Arabidopsis Glutaredoxin S17 Contributes to Vegetative Growth, Mineral Accumulation, and Redox Balance during Iron Deficiency

Iron (Fe) is an essential mineral nutrient and a metal cofactor required for many proteins and enzymes involved in the processes of DNA synthesis, respiration, and photosynthesis. Iron limitation can have detrimental effects on plant growth and development. Such effects are mediated, at least in par...

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Main Authors: Han Yu, Jian Yang, Yafei Shi, Jimmonique Donelson, Sean M. Thompson, Stuart Sprague, Tony Roshan, Da-Li Wang, Jianzhong Liu, Sunghun Park, Paul A. Nakata, Erin L. Connolly, Kendal D. Hirschi, Michael A. Grusak, Ninghui Cheng
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-06-01
Series:Frontiers in Plant Science
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Online Access:http://journal.frontiersin.org/article/10.3389/fpls.2017.01045/full
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author Han Yu
Jian Yang
Yafei Shi
Jimmonique Donelson
Sean M. Thompson
Stuart Sprague
Tony Roshan
Da-Li Wang
Jianzhong Liu
Sunghun Park
Paul A. Nakata
Erin L. Connolly
Kendal D. Hirschi
Kendal D. Hirschi
Michael A. Grusak
Michael A. Grusak
Ninghui Cheng
author_facet Han Yu
Jian Yang
Yafei Shi
Jimmonique Donelson
Sean M. Thompson
Stuart Sprague
Tony Roshan
Da-Li Wang
Jianzhong Liu
Sunghun Park
Paul A. Nakata
Erin L. Connolly
Kendal D. Hirschi
Kendal D. Hirschi
Michael A. Grusak
Michael A. Grusak
Ninghui Cheng
author_sort Han Yu
collection DOAJ
description Iron (Fe) is an essential mineral nutrient and a metal cofactor required for many proteins and enzymes involved in the processes of DNA synthesis, respiration, and photosynthesis. Iron limitation can have detrimental effects on plant growth and development. Such effects are mediated, at least in part, through the generation of reactive oxygen species (ROS). Thus, plants have evolved a complex regulatory network to respond to conditions of iron limitations. However, the mechanisms that couple iron deficiency and oxidative stress responses are not fully understood. Here, we report the discovery that an Arabidopsis thaliana monothiol glutaredoxin S17 (AtGRXS17) plays a critical role in the plants ability to respond to iron deficiency stress and maintain redox homeostasis. In a yeast expression assay, AtGRXS17 was able to suppress the iron accumulation in yeast ScGrx3/ScGrx4 mutant cells. Genetic analysis indicated that plants with reduced AtGRXS17 expression were hypersensitive to iron deficiency and showed increased iron concentrations in mature seeds. Disruption of AtGRXS17 caused plant sensitivity to exogenous oxidants and increased ROS production under iron deficiency. Addition of reduced glutathione rescued the growth and alleviates the sensitivity of atgrxs17 mutants to iron deficiency. These findings suggest AtGRXS17 helps integrate redox homeostasis and iron deficiency responses.
