SgNramp1, a plasma membrane-localized transporter, involves in manganese uptake in Stylosanthes guianensis

Transporters belonging to the natural resistance-associated macrophage protein (Nramp) family play important roles in metal uptake and homeostasis. Although Nramp members have been functionally characterized in plants, the role of Nramp in the important tropical forage legume Stylosanthes guianensis...

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Main Authors: Xiaoyan Zou, Rui Huang, Linjie Wang, Guihua Wang, Ye Miao, Idupulapati Rao, Guodao Liu, Zhijian Chen
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-10-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.1027551/full
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author Xiaoyan Zou
Xiaoyan Zou
Rui Huang
Linjie Wang
Linjie Wang
Guihua Wang
Ye Miao
Ye Miao
Idupulapati Rao
Guodao Liu
Zhijian Chen
Zhijian Chen
author_facet Xiaoyan Zou
Xiaoyan Zou
Rui Huang
Linjie Wang
Linjie Wang
Guihua Wang
Ye Miao
Ye Miao
Idupulapati Rao
Guodao Liu
Zhijian Chen
Zhijian Chen
author_sort Xiaoyan Zou
collection DOAJ
description Transporters belonging to the natural resistance-associated macrophage protein (Nramp) family play important roles in metal uptake and homeostasis. Although Nramp members have been functionally characterized in plants, the role of Nramp in the important tropical forage legume Stylosanthes guianensis (stylo) is largely unknown. This study aimed to determine the responses of Nramp genes to metal stresses and investigate its metal transport activity in stylo. Five SgNramp genes were identified from stylo. Expression analysis showed that SgNramp genes exhibited tissue preferential expressions and diverse responses to metal stresses, especially for manganese (Mn), suggesting the involvement of SgNramps in the response of stylo to metal stresses. Of the five SgNramps, SgNramp1 displayed the highest expression in stylo roots. A close correlation between SgNramp1 expression and root Mn concentration was observed among nine stylo cultivars under Mn limited condition. The higher expression of SgNramp1 was correlated with a high Mn uptake in stylo. Subsequent subcellular localization analysis showed that SgNramp1 was localized to the plasma membrane. Furthermore, heterologous expression of SgNramp1 complemented the phenotype of the Mn uptake-defective yeast (Saccharomyces cerevisiae) mutant Δsmf1. Mn concentration in the yeast cells expressing SgNramp1 was higher than that of the empty vector control, suggesting the transport activity of SgNramp1 for Mn in yeast. Taken together, this study reveals that SgNramp1 is a plasma membrane–localized transporter responsible for Mn uptake in stylo.
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spelling doaj.art-420c20a25c45400cb276ace22e8b21aa2022-12-22T03:54:36ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-10-011310.3389/fpls.2022.10275511027551SgNramp1, a plasma membrane-localized transporter, involves in manganese uptake in Stylosanthes guianensisXiaoyan Zou0Xiaoyan Zou1Rui Huang2Linjie Wang3Linjie Wang4Guihua Wang5Ye Miao6Ye Miao7Idupulapati Rao8Guodao Liu9Zhijian Chen10Zhijian Chen11Key Laboratory of Tropical Crops Germplasm Resources Genetic Improvement and Innovation of Hainan Province, Institute of Tropical Crop Genetic Resources, Chinese Academy of Tropical Agricultural Sciences, Haikou, ChinaCollege of Tropical Crops, Hainan University, Haikou, ChinaKey Laboratory of Tropical Crops Germplasm Resources Genetic Improvement and Innovation of Hainan Province, Institute of Tropical Crop Genetic Resources, Chinese Academy of Tropical Agricultural Sciences, Haikou, ChinaKey Laboratory of Tropical Crops Germplasm Resources Genetic Improvement and Innovation of Hainan Province, Institute of Tropical Crop Genetic Resources, Chinese Academy of Tropical Agricultural Sciences, Haikou, ChinaCollege of Tropical Crops, Hainan University, Haikou, ChinaRubber