| Peer-Reviewed

Phytotoxicity and Iron Homeostasis Disturbance of Bismuth on IRT1 Promoter Knockout Arabidopsis thaliana

Published in Plant (Volume 9, Issue 3)
Received: 16 July 2021    Accepted: 28 July 2021    Published: 4 August 2021
Views:       Downloads:
Abstract

Bismuth (Bi) is used in semiconductors and water pipes as a substitute for lead. The Bi concentration in the soil has not been investigated, and there is no environmental quality standard for Bi in Japan. We previously reported Bi accumulation and phytotoxicity in Arabidopsis thaliana (A. thaliana) and Solanum lycopersicum, which were presented that Bi disturb iron (Fe) homeostasis in both plants. However, the mechanism of Bi phytotoxicity remains unclear. We examined the toxic effect of Bi for the expression of Fe-related genes in A. thaliana. The microarray analysis revealed an increase of the Fe regulation cascade including the subgroup Ib transcription factor. We tried to clear the effect to Fe homeostasis using the Iron-Regulated Transporter 1 (IRT1) promoter knockout line. Bi inhibits the root growth and lateral root development, while Bi induces Fe contents. In wild type, Fe was located in the stem cell niche (SCN) without Bi condition. Fe location in IRT1 promoter knockout line was disturbed by 2 µM Bi treatment. Moreover, the cell death in root was found in 2 µM Bi treated-roots. These results suggest that Bi disturbed the Fe homeostasis, Fe overaccumulation enhanced cell death in A. thaliana, and Bi damaged SCN in the root tip.

Published in Plant (Volume 9, Issue 3)
DOI 10.11648/j.plant.20210903.12
Page(s) 48-57
Creative Commons

This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited.

Copyright

Copyright © The Author(s), 2021. Published by Science Publishing Group

Keywords

Bismuth (Bi), Iron (Fe), Iron-Regulated Transporter 1 (IRT1), Stem Cell Niche (SCN), Quiescent Center (QC)

