<i>Kandelia candel</i> Thioredoxin f Confers Osmotic Stress Tolerance in Transgenic Tobacco

Water deficit caused by osmotic stress and drought limits crop yield and tree growth worldwide. Screening and identifying candidate genes from stress-resistant species are a genetic engineering strategy to increase drought resistance. In this study, an increased concentration of mannitol resulted in...

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Main Authors: Xiaoshu Jing, Jun Yao, Xujun Ma, Yanli Zhang, Yuanling Sun, Min Xiang, Peichen Hou, Niya Li, Rui Zhao, Jinke Li, Xiaoyang Zhou, Shaoliang Chen
Format: Article
Language:English
Published: MDPI AG 2020-05-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/21/9/3335
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author Xiaoshu Jing
Jun Yao
Xujun Ma
Yanli Zhang
Yuanling Sun
Min Xiang
Peichen Hou
Niya Li
Rui Zhao
Jinke Li
Xiaoyang Zhou
Shaoliang Chen
author_facet Xiaoshu Jing
Jun Yao
Xujun Ma
Yanli Zhang
Yuanling Sun
Min Xiang
Peichen Hou
Niya Li
Rui Zhao
Jinke Li
Xiaoyang Zhou
Shaoliang Chen
author_sort Xiaoshu Jing
collection DOAJ
description Water deficit caused by osmotic stress and drought limits crop yield and tree growth worldwide. Screening and identifying candidate genes from stress-resistant species are a genetic engineering strategy to increase drought resistance. In this study, an increased concentration of mannitol resulted in elevated expression of thioredoxin f (<i>KcTrxf</i>) in the nonsecretor mangrove species <i>Kandelia candel</i>. By means of amino acid sequence and phylogenetic analysis, the mangrove Trx was classified as an f-type thioredoxin. Subcellular localization showed that KcTrxf localizes to chloroplasts. Enzymatic activity characterization revealed that KcTrxf recombinant protein possesses the disulfide reductase function. <i>KcTrxf</i> overexpression contributes to osmotic and drought tolerance in tobacco in terms of fresh weight, root length, malondialdehyde (MDA) content, and hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>) production. KcTrxf was shown to reduce the stomatal aperture by enhancing K<sup>+</sup> efflux in guard cells, which increased the water-retaining capacity in leaves under drought conditions. Notably, the abscisic acid (ABA) sensitivity was increased in <i>KcTrxf</i>-transgenic tobacco, which benefits plants exposed to drought by reducing water loss by promoting stomatal closure. <i>KcTrxf</i>-transgenic plants limited drought-induced H<sub>2</sub>O<sub>2</sub> in leaves, which could reduce lipid peroxidation and retain the membrane integrity. Additionally, glutathione (GSH) contributing to reactive oxygen species (ROS) scavenging and transgenic plants are more efficient at regenerating GSH from oxidized glutathione (GSSG) under conditions of drought stress. Notably, <i>KcTrxf</i>-transgenic plants had increased glucose and fructose contents under drought stress conditions, presumably resulting from KcTrxf-promoted starch degradation under water stress. We conclude that KcTrxf contributes to drought tolerance by increasing the water status, by enhancing osmotic adjustment, and by maintaining ROS homeostasis in transgene plants.
