Genome-Wide Identification of the <i>Gossypium hirsutum</i> NHX Genes Reveals that the Endosomal-Type <i>GhNHX4A</i> is Critical for the Salt Tolerance of Cotton

Soil salinization, which is primarily due to excessive Na<sup>+</sup> levels, is a major abiotic stress adversely affecting plant growth and development. The Na<sup>+</sup>/H<sup>+</sup> antiporter (NHX) is a transmembrane protein mediating the transport of Na<...

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Main Authors: Wenyu Ma, Zhongying Ren, Yang Zhou, Junjie Zhao, Fei Zhang, Junping Feng, Wei Liu, Xiongfeng Ma
Format: Article
Language:English
Published: MDPI AG 2020-10-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/21/20/7712
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spelling doaj-3b41e18a863a455790fb2d04c8d6617d2020-11-25T02:25:45ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-10-01217712771210.3390/ijms21207712Genome-Wide Identification of the <i>Gossypium hirsutum</i> NHX Genes Reveals that the Endosomal-Type <i>GhNHX4A</i> is Critical for the Salt Tolerance of CottonWenyu Ma0Zhongying Ren1Yang Zhou2Junjie Zhao3Fei Zhang4Junping Feng5Wei Liu6Xiongfeng Ma7State Key Laboratory of Cotton Biology, Institute of Cotton Research of the Chinese Academy of Agricultural Sciences, Anyang 455000, ChinaState Key Laboratory of Cotton Biology, Institute of Cotton Research of the Chinese Academy of Agricultural Sciences, Anyang 455000, ChinaHainan Key Laboratory for Biotechnology of Salt Tolerant Crops, College of Horticulture, Hainan University, Haikou 570228, ChinaState Key Laboratory of Cotton Biology, Institute of Cotton Research of the Chinese Academy of Agricultural Sciences, Anyang 455000, ChinaState Key Laboratory of Cotton Biology, Institute of Cotton Research of the Chinese Academy of Agricultural Sciences, Anyang 455000, ChinaCollaborative Innovation Center of Henan Grain Crops, Agronomy College, Henan Agricultural University, Zhengzhou 450002, ChinaCollaborative Innovation Center of Henan Grain Crops, Agronomy College, Henan Agricultural University, Zhengzhou 450002, ChinaState Key Laboratory of Cotton Biology, Institute of Cotton Research of the Chinese Academy of Agricultural Sciences, Anyang 455000, ChinaSoil salinization, which is primarily due to excessive Na<sup>+</sup> levels, is a major abiotic stress adversely affecting plant growth and development. The Na<sup>+</sup>/H<sup>+</sup> antiporter (NHX) is a transmembrane protein mediating the transport of Na<sup>+</sup> or K<sup>+</sup> and H<sup>+</sup> across the membrane to modulate the ionic balance of plants in response to salt stress. Research regarding NHXs has mainly focused on the vacuolar-type NHX family members. However, the biological functions of the endosomal-type NHXs remain relatively uncharacterized. In this study, 22 NHX family members were identified in <i>Gossypium hirsutum</i>. A phylogenetic analysis divided the <i>GhNHX</i> genes into two categories, with 18 and 4 in the vacuolar and endosomal groups, respectively. The chromosomal distribution of the NHX genes revealed the significant impact of genome-wide duplication during the polyploidization process on the number of <i>GhNHX</i> genes. Analyses of gene structures and conserved motifs indicated that <i>GhNHX </i>genes in the same phylogenetic cluster are conserved. Additionally, the salt-induced expression patterns confirmed that the expression levels of most of the <i>GhNHX</i> genes are affected by salinity. Specifically, in the endosomal group, <i>GhNHX4A</i> expression was substantially up-regulated by salt stress. A yeast functional complementation test proved that <i>GhNHX4A</i> can partially restore the salt tolerance of the salt-sensitive yeast mutant AXT3. Silencing <i>GhNHX4A</i> expression decreased the resistance of cotton to salt stress because of an increase in the accumulation of Na<sup>+</sup> in stems and a decrease in the accumulation of K<sup>+</sup> in roots. The results of this study may provide the basis for an in-depth characterization of the regulatory functions of NHX genes related to cotton salt tolerance, especially the endosomal-type <i>GhNHX4A</i>. Furthermore, the presented data may be useful for selecting appropriate candidate genes for the breeding of new salt-tolerant cotton varieties.https://www.mdpi.com/1422-0067/21/20/7712<i>Gossypium hirsutum</i>salt stressNa<sup>+</sup>/H<sup>+</sup> antiportergenome-wide identificationvirus-induced gene silencing