References
[1] The Japanese Pharmacopoeia 17th, Jihou-sha (2016).
[2] Srinarong C, Siramolpiwat S, Wongcha-Um A, Mahachai V, Vilaichone RK (2014) Improved Eradication Rate of Standard Triple Therapy by Adding Bismuth and Probiotic Supplement for Helicobacter pylori Treatment in Thailand. Asian Pac J Cancer Prev 15: 9909-9913.
[3] Shanika LGT, Jayamanne S, Wijekoon CN, Coombes J, Perera D, Mohamed F, Coombes I, De Silva HA, Dawson AH (2018) Ward-based clinical pharmacists and hospital readmission: a non-randomized controlled trial in Sri Lanka. Bull World Health Organ 96: 155-164.
[4] Kubota M, Asami T, Matsuki M (1988) Antimony and bismuth concentrations in the paddy soils and the river sediments polluted by cadmium in Nanakai-mura, Ibraki-ken, Japan. J Society Soil Sci Plant Nutr 59: 614-616 (in Japanese).
[5] Kubota M, Asami T, Matsuki M, Kashimura A (1990) Soil pollution by bismuth and the related heavy metals discharged from a bismuth smelter. J Society Soil Sci Plant Nutr 61: 190-192 (in Japanese).
[6] Li X, Thornton I (1993) Arsenic, antimony and bismuth in soil and pasture herbage in some old metalliferous mining areas in England. Environ Geochem Health 15: 135-144.
[7] Machado RC, Amaral CDB, Nóbrega JA, Araujo Nogueira AR (2017) Multielemental determination of As, Bi, Ge, Sb, and Sn in agricultural samples using hydride generation coupled to microwave-induced plasma optical emission spectrometry. J Agric Food Chem 14: 4839-4842.
[8] Liman R (2013) Genotoxic effects of bismuth (III) oxide nanoparticles by allium and comet assay. Chemosphere 93: 269-73.
[9] Nagata T (2015) Growth inhibition and IRT1 induction of Arabidopsis thaliana in response to bismuth. J Plant Biol 58: 311-371.
[10] Nagata T, Kimoto S (2020) Growth inhibition and root damage of bismuth in Solanum lycopersicum. SCIREA J of Biol 54: 72-86.
[11] Vert G, Grotz N, Dédaldéchamp F, Gaymard F, Guerinot ML, Briat JF, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14: 1223–1233.
[12] Halliwell B, Gutteridge JM (1992) Biologically relevant metal ion-dependent hydroxyl radical generation. An update. FEBS Lett 307: 108–112.
[13] Bashir K, Hanada K, Shimizu M, Seki M, Nakanishi H, Nishizawa NK (2014) Transcriptomic analysis of rice in response to iron deficiency and excess. Rice (NY) 7: 18.
[14] Hell R, Stephan UW (2003) Iron uptake, trafficking and homeostasis in plants. Planta 216: 541–551.
[15] Kim SA, LaCroix IS, Gerber SA, Guerinot ML (2019) The iron deficiency response in Arabidopsis thaliana requires the phosphorylated transcription factor URI. Proc Natl Acad Sci USA 116: 24933-24942.
[16] Zhang J, Liu B, Li M, Feng D, Jin H, Wang P, Liu J, Xiong F, Wang J, Wang HB (2015) The bHLH transcription factor bHLH104 interacts with IAA-LEUCINE RESISTANT3 and modulates iron homeostasis in Arabidopsis. Plant Cell 27: 787–805.
[17] Li X, Zhang H, Ai Q, Liang G, Yu D (2016) Two bHLH transcription factors, bHLH34 and bHLH104, regulate iron homeostasis in Arabidopsis thaliana. Plant Physiol 170, 2478–2493.
[18] Liang G, Zhang H, Li X, Ai Q, Yu D (2017) bHLH transcription factor bHLH115 regulates iron homeostasis in Arabidopsis thaliana. J. Exp. Bot 68, 1743–1755.
[19] Long TA, Tsukagoshi H, Busch W, Lahner B, Salt DE, Benfey PN (2010) The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell 22: 2219-2236.
[20] Selote D, Samira R, Matthiadis A, Gillikin JW, Long TA (2015) Iron-binding E3 ligase mediates iron response in plants by targeting basic helix-loop-helix transcription factors. Plant Physiol 167: 273-286.
[21] Yuan Y, Wu H, Wang N, Li J, Zhao W, Du J, Wang D, Ling HQ (2008) FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Res 18: 385–397.
[22] Wang N, Cui Y, Liu Y, Fan H, Du J, Huang Z, Yuan Y, Wu H, Ling HQ (2013) Requirement and functional redundancy of Ib subgroup bHLH proteins for iron deficiency responses and uptake in Arabidopsis thaliana. Mol Plant 6: 503–513.
[23] Dinneny JR, Benfey PN (2008) Plant stem cell niches: standing the test of time. Cell 132: 553-557.
[24] Di Mambro R, Sabatini S, Dello Ioio R (2018) Patterning the Axes: A Lesson from the Root. Plants (Basel) 8: 8.
[25] Müller J, Toev T, Heisters M, Teller J, Moore KL, Hause G, Dinesh DC, Bürstenbinder K, Abel S (2015) Iron-dependent callose deposition adjusts root meristem maintenance to phosphate availability Dev Cell 33: 216-230.
[26] Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol Plant 15: 473–497.
[27] Hasegawa J, Sakamoto Y, Nakagami S, Aida M, Sawa S, Matsunaga S (2016) Three-dimensional imaging of plant organs using a simple and rapid transparency technique. Plant Cell Physiol 57: 462-472.
[28] Nagata T, Morita H, Akizawa T, Pan-Hou H (2010) Development of a transgenic tobacco plant for phytoremediation of methylmercury pollution. Appl Microbiol Biotechnol 87: 781-786.
[29] Nagata T (2014) Expression analysis of new Metallothionein2-like protein under mercury stress in tomato seedling. Plant Root 8: 72-81.
[30] Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365–386.
[31] Cointry V, Vert G (2019) The bifunctional transporter-receptor IRT1 at the heart of metal sensing and signalling. New Phytol 223: 1173-1178.
[32] Sivitz AB, Hermand V, Curie C, Vert G (2012) Arabidopsis bHLH100 and bHLH101 control iron homeostasis via a FIT-independent pathway. PLoS One 7: e44843.
[33] Forouzesh E, Goel A, Mackenzie SA, Turner JA (2013) In vivo extraction of Arabidopsis cell turgor pressure using nanoindentation in conjunction with finite element modeling. Plant J 73: 509-520.
[34] Takahashi K, Hayashi K, Kinoshita T (2012) Auxin Activates the Plasma Membrane H+-ATPase by Phosphorylation during Hypocotyl Elongation in Arabidopsis. Plant Physiol 159: 632-641.
[35] Nishida S, Tsuzuki C, Kato A, Aisu A, Yoshida J, Mizuno T (2011) AtIRT1, the Primary Iron Uptake Transporter in the Root, Mediates Excess Nickel Accumulation in Arabidopsis thaliana. Plant Cell Physiol 52: 1433-1442.
[36] Huang W, Yang X, Yao S, LwinOo T, He H, Wang A, Li C, He L (2014) Reactive oxygen species burst induced by aluminum stress triggers mitochondria-dependent programmed cell death in peanut root tip cells. Plant Physiol Biochem 82: 76–84.
[37] Xu H, Xu W, Xi H, Ma W, He Z, Ma M (2013) The ER luminal binding protein (BiP) alleviates Cd2+-induced programmed cell death through endoplasmic reticulum stress-cell death signalling pathway in tobacco cells. J Plant Physiol 170: 1434–1441.
Cite This Article
  • APA Style

