PIN FORMED 2 Modulates the Transport of Arsenite in Arabidopsis thaliana
Arsenic contamination is a major environmental issue, as it may lead to serious health hazard. The reduced trivalent form of inorganic arsenic, arsenite, is in general more toxic to plants compared with the fully oxidized pentavalent arsenate. The uptake of arsenite in plants has been shown to be me...
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Format: | Article |
Language: | English |
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Elsevier
2020-05-01
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Series: | Plant Communications |
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Online Access: | http://www.sciencedirect.com/science/article/pii/S2590346219300094 |
id |
doaj-5d42e4d507a741ffb01f6dc1c78d4ea4 |
---|---|
record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Mohammad Arif Ashraf Kana Umetsu Olena Ponomarenko Michiko Saito Mohammad Aslam Olga Antipova Natalia Dolgova Cheyenne D. Kiani Susan Nehzati Keitaro Tanoi Katsuyuki Minegishi Kotaro Nagatsu Takehiro Kamiya Toru Fujiwara Christian Luschnig Karen Tanino Ingrid Pickering Graham N. George Abidur Rahman |
spellingShingle |
Mohammad Arif Ashraf Kana Umetsu Olena Ponomarenko Michiko Saito Mohammad Aslam Olga Antipova Natalia Dolgova Cheyenne D. Kiani Susan Nehzati Keitaro Tanoi Katsuyuki Minegishi Kotaro Nagatsu Takehiro Kamiya Toru Fujiwara Christian Luschnig Karen Tanino Ingrid Pickering Graham N. George Abidur Rahman PIN FORMED 2 Modulates the Transport of Arsenite in Arabidopsis thaliana Plant Communications auxin arsenite PIN2 trafficking transport |
author_facet |
Mohammad Arif Ashraf Kana Umetsu Olena Ponomarenko Michiko Saito Mohammad Aslam Olga Antipova Natalia Dolgova Cheyenne D. Kiani Susan Nehzati Keitaro Tanoi Katsuyuki Minegishi Kotaro Nagatsu Takehiro Kamiya Toru Fujiwara Christian Luschnig Karen Tanino Ingrid Pickering Graham N. George Abidur Rahman |
author_sort |
Mohammad Arif Ashraf |
title |
PIN FORMED 2 Modulates the Transport of Arsenite in Arabidopsis thaliana |
title_short |
PIN FORMED 2 Modulates the Transport of Arsenite in Arabidopsis thaliana |
title_full |
PIN FORMED 2 Modulates the Transport of Arsenite in Arabidopsis thaliana |
title_fullStr |
PIN FORMED 2 Modulates the Transport of Arsenite in Arabidopsis thaliana |
title_full_unstemmed |
PIN FORMED 2 Modulates the Transport of Arsenite in Arabidopsis thaliana |
title_sort |
pin formed 2 modulates the transport of arsenite in arabidopsis thaliana |
publisher |
Elsevier |
series |
Plant Communications |
issn |
2590-3462 |
publishDate |
2020-05-01 |
description |
Arsenic contamination is a major environmental issue, as it may lead to serious health hazard. The reduced trivalent form of inorganic arsenic, arsenite, is in general more toxic to plants compared with the fully oxidized pentavalent arsenate. The uptake of arsenite in plants has been shown to be mediated through a large subfamily of plant aquaglyceroporins, nodulin 26-like intrinsic proteins (NIPs). However, the efflux mechanisms, as well as the mechanism of arsenite-induced root growth inhibition, remain poorly understood. Using molecular physiology, synchrotron imaging, and root transport assay approaches, we show that the cellular transport of trivalent arsenicals in Arabidopsis thaliana is strongly modulated by PIN FORMED 2 (PIN2) auxin efflux transporter. Root transport assay using radioactive arsenite, X-ray fluorescence imaging (XFI) coupled with X-ray absorption spectroscopy (XAS), and inductively coupled plasma mass spectrometry analysis revealed that pin2 plants accumulate higher concentrations of arsenite in roots compared with the wild-type. At the cellular level, arsenite specifically targets intracellular sorting of PIN2 and thereby alters the cellular auxin homeostasis. Consistently, loss of PIN2 function results in arsenite hypersensitivity in roots. XFI coupled with XAS further revealed that loss of PIN2 function results in specific accumulation of arsenical species, but not the other metals such as iron, zinc, or calcium in the root tip. Collectively, these results suggest that PIN2 likely functions as an arsenite efflux transporter for the distribution of arsenical species in planta. |
topic |
auxin arsenite PIN2 trafficking transport |
url |
http://www.sciencedirect.com/science/article/pii/S2590346219300094 |
