Phosphorus Starvation- and Zinc Excess-Induced <i>Astragalus sinicus</i> AsZIP2 Zinc Transporter Is Suppressed by Arbuscular Mycorrhizal Symbiosis

Zinc (Zn) is one of the most essential micronutrients for plant growth and metabolism, but Zn excess can impair many basic metabolic processes in plant cells. In agriculture, crops often experience low phosphate (Pi) and high Zn double nutrient stresses because of inordinate agro-industrial activiti...

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Main Authors: Xianan Xie, Xiaoning Fan, Hui Chen, Ming Tang
Format: Article
Language:English
Published: MDPI AG 2021-10-01
Series:Journal of Fungi
Subjects:
Online Access:https://www.mdpi.com/2309-608X/7/11/892
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author Xianan Xie
Xiaoning Fan
Hui Chen
Ming Tang
author_facet Xianan Xie
Xiaoning Fan
Hui Chen
Ming Tang
author_sort Xianan Xie
collection DOAJ
description Zinc (Zn) is one of the most essential micronutrients for plant growth and metabolism, but Zn excess can impair many basic metabolic processes in plant cells. In agriculture, crops often experience low phosphate (Pi) and high Zn double nutrient stresses because of inordinate agro-industrial activities, while the dual benefit of arbuscular mycorrhizal (AM) fungi protects plants from experiencing both deficient and toxic nutrient stresses. Although crosstalk between Pi and Zn nutrients in plants have been extensively studied at the physiological level, the molecular basis of how Pi starvation triggers Zn over-accumulation in plants and how AM plants coordinately modulate the Pi and Zn nutrient homeostasis remains to be elucidated. Here, we report that a novel <i>AsZIP2</i> gene, a Chinese milk vetch (<i>Astragalus sinicus</i>) member of the <i>ZIP</i> gene family, participates in the interaction between Pi and Zn nutrient homeostasis in plants. Phylogenetic analysis revealed that this AsZIP2 protein was closely related to the orthologous Medicago MtZIP2 and Arabidopsis AtZIP2 transporters. Gene expression analysis indicated that <i>AsZIP2</i> was highly induced in roots by Pi starvation or Zn excess yet attenuated by arbuscular mycorrhization in a Pi-dependent manner. Subcellular localization and heterologous expression experiments further showed that <i>AsZIP2</i> encoded a functional plasma membrane-localized transporter that mediated Zn uptake in yeast. Moreover, overexpression of <i>AsZIP2</i> in <i>A. sinicus</i> resulted in the over-accumulation of Zn concentration in roots at low Pi or excessive Zn concentrations, whereas <i>AsZIP2</i> silencing lines displayed an even more reduced Zn concentration than control lines under such conditions. Our results reveal that the AsZIP2 transporter functioned in Zn over-accumulation in roots during Pi starvation or high Zn supply but was repressed by AM symbiosis in a Pi-dependent manner. These findings also provide new insights into the <i>AsZIP2</i> gene acting in the regulation of Zn homeostasis in mycorrhizal plants through Pi signal.