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spelling doaj.art-795664211d074398bdd22ccd84d284462022-12-21T23:51:59ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2017-06-01810.3389/fpls.2017.01045274897Arabidopsis Glutaredoxin S17 Contributes to Vegetative Growth, Mineral Accumulation, and Redox Balance during Iron DeficiencyHan Yu0Jian Yang1Yafei Shi2Jimmonique Donelson3Sean M. Thompson4Stuart Sprague5Tony Roshan6Da-Li Wang7Jianzhong Liu8Sunghun Park9Paul A. Nakata10Erin L. Connolly11Kendal D. Hirschi12Kendal D. Hirschi13Michael A. Grusak14Michael A. Grusak15Ninghui Cheng16USDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, HoustonTX, United StatesUSDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, HoustonTX, United StatesCollege of Chemistry and Life Science, Zhejiang Normal UniversityJinhua, ChinaUSDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, HoustonTX, United StatesDepartment of Horticultural Sciences, Texas A&M University, College StationTX, United StatesDepartment of Horticulture, Forestry and Recreation Resources, Kansas State University, ManhattanKS, United StatesUSDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, HoustonTX, United StatesCollege of Chemistry and Life Science, Zhejiang Normal UniversityJinhua, ChinaCollege of Chemistry and Life Science, Zhejiang Normal UniversityJinhua, ChinaDepartment of Horticulture, Forestry and Recreation Resources, Kansas State University, ManhattanKS, United StatesUSDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, HoustonTX, United StatesDepartment of Plant Science, Penn State University, University ParkPA, United StatesUSDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, HoustonTX, United StatesVegetable and Fruit Improvement Center, Texas A&M University, College StationTX, United StatesUSDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, HoustonTX, United StatesUSDA/ARS Red River Valley Agricultural Research Center, FargoND, United StatesUSDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, HoustonTX, United StatesIron (Fe) is an essential mineral nutrient and a metal cofactor required for many proteins and enzymes involved in the processes of DNA synthesis, respiration, and photosynthesis. Iron limitation can have detrimental effects on plant growth and development. Such effects are mediated, at least in part, through the generation of reactive oxygen species (ROS). Thus, plants have evolved a complex regulatory network to respond to conditions of iron limitations. However, the mechanisms that couple iron deficiency and oxidative stress responses are not fully understood. Here, we report the discovery that an Arabidopsis thaliana monothiol glutaredoxin S17 (AtGRXS17) plays a critical role in the plants ability to respond to iron deficiency stress and maintain redox homeostasis. In a yeast expression assay, AtGRXS17 was able to suppress the iron accumulation in yeast ScGrx3/ScGrx4 mutant cells. Genetic analysis indicated that plants with reduced AtGRXS17 expression were hypersensitive to iron deficiency and showed increased iron concentrations in mature seeds. Disruption of AtGRXS17 caused plant sensitivity to exogenous oxidants and increased ROS production under iron deficiency. Addition of reduced glutathione rescued the growth and alleviates the sensitivity of atgrxs17 mutants to iron deficiency. These findings suggest AtGRXS17 helps integrate redox homeostasis and iron deficiency responses.http://journal.frontiersin.org/article/10.3389/fpls.2017.01045/fulliron deficiencyoxidative stressredox homeostasisglutaredoxinArabidopsis
spellingShingle Han Yu
Jian Yang
Yafei Shi
Jimmonique Donelson
Sean M. Thompson
Stuart Sprague
Tony Roshan
Da-Li Wang
Jianzhong Liu
Sunghun Park
Paul A. Nakata
Erin L. Connolly
Kendal D. Hirschi
Kendal D. Hirschi
Michael A. Grusak
Michael A. Grusak
Ninghui Cheng
Arabidopsis Glutaredoxin S17 Contributes to Vegetative Growth, Mineral Accumulation, and Redox Balance during Iron Deficiency
Frontiers in Plant Science
iron deficiency
oxidative stress
redox homeostasis
glutaredoxin
Arabidopsis
title Arabidopsis Glutaredoxin S17 Contributes to Vegetative Growth, Mineral Accumulation, and Redox Balance during Iron Deficiency
title_full Arabidopsis Glutaredoxin S17 Contributes to Vegetative Growth, Mineral Accumulation, and Redox Balance during Iron Deficiency
title_fullStr Arabidopsis Glutaredoxin S17 Contributes to Vegetative Growth, Mineral Accumulation, and Redox Balance during Iron Deficiency
title_full_unstemmed Arabidopsis Glutaredoxin S17 Contributes to Vegetative Growth, Mineral Accumulation, and Redox Balance during Iron Deficiency
title_short Arabidopsis Glutaredoxin S17 Contributes to Vegetative Growth, Mineral Accumulation, and Redox Balance during Iron Deficiency
title_sort arabidopsis glutaredoxin s17 contributes to vegetative growth mineral accumulation and redox balance during iron deficiency
topic iron deficiency
oxidative stress
redox homeostasis
glutaredoxin
Arabidopsis
url http://journal.frontiersin.org/article/10.3389/fpls.2017.01045/full
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