PIN FORMED 2 Modulates the Transport of Arsenite in Arabidopsis thaliana

Ashraf, Mohammad Arif; Umetsu, Kana; Ponomarenko, Olena; Saito, Michiko; Aslam, Mohammad; Antipova, Olga; Dolgova, Natalia; Kiani, Cheyenne D.; Nehzati, Susan; Tanoi, Keitaro; Minegishi, Katsuyuki; Nagatsu, Kotaro; Kamiya, Takehiro; Fujiwara, Toru; Luschnig, Christian; Tanino, Karen; Pickering, Ingrid; George, Graham N.; Rahman, Abidur

doi:10.1016/j.xplc.2019.100009

Title: PIN FORMED 2 Modulates the Transport of Arsenite in Arabidopsis thaliana

Abstract

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 othermore »« less

Publication Date:: Fri May 01 00:00:00 EDT 2020

Research Org.:: Argonne National Lab. (ANL), Argonne, IL (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:: 1581466

Alternate Identifier(s):: OSTI ID: 1668068

Grant/Contract Number:: AC02-06CH11357

Resource Type:: Published Article

Journal Name:: Plant Communications

Additional Journal Information:: Journal Name: Plant Communications Journal Volume: 1 Journal Issue: 3; Journal ID: ISSN 2590-3462

Publisher:: Elsevier

Country of Publication:: Country unknown/Code not available

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; Arsenic; X-ray Fluorescence Microscopy; plant root imaging

Citation Formats


                    Ashraf, Mohammad Arif, Umetsu, Kana, Ponomarenko, Olena, Saito, Michiko, Aslam, Mohammad, Antipova, Olga, Dolgova, Natalia, Kiani, Cheyenne D., Nehzati, Susan, Tanoi, Keitaro, Minegishi, Katsuyuki, Nagatsu, Kotaro, Kamiya, Takehiro, Fujiwara, Toru, Luschnig, Christian, Tanino, Karen, Pickering, Ingrid, George, Graham N., and Rahman, Abidur. PIN FORMED 2 Modulates the Transport of Arsenite in Arabidopsis thaliana.  Country unknown/Code not available: N. p., 2020. 
Web.  doi:10.1016/j.xplc.2019.100009.

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                    Ashraf, Mohammad Arif, Umetsu, Kana, Ponomarenko, Olena, Saito, Michiko, Aslam, Mohammad, Antipova, Olga, Dolgova, Natalia, Kiani, Cheyenne D., Nehzati, Susan, Tanoi, Keitaro, Minegishi, Katsuyuki, Nagatsu, Kotaro, Kamiya, Takehiro, Fujiwara, Toru, Luschnig, Christian, Tanino, Karen, Pickering, Ingrid, George, Graham N., & Rahman, Abidur. PIN FORMED 2 Modulates the Transport of Arsenite in Arabidopsis thaliana.  Country unknown/Code not available.  https://doi.org/10.1016/j.xplc.2019.100009

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                    Ashraf, Mohammad Arif, Umetsu, Kana, Ponomarenko, Olena, Saito, Michiko, Aslam, Mohammad, Antipova, Olga, Dolgova, Natalia, Kiani, Cheyenne D., Nehzati, Susan, Tanoi, Keitaro, Minegishi, Katsuyuki, Nagatsu, Kotaro, Kamiya, Takehiro, Fujiwara, Toru, Luschnig, Christian, Tanino, Karen, Pickering, Ingrid, George, Graham N., and Rahman, Abidur. Fri .  
"PIN FORMED 2 Modulates the Transport of Arsenite in Arabidopsis thaliana".  Country unknown/Code not available.  https://doi.org/10.1016/j.xplc.2019.100009.

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@article{osti_1581466,

  title        = {PIN FORMED 2 Modulates the Transport of Arsenite in Arabidopsis thaliana},

  author       = {Ashraf, Mohammad Arif and Umetsu, Kana and Ponomarenko, Olena and Saito, Michiko and Aslam, Mohammad and Antipova, Olga and Dolgova, Natalia and Kiani, Cheyenne D. and Nehzati, Susan and Tanoi, Keitaro and Minegishi, Katsuyuki and Nagatsu, Kotaro and Kamiya, Takehiro and Fujiwara, Toru and Luschnig, Christian and Tanino, Karen and Pickering, Ingrid and George, Graham N. and Rahman, Abidur},

  abstractNote = {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.},

  doi          = {10.1016/j.xplc.2019.100009},

  journal      = {Plant Communications},

  number       = 3,

  volume       = 1,

  place        = {Country unknown/Code not available},

  year         = {Fri May 01 00:00:00 EDT 2020},

  month        = {Fri May 01 00:00:00 EDT 2020}

}

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Figures / Tables:

Table 1: Homology of Plant Auxin Efflux Carrier (PINs) and Arsenite Transporters. Identity matrix of Saccharomyces cerevisiae Acr3 (SsAcr3), Pteris vittataAcr3 (PvAcr3) and Escherichia coli arsenite transporter (arsB), Oryza sativa silicon transporter (OsLsi2), and Arabidopsis thaliana PINs (AtPIN1, AtPIN2, AtPIN3).

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