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spelling doaj.art-b142aed724db4779a7c41f354b9703552023-11-22T23:55:01ZengMDPI AGJournal of Fungi2309-608X2021-10-0171189210.3390/jof7110892Phosphorus Starvation- and Zinc Excess-Induced <i>Astragalus sinicus</i> AsZIP2 Zinc Transporter Is Suppressed by Arbuscular Mycorrhizal SymbiosisXianan Xie0Xiaoning Fan1Hui Chen2Ming Tang3State Key Laboratory of Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou 510642, ChinaState Key Laboratory of Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou 510642, ChinaState Key Laboratory of Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou 510642, ChinaState Key Laboratory of Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou 510642, ChinaZinc (Zn) is one of the most essential micronutrients for plant growth and metabolism, but Zn excess can impair many basic metabolic processes in plant cells. In agriculture, crops often experience low phosphate (Pi) and high Zn double nutrient stresses because of inordinate agro-industrial activities, while the dual benefit of arbuscular mycorrhizal (AM) fungi protects plants from experiencing both deficient and toxic nutrient stresses. Although crosstalk between Pi and Zn nutrients in plants have been extensively studied at the physiological level, the molecular basis of how Pi starvation triggers Zn over-accumulation in plants and how AM plants coordinately modulate the Pi and Zn nutrient homeostasis remains to be elucidated. Here, we report that a novel <i>AsZIP2</i> gene, a Chinese milk vetch (<i>Astragalus sinicus</i>) member of the <i>ZIP</i> gene family, participates in the interaction between Pi and Zn nutrient homeostasis in plants. Phylogenetic analysis revealed that this AsZIP2 protein was closely related to the orthologous Medicago MtZIP2 and Arabidopsis AtZIP2 transporters. Gene expression analysis indicated that <i>AsZIP2</i> was highly induced in roots by Pi starvation or Zn excess yet attenuated by arbuscular mycorrhization in a Pi-dependent manner. Subcellular localization and heterologous expression experiments further showed that <i>AsZIP2</i> encoded a functional plasma membrane-localized transporter that mediated Zn uptake in yeast. Moreover, overexpression of <i>AsZIP2</i> in <i>A. sinicus</i> resulted in the over-accumulation of Zn concentration in roots at low Pi or excessive Zn concentrations, whereas <i>AsZIP2</i> silencing lines displayed an even more reduced Zn concentration than control lines under such conditions. Our results reveal that the AsZIP2 transporter functioned in Zn over-accumulation in roots during Pi starvation or high Zn supply but was repressed by AM symbiosis in a Pi-dependent manner. These findings also provide new insights into the <i>AsZIP2</i> gene acting in the regulation of Zn homeostasis in mycorrhizal plants through Pi signal.https://www.mdpi.com/2309-608X/7/11/892Zincphosphatearbuscular mycorrhizal fungi<i>Astragalus sinicus</i><i>ZIP</i> gene familyAsZIP2 transporter
spellingShingle Xianan Xie
Xiaoning Fan
Hui Chen
Ming Tang
Phosphorus Starvation- and Zinc Excess-Induced <i>Astragalus sinicus</i> AsZIP2 Zinc Transporter Is Suppressed by Arbuscular Mycorrhizal Symbiosis
Journal of Fungi
Zinc
phosphate
arbuscular mycorrhizal fungi
<i>Astragalus sinicus</i>
<i>ZIP</i> gene family
AsZIP2 transporter
title Phosphorus Starvation- and Zinc Excess-Induced <i>Astragalus sinicus</i> AsZIP2 Zinc Transporter Is Suppressed by Arbuscular Mycorrhizal Symbiosis
title_full Phosphorus Starvation- and Zinc Excess-Induced <i>Astragalus sinicus</i> AsZIP2 Zinc Transporter Is Suppressed by Arbuscular Mycorrhizal Symbiosis
title_fullStr Phosphorus Starvation- and Zinc Excess-Induced <i>Astragalus sinicus</i> AsZIP2 Zinc Transporter Is Suppressed by Arbuscular Mycorrhizal Symbiosis
title_full_unstemmed Phosphorus Starvation- and Zinc Excess-Induced <i>Astragalus sinicus</i> AsZIP2 Zinc Transporter Is Suppressed by Arbuscular Mycorrhizal Symbiosis
title_short Phosphorus Starvation- and Zinc Excess-Induced <i>Astragalus sinicus</i> AsZIP2 Zinc Transporter Is Suppressed by Arbuscular Mycorrhizal Symbiosis
title_sort phosphorus starvation and zinc excess induced i astragalus sinicus i aszip2 zinc transporter is suppressed by arbuscular mycorrhizal symbiosis
topic Zinc
phosphate
arbuscular mycorrhizal fungi
<i>Astragalus sinicus</i>
<i>ZIP</i> gene family
AsZIP2 transporter
url https://www.mdpi.com/2309-608X/7/11/892
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