collection DOAJ
language English
format Article
sources DOAJ
author Wenyu Ma
Zhongying Ren
Yang Zhou
Junjie Zhao
Fei Zhang
Junping Feng
Wei Liu
Xiongfeng Ma
spellingShingle Wenyu Ma
Zhongying Ren
Yang Zhou
Junjie Zhao
Fei Zhang
Junping Feng
Wei Liu
Xiongfeng Ma
Genome-Wide Identification of the <i>Gossypium hirsutum</i> NHX Genes Reveals that the Endosomal-Type <i>GhNHX4A</i> is Critical for the Salt Tolerance of Cotton
International Journal of Molecular Sciences
<i>Gossypium hirsutum</i>
salt stress
Na<sup>+</sup>/H<sup>+</sup> antiporter
genome-wide identification
virus-induced gene silencing
author_facet Wenyu Ma
Zhongying Ren
Yang Zhou
Junjie Zhao
Fei Zhang
Junping Feng
Wei Liu
Xiongfeng Ma
author_sort Wenyu Ma
title Genome-Wide Identification of the <i>Gossypium hirsutum</i> NHX Genes Reveals that the Endosomal-Type <i>GhNHX4A</i> is Critical for the Salt Tolerance of Cotton
title_short Genome-Wide Identification of the <i>Gossypium hirsutum</i> NHX Genes Reveals that the Endosomal-Type <i>GhNHX4A</i> is Critical for the Salt Tolerance of Cotton
title_full Genome-Wide Identification of the <i>Gossypium hirsutum</i> NHX Genes Reveals that the Endosomal-Type <i>GhNHX4A</i> is Critical for the Salt Tolerance of Cotton
title_fullStr Genome-Wide Identification of the <i>Gossypium hirsutum</i> NHX Genes Reveals that the Endosomal-Type <i>GhNHX4A</i> is Critical for the Salt Tolerance of Cotton
title_full_unstemmed Genome-Wide Identification of the <i>Gossypium hirsutum</i> NHX Genes Reveals that the Endosomal-Type <i>GhNHX4A</i> is Critical for the Salt Tolerance of Cotton
title_sort genome-wide identification of the <i>gossypium hirsutum</i> nhx genes reveals that the endosomal-type <i>ghnhx4a</i> is critical for the salt tolerance of cotton
publisher MDPI AG
series International Journal of Molecular Sciences
issn 1661-6596
1422-0067
publishDate 2020-10-01
description Soil salinization, which is primarily due to excessive Na<sup>+</sup> levels, is a major abiotic stress adversely affecting plant growth and development. The Na<sup>+</sup>/H<sup>+</sup> antiporter (NHX) is a transmembrane protein mediating the transport of Na<sup>+</sup> or K<sup>+</sup> and H<sup>+</sup> across the membrane to modulate the ionic balance of plants in response to salt stress. Research regarding NHXs has mainly focused on the vacuolar-type NHX family members. However, the biological functions of the endosomal-type NHXs remain relatively uncharacterized. In this study, 22 NHX family members were identified in <i>Gossypium hirsutum</i>. A phylogenetic analysis divided the <i>GhNHX</i> genes into two categories, with 18 and 4 in the vacuolar and endosomal groups, respectively. The chromosomal distribution of the NHX genes revealed the significant impact of genome-wide duplication during the polyploidization process on the number of <i>GhNHX</i> genes. Analyses of gene structures and conserved motifs indicated that <i>GhNHX </i>genes in the same phylogenetic cluster are conserved. Additionally, the salt-induced expression patterns confirmed that the expression levels of most of the <i>GhNHX</i> genes are affected by salinity. Specifically, in the endosomal group, <i>GhNHX4A</i> expression was substantially up-regulated by salt stress. A yeast functional complementation test proved that <i>GhNHX4A</i> can partially restore the salt tolerance of the salt-sensitive yeast mutant AXT3. Silencing <i>GhNHX4A</i> expression decreased the resistance of cotton to salt stress because of an increase in the accumulation of Na<sup>+</sup> in stems and a decrease in the accumulation of K<sup>+</sup> in roots. The results of this study may provide the basis for an in-depth characterization of the regulatory functions of NHX genes related to cotton salt tolerance, especially the endosomal-type <i>GhNHX4A</i>. Furthermore, the presented data may be useful for selecting appropriate candidate genes for the breeding of new salt-tolerant cotton varieties.
topic <i>Gossypium hirsutum</i>
salt stress
Na<sup>+</sup>/H<sup>+</sup> antiporter
genome-wide identification
virus-induced gene silencing
url https://www.mdpi.com/1422-0067/21/20/7712
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