    Makoto Nishimura, Takeshi Nagata. (2021). Phytotoxicity and Iron Homeostasis Disturbance of Bismuth on IRT1 Promoter Knockout Arabidopsis thaliana. Plant, 9(3), 48-57. https://doi.org/10.11648/j.plant.20210903.12

    Copy | Download

    ACS Style

    Makoto Nishimura; Takeshi Nagata. Phytotoxicity and Iron Homeostasis Disturbance of Bismuth on IRT1 Promoter Knockout Arabidopsis thaliana. Plant. 2021, 9(3), 48-57. doi: 10.11648/j.plant.20210903.12

    Copy | Download

    AMA Style

    Makoto Nishimura, Takeshi Nagata. Phytotoxicity and Iron Homeostasis Disturbance of Bismuth on IRT1 Promoter Knockout Arabidopsis thaliana. Plant. 2021;9(3):48-57. doi: 10.11648/j.plant.20210903.12

    Copy | Download

  • @article{10.11648/j.plant.20210903.12,
      author = {Makoto Nishimura and Takeshi Nagata},
      title = {Phytotoxicity and Iron Homeostasis Disturbance of Bismuth on IRT1 Promoter Knockout Arabidopsis thaliana},
      journal = {Plant},
      volume = {9},
      number = {3},
      pages = {48-57},
      doi = {10.11648/j.plant.20210903.12},
      url = {https://doi.org/10.11648/j.plant.20210903.12},
      eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.plant.20210903.12},
      abstract = {Bismuth (Bi) is used in semiconductors and water pipes as a substitute for lead. The Bi concentration in the soil has not been investigated, and there is no environmental quality standard for Bi in Japan. We previously reported Bi accumulation and phytotoxicity in Arabidopsis thaliana (A. thaliana) and Solanum lycopersicum, which were presented that Bi disturb iron (Fe) homeostasis in both plants. However, the mechanism of Bi phytotoxicity remains unclear. We examined the toxic effect of Bi for the expression of Fe-related genes in A. thaliana. The microarray analysis revealed an increase of the Fe regulation cascade including the subgroup Ib transcription factor. We tried to clear the effect to Fe homeostasis using the Iron-Regulated Transporter 1 (IRT1) promoter knockout line. Bi inhibits the root growth and lateral root development, while Bi induces Fe contents. In wild type, Fe was located in the stem cell niche (SCN) without Bi condition. Fe location in IRT1 promoter knockout line was disturbed by 2 µM Bi treatment. Moreover, the cell death in root was found in 2 µM Bi treated-roots. These results suggest that Bi disturbed the Fe homeostasis, Fe overaccumulation enhanced cell death in A. thaliana, and Bi damaged SCN in the root tip.},
     year = {2021}
    }
    

    Copy | Download

  • TY  - JOUR
    T1  - Phytotoxicity and Iron Homeostasis Disturbance of Bismuth on IRT1 Promoter Knockout Arabidopsis thaliana
    AU  - Makoto Nishimura
    AU  - Takeshi Nagata
    Y1  - 2021/08/04
    PY  - 2021
    N1  - https://doi.org/10.11648/j.plant.20210903.12
    DO  - 10.11648/j.plant.20210903.12
    T2  - Plant
    JF  - Plant
    JO  - Plant
    SP  - 48
    EP  - 57
    PB  - Science Publishing Group
    SN  - 2331-0677
    UR  - https://doi.org/10.11648/j.plant.20210903.12
    AB  - Bismuth (Bi) is used in semiconductors and water pipes as a substitute for lead. The Bi concentration in the soil has not been investigated, and there is no environmental quality standard for Bi in Japan. We previously reported Bi accumulation and phytotoxicity in Arabidopsis thaliana (A. thaliana) and Solanum lycopersicum, which were presented that Bi disturb iron (Fe) homeostasis in both plants. However, the mechanism of Bi phytotoxicity remains unclear. We examined the toxic effect of Bi for the expression of Fe-related genes in A. thaliana. The microarray analysis revealed an increase of the Fe regulation cascade including the subgroup Ib transcription factor. We tried to clear the effect to Fe homeostasis using the Iron-Regulated Transporter 1 (IRT1) promoter knockout line. Bi inhibits the root growth and lateral root development, while Bi induces Fe contents. In wild type, Fe was located in the stem cell niche (SCN) without Bi condition. Fe location in IRT1 promoter knockout line was disturbed by 2 µM Bi treatment. Moreover, the cell death in root was found in 2 µM Bi treated-roots. These results suggest that Bi disturbed the Fe homeostasis, Fe overaccumulation enhanced cell death in A. thaliana, and Bi damaged SCN in the root tip.
    VL  - 9
    IS  - 3
    ER  - 

    Copy | Download

Author Information
  • Department of Life Science, Setsunan University, Osaka, Japan

  • Department of Life Science, Setsunan University, Osaka, Japan

  • Sections