Research Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, ChinaKey Laboratory of Tropical Crops Germplasm Resources Genetic Improvement and Innovation of Hainan Province, Institute of Tropical Crop Genetic Resources, Chinese Academy of Tropical Agricultural Sciences, Haikou, ChinaCollege of Tropical Crops, Hainan University, Haikou, ChinaCrops for Nutrition and Health, Alliance of Bioversity International and International Center for Tropical Agriculture, Cali, ColombiaKey Laboratory of Tropical Crops Germplasm Resources Genetic Improvement and Innovation of Hainan Province, Institute of Tropical Crop Genetic Resources, Chinese Academy of Tropical Agricultural Sciences, Haikou, ChinaKey Laboratory of Tropical Crops Germplasm Resources Genetic Improvement and Innovation of Hainan Province, Institute of Tropical Crop Genetic Resources, Chinese Academy of Tropical Agricultural Sciences, Haikou, ChinaCollege of Tropical Crops, Hainan University, Haikou, ChinaTransporters belonging to the natural resistance-associated macrophage protein (Nramp) family play important roles in metal uptake and homeostasis. Although Nramp members have been functionally characterized in plants, the role of Nramp in the important tropical forage legume Stylosanthes guianensis (stylo) is largely unknown. This study aimed to determine the responses of Nramp genes to metal stresses and investigate its metal transport activity in stylo. Five SgNramp genes were identified from stylo. Expression analysis showed that SgNramp genes exhibited tissue preferential expressions and diverse responses to metal stresses, especially for manganese (Mn), suggesting the involvement of SgNramps in the response of stylo to metal stresses. Of the five SgNramps, SgNramp1 displayed the highest expression in stylo roots. A close correlation between SgNramp1 expression and root Mn concentration was observed among nine stylo cultivars under Mn limited condition. The higher expression of SgNramp1 was correlated with a high Mn uptake in stylo. Subsequent subcellular localization analysis showed that SgNramp1 was localized to the plasma membrane. Furthermore, heterologous expression of SgNramp1 complemented the phenotype of the Mn uptake-defective yeast (Saccharomyces cerevisiae) mutant Δsmf1. Mn concentration in the yeast cells expressing SgNramp1 was higher than that of the empty vector control, suggesting the transport activity of SgNramp1 for Mn in yeast. Taken together, this study reveals that SgNramp1 is a plasma membrane–localized transporter responsible for Mn uptake in stylo.https://www.frontiersin.org/articles/10.3389/fpls.2022.1027551/fullnramptrace metalmetal homeostasisgene expressionsubcellular localization
spellingShingle Xiaoyan Zou
Xiaoyan Zou
Rui Huang
Linjie Wang
Linjie Wang
Guihua Wang
Ye Miao
Ye Miao
Idupulapati Rao
Guodao Liu
Zhijian Chen
Zhijian Chen
SgNramp1, a plasma membrane-localized transporter, involves in manganese uptake in Stylosanthes guianensis
Frontiers in Plant Science
nramp
trace metal
metal homeostasis
gene expression
subcellular localization
title SgNramp1, a plasma membrane-localized transporter, involves in manganese uptake in Stylosanthes guianensis
title_full SgNramp1, a plasma membrane-localized transporter, involves in manganese uptake in Stylosanthes guianensis
title_fullStr SgNramp1, a plasma membrane-localized transporter, involves in manganese uptake in Stylosanthes guianensis
title_full_unstemmed SgNramp1, a plasma membrane-localized transporter, involves in manganese uptake in Stylosanthes guianensis
title_short SgNramp1, a plasma membrane-localized transporter, involves in manganese uptake in Stylosanthes guianensis
title_sort sgnramp1 a plasma membrane localized transporter involves in manganese uptake in stylosanthes guianensis
topic nramp
trace metal
metal homeostasis
gene expression
subcellular localization
url https://www.frontiersin.org/articles/10.3389/fpls.2022.1027551/full
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