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doaj-5d42e4d507a741ffb01f6dc1c78d4ea42020-11-25T03:51:00ZengElsevierPlant Communications2590-34622020-05-0113PIN FORMED 2 Modulates the Transport of Arsenite in Arabidopsis thalianaMohammad Arif Ashraf0Kana Umetsu1Olena Ponomarenko2Michiko Saito3Mohammad Aslam4Olga Antipova5Natalia Dolgova6Cheyenne D. Kiani7Susan Nehzati8Keitaro Tanoi9Katsuyuki Minegishi10Kotaro Nagatsu11Takehiro Kamiya12Toru Fujiwara13Christian Luschnig14Karen Tanino15Ingrid Pickering16Graham N. George17Abidur Rahman18United Graduate School of Agricultural Sciences, Iwate University, Morioka, Iwate, JapanDepartment of Plant Bio Sciences, Faculty of Agriculture, Iwate University, Morioka, Iwate, JapanMolecular and Environmental Science Research Group, Department of Geological Sciences, University of Saskatchewan, Saskatoon, SK, CanadaDepartment of Plant Bio Sciences, Faculty of Agriculture, Iwate University, Morioka, Iwate, JapanDepartment of Plant Bio Sciences, Faculty of Agriculture, Iwate University, Morioka, Iwate, JapanArgonne National Lab, Advanced Photon Source, XSD-MIC, Lemont, IL, USAMolecular and Environmental Science Research Group, Department of Geological Sciences, University of Saskatchewan, Saskatoon, SK, CanadaMolecular and Environmental Science Research Group, Department of Geological Sciences, University of Saskatchewan, Saskatoon, SK, CanadaMolecular and Environmental Science Research Group, Department of Geological Sciences, University of Saskatchewan, Saskatoon, SK, CanadaIsotope Facility for Agricultural Education and Research, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo, JapanDepartment of Radiopharmaceuticals Development, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Inage, Chiba, JapanDepartment of Radiopharmaceuticals Development, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Inage, Chiba, JapanDepartment of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo, JapanDepartment of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo, JapanDepartment of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Vienna (BOKU), Muthgasse 18, 1180 Wien, AustriaDepartment of Plant Sciences, College of Agriculture and Bioresources, University of Saskatchewan, Saskatoon, SK, CanadaMolecular and Environmental Science Research Group, Department of Geological Sciences, University of Saskatchewan, Saskatoon, SK, CanadaMolecular and Environmental Science Research Group, Department of Geological Sciences, University of Saskatchewan, Saskatoon, SK, CanadaUnited Graduate School of Agricultural Sciences, Iwate University, Morioka, Iwate, Japan; Department of Plant Bio Sciences, Faculty of Agriculture, Iwate University, Morioka, Iwate, Japan; Agri-Innovation Center, Iwate University, Morioka, Iwate, Japan; Corresponding authorArsenic contamination is a major environmental issue, as it may lead to serious health hazard. The reduced trivalent form of inorganic arsenic, arsenite, is in general more toxic to plants compared with the fully oxidized pentavalent arsenate. The uptake of arsenite in plants has been shown to be mediated through a large subfamily of plant aquaglyceroporins, nodulin 26-like intrinsic proteins (NIPs). However, the efflux mechanisms, as well as the mechanism of arsenite-induced root growth inhibition, remain poorly understood. Using molecular physiology, synchrotron imaging, and root transport assay approaches, we show that the cellular transport of trivalent arsenicals in Arabidopsis thaliana is strongly modulated by PIN FORMED 2 (PIN2) auxin efflux transporter. Root transport assay using radioactive arsenite, X-ray fluorescence imaging (XFI) coupled with X-ray absorption spectroscopy (XAS), and inductively coupled plasma mass spectrometry analysis revealed that pin2 plants accumulate higher concentrations of arsenite in roots compared with the wild-type. At the cellular level, arsenite specifically targets intracellular sorting of PIN2 and thereby alters the cellular auxin homeostasis. Consistently, loss of PIN2 function results in arsenite hypersensitivity in roots. XFI coupled with XAS further revealed that loss of PIN2 function results in specific accumulation of arsenical species, but not the other metals such as iron, zinc, or calcium in the root tip. Collectively, these results suggest that PIN2 likely functions as an arsenite efflux transporter for the distribution of arsenical species in planta.http://www.sciencedirect.com/science/article/pii/S2590346219300094auxinarsenitePIN2traffickingtransport |