cell nuclei. Survival rate, relative water content, and shoot length were higher in TaPRX-2A-overexpressing wheat than in the WT wheat, whereas root length was not significantly different. The activities of superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) were enhanced in TaPRX-2A-overexpressing wheat compared with those in the WT wheat, resulting in the reduction of reactive oxygen species (ROS) accumulation and malondialdehyde (MDA) content. The expression levels of downstream stress-related genes showed that RD22, TLP4, ABAI, GST22, FeSOD, and CAT exhibited higher expressions in TaPRX-2A-overexpressing wheat than in WT under salt stress.

          Conclusions

          The results show that TaPRX-2A plays a positive role in the response to salt stress by scavenging ROS and regulating stress-related genes.

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          Most cited references53

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          MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets.

          We present the latest version of the Molecular Evolutionary Genetics Analysis (Mega) software, which contains many sophisticated methods and tools for phylogenomics and phylomedicine. In this major upgrade, Mega has been optimized for use on 64-bit computing systems for analyzing larger datasets. Researchers can now explore and analyze tens of thousands of sequences in Mega The new version also provides an advanced wizard for building timetrees and includes a new functionality to automatically predict gene duplication events in gene family trees. The 64-bit Mega is made available in two interfaces: graphical and command line. The graphical user interface (GUI) is a native Microsoft Windows application that can also be used on Mac OS X. The command line Mega is available as native applications for Windows, Linux, and Mac OS X. They are intended for use in high-throughput and scripted analysis. Both versions are available from www.megasoftware.net free of charge.
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            Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways.

            Recently, a major transcription system that controls abscisic-acid-independent gene expression in response to dehydration and low temperature has been identified. The system includes the DRE/CRT (dehydration-responsive element/C-repeat) cis-acting element and its DNA-binding protein, DREB/CBF (DRE-binding protein/C-repeat binding factor), which has an AP2 domain. DREB/CBF contains two subclasses, DREB1/CBF and DREB2, which are induced by cold and dehydration, respectively, and control the expression of various genes involved in stress tolerance. Recent studies are providing evidence of differences between dehydration-signaling and cold-stress-signaling cascades, and of cross-talk between them.
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              ROS Regulation During Abiotic Stress Responses in Crop Plants

              Abiotic stresses such as drought, cold, salt and heat cause reduction of plant growth and loss of crop yield worldwide. Reactive oxygen species (ROS) including hydrogen peroxide (H2O2), superoxide anions (O2 •-), hydroxyl radical (OH•) and singlet oxygen (1O2) are by-products of physiological metabolisms, and are precisely controlled by enzymatic and non-enzymatic antioxidant defense systems. ROS are significantly accumulated under abiotic stress conditions, which cause oxidative damage and eventually resulting in cell death. Recently, ROS have been also recognized as key players in the complex signaling network of plants stress responses. The involvement of ROS in signal transduction implies that there must be coordinated function of regulation networks to maintain ROS at non-toxic levels in a delicate balancing act between ROS production, involving ROS generating enzymes and the unavoidable production of ROS during basic cellular metabolism, and ROS-scavenging pathways. Increasing evidence showed that ROS play crucial roles in abiotic stress responses of crop plants for the activation of stress-response and defense pathways. More importantly, manipulating ROS levels provides an opportunity to enhance stress tolerances of crop plants under a variety of unfavorable environmental conditions. This review presents an overview of current knowledge about homeostasis regulation of ROS in crop plants. In particular, we summarize the essential proteins that are involved in abiotic stress tolerance of crop plants through ROS regulation. Finally, the challenges toward the improvement of abiotic stress tolerance through ROS regulation in crops are discussed.
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                Author and article information

                Contributors
                pssu2014@163.com
                xinsinian2006@163.com
                2832802566@qq.com
                wangzi651@163.com
                17863800651@163.com
                maxin138@163.com
                lianfei@sdau.edu.cn
                wanghongwei@sdau.edu.cn
                lkong@sdau.edu.cn
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                26 August 2020
                26 August 2020
                2020
                : 20
                : 392
                Affiliations
                [1 ]GRID grid.440622.6, ISNI 0000 0000 9482 4676, State Key Laboratory of Crop Biology, Shandong Key Laboratory of Crop Biology, College of Agronomy, , Shandong Agricultural University, ; Tai’an, 271018 People’s Republic of China
                [2 ]GRID grid.440622.6, ISNI 0000 0000 9482 4676, College of Information Science and Engineering, , Shandong Agricultural University, ; Tai’an, Shandong 271018 People’s Republic of China
                Article
                2602
                10.1186/s12870-020-02602-1
                7449071
                32847515
                868f1d3d-e48b-4339-9a2b-8f7ffc1bf703
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.

                History
                : 30 December 2019
                : 16 August 2020
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2020

                Plant science & Botany
                wheat,salinity stresses,peroxidases,taprx-2a
                Plant science & Botany
                wheat, salinity stresses, peroxidases, taprx-2a

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