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spelling doaj.art-ca4f87b19ff94fb2b2d0cd6e47a236e52023-11-19T23:48:59ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-05-01219333510.3390/ijms21093335<i>Kandelia candel</i> Thioredoxin f Confers Osmotic Stress Tolerance in Transgenic TobaccoXiaoshu Jing0Jun Yao1Xujun Ma2Yanli Zhang3Yuanling Sun4Min Xiang5Peichen Hou6Niya Li7Rui Zhao8Jinke Li9Xiaoyang Zhou10Shaoliang Chen11Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, ChinaBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, ChinaUrat Desert-Grassland Research Station, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Science, Lanzhou 730000, ChinaBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, ChinaBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, ChinaDepartment of Biology, College of Life Science, Hainan Normal University, Haikou 571158, ChinaBeijing Research Center of Intelligent Equipment for Agriculture, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, ChinaDepartment of Biology, College of Life Science, Hainan Normal University, Haikou 571158, ChinaBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, ChinaBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, ChinaBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, ChinaBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, ChinaWater deficit caused by osmotic stress and drought limits crop yield and tree growth worldwide. Screening and identifying candidate genes from stress-resistant species are a genetic engineering strategy to increase drought resistance. In this study, an increased concentration of mannitol resulted in elevated expression of thioredoxin f (<i>KcTrxf</i>) in the nonsecretor mangrove species <i>Kandelia candel</i>. By means of amino acid sequence and phylogenetic analysis, the mangrove Trx was classified as an f-type thioredoxin. Subcellular localization showed that KcTrxf localizes to chloroplasts. Enzymatic activity characterization revealed that KcTrxf recombinant protein possesses the disulfide reductase function. <i>KcTrxf</i> overexpression contributes to osmotic and drought tolerance in tobacco in terms of fresh weight, root length, malondialdehyde (MDA) content, and hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>) production. KcTrxf was shown to reduce the stomatal aperture by enhancing K<sup>+</sup> efflux in guard cells, which increased the water-retaining capacity in leaves under drought conditions. Notably, the abscisic acid (ABA) sensitivity was increased in <i>KcTrxf</i>-transgenic tobacco, which benefits plants exposed to drought by reducing water loss by promoting stomatal closure. <i>KcTrxf</i>-transgenic plants limited drought-induced H<sub>2</sub>O<sub>2</sub> in leaves, which could reduce lipid peroxidation and retain the membrane integrity. Additionally, glutathione (GSH) contributing to reactive oxygen species (ROS) scavenging and transgenic plants are more efficient at regenerating GSH from oxidized glutathione (GSSG) under conditions of drought stress. Notably, <i>KcTrxf</i>-transgenic plants had increased glucose and fructose contents under drought stress conditions, presumably resulting from KcTrxf-promoted starch degradation under water stress. We conclude that KcTrxf contributes to drought tolerance by increasing the water status, by enhancing osmotic adjustment, and by maintaining ROS homeostasis in transgene plants.https://www.mdpi.com/1422-0067/21/9/3335thioredoxin<i>Kandelia candel</i>mannitoldroughtwater retaining capacitysoluble sugar
spellingShingle Xiaoshu Jing
Jun Yao
Xujun Ma
Yanli Zhang
Yuanling Sun
Min Xiang
Peichen Hou
Niya Li
Rui Zhao
Jinke Li
Xiaoyang Zhou
Shaoliang Chen
<i>Kandelia candel</i> Thioredoxin f Confers Osmotic Stress Tolerance in Transgenic Tobacco
International Journal of Molecular Sciences
thioredoxin
<i>Kandelia candel</i>
mannitol
drought
water retaining capacity
soluble sugar
title <i>Kandelia candel</i> Thioredoxin f Confers Osmotic Stress Tolerance in Transgenic Tobacco
title_full <i>Kandelia candel</i> Thioredoxin f Confers Osmotic Stress Tolerance in Transgenic Tobacco
title_fullStr <i>Kandelia candel</i> Thioredoxin f Confers Osmotic Stress Tolerance in Transgenic Tobacco
title_full_unstemmed <i>Kandelia candel</i> Thioredoxin f Confers Osmotic Stress Tolerance in Transgenic Tobacco
title_short <i>Kandelia candel</i> Thioredoxin f Confers Osmotic Stress Tolerance in Transgenic Tobacco
title_sort i kandelia candel i thioredoxin f confers osmotic stress tolerance in transgenic tobacco
topic thioredoxin
<i>Kandelia candel</i>
mannitol
drought
water retaining capacity
soluble sugar
url https://www.mdpi.com/1422-0067/21/9/3335
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