Skip to main content
SpringerLink
Log in

Members of rice plasma membrane intrinsic proteins subfamily are involved in arsenite permeability and tolerance in plants

  • Original Paper
  • Published:
Transgenic Research Aims and scope Submit manuscript

Abstract

Rice accumulates high level of arsenic (As) in its edible parts and thus plays an important role in the transfer of As into the food chain. However, the mechanisms of As uptake and its detoxification in rice are not well understood. Recently, members of the Nodulin 26-like intrinsic protein (NIP) subfamily of plant aquaporins were shown to transport arsenite in rice and Arabidopsis. Here we report that members of the rice plasma membrane intrinsic protein (PIP) subfamily are also involved in As tolerance and transport. Based on the homology search with the mammalian AQP9 and yeast Fps1 arsenite transporters, we identified and cloned five rice PIP gene subfamily members. qRT-PCR analysis of PIPs in rice root and shoot tissues revealed a significant down regulation of transcripts encoding OsPIP1;2, OsPIP1;3, OsPIP2;4, OsPIP2;6, and OsPIP2;7 in response to arsenite treatment. Heterologous expression of OsPIP2;4, OsPIP2;6, and OsPIP2;7 in Xenopus laevis oocytes significantly increased the uptake of arsenite. Overexpression of OsPIP2;4, OsPIP2;6, and OsPIP2;7 in Arabidopsis yielded enhanced arsenite tolerance and higher biomass accumulation. Further, these transgenic plants showed no significant accumulation of As in shoot and root tissues in long term uptake assays. Whereas, short duration exposure to arsenite caused both active influx and efflux of As in the roots. The data suggests a bidirectional arsenite permeability of rice PIPs in plants. These rice PIPs genes will be highly useful for engineering important food and biofuel crops for enhanced crop productivity on contaminated soils without increasing the accumulation of toxic As in the biomass or edible tissues.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abedin MJ, Cotter-Howells J, Meharg AA (2002a) Arsenic uptake and accumulation in rice (oryza sativa L.) irrigated with contaminated water. Plant Soil 240(2):311–319

    Article  CAS  Google Scholar 

  • Abedin MJ, Cresser MS, Meharg AA, Feldmann J, Cotter-Howells J (2002b) Arsenic accumulation and metabolism in rice (oryza sativa L.). Environ Sci Technol 36(5):962–968

    Article  PubMed  CAS  Google Scholar 

  • Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y et al (2003) Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. Plant Cell 15(2):439–447

    Article  PubMed  CAS  Google Scholar 

  • Alexandersson E, Danielson JA, Rade J, Moparthi VK, Fontes M, Kjellbom P, Johanson U (2010) Transcriptional regulation of aquaporins in accessions of Arabidopsis in response to drought stress. Plant J 61(4):650–660

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Bechtold N, Pelletier G (1997) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Anonymous Arabidopsis Protocols, In, pp 259–266

    Google Scholar 

  • Bentley R, Chasteen TG (2002) Microbial methylation of metalloids: arsenic, antimony, and bismuth. Microbiol Mol Biol Rev 66(2):250–271

    Article  PubMed  CAS  Google Scholar 

  • Bienert G, Thorsen M, Schussler M, Nilsson H, Wagner A et al (2008) A subgroup of plant aquaporins facilitate the bi-directional diffusion of as(OH)3 and sb(OH)3 across membranes. BMC Biol 6(1):26

    Article  PubMed  Google Scholar 

  • Chaumont F, Moshelion M, Daniels MJ (2005) Regulation of plant aquaporin activity. Biol Cell 97(10):749–764

    Article  PubMed  CAS  Google Scholar 

  • Dallagnol LJ, Rodrigues FÃ, Mielli MVB, Ma JF, Datnoff LE (2009) Defective active silicon uptake affects some components of rice resistance to brown spot. Phytopathology 99(1):116–121

    Article  PubMed  CAS  Google Scholar 

  • Dhankher OP (2005) Arsenic metabolism in plants: an inside story. New Phytol 168(3):503–505

    Article  PubMed  CAS  Google Scholar 

  • Dhankher OP, Li Y, Rosen BP, Shi J, Salt D et al (2002) Engineering tolerance and hyperaccumulation of arsenic in plants by combining arsenate reductase and [gamma]-glutamylcysteine synthetase expression. Nat Biotech 20(11):1140–1145

    Article  CAS  Google Scholar 

  • Fageria NK (2007) Yield physiology of rice. J Plant Nutr 30(6):843–879

    Article  CAS  Google Scholar 

  • Fitzpatrick KL, Reid RJ (2009) The involvement of aquaglyceroporins in transport of boron in barley roots. Plant Cell Environ 32(10):1357–1365

    Article  PubMed  CAS  Google Scholar 

  • Guo L, Wang ZY, Lin H, Cui WE, Chen J, Liu M, Chen ZL, Qu LJ, Gu H (2006) Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Res 16(3):277–286

    Article  PubMed  CAS  Google Scholar 

  • IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (2004) Some drinking-water disinfectants and contaminants, including arsenic. monographs on chloramine, chloral and chloral hydrate, dichloroacetic acid, trichloroacetic acid and 3-chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone. IARC Monogr Eval Carcinog Risks Hum 84:269–477

    Google Scholar 

  • Isayenkov SV, Maathuis FJM (2008) The Arabidopsis thaliana aquaglyceroporin AtNIP7;1 is a pathway for arsenite uptake. FEBS Lett 582(11):1625–1628

    Article  PubMed  CAS  Google Scholar 

  • Jang JY, Kim DG, Kim YO, Kim JS, Kang H (2004) An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol Biol 54(5):713–725

    Article  PubMed  CAS  Google Scholar 

  • Jang JY, Lee SH, Rhee JY, Chung GC, Ahn SJ, Kang H (2007) Transgenic Arabidopsis and tobacco plants overexpressing an aquaporin respond differently to various abiotic stresses. Plant Mol Biol 64(6):621–632

    Article  PubMed  CAS  Google Scholar 

  • Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjovall S et al (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 126(4):1358–1369

    Article  PubMed  CAS  Google Scholar 

  • Johansson I, Karlsson M, Johanson U, Larsson C, Kjellbom P (2000) The role of aquaporins in cellular and whole plant water balance. Biochimica Et Biophysica Acta (BBA) (Biomembranes) 1465(1–2):324–342

    Article  CAS  Google Scholar 

  • Juhasz AL, Naidu R, Zhu YG, Wang LS, Jiang JY et al (2003) Toxicity issues associated with geogenic arsenic in the groundwater–soil–plant–human continuum. Bull Environ Contam Toxicol 71(6):1100–1107

    Article  PubMed  CAS  Google Scholar 

  • Kamiya T, Tanaka M, Mitani N, Ma JF, Maeshima M et al (2009) NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana. J Biol Chem 284(4):2114–2120

    Article  PubMed  CAS  Google Scholar 

  • Li GW, Zhang MH, Cai WM, Sun WN, Su WA (2008) Characterization of OsPIP2;7, a water channel protein in rice. Plant Cell Physiol 49(2):1851–1858

    Article  PubMed  CAS  Google Scholar 

  • Li R, Ago Y, Liu W, Mitani N, Feldmann J et al (2009) The rice aquaporin Lsi1 mediates uptake of methylated arsenic species. Plant Physiol 150(4):2071–2080

    Article  PubMed  CAS  Google Scholar 

  • Lian H, Yu X, Ye Q, Ding X, Kitagawa Y et al (2004) The role of aquaporin RWC3 in drought avoidance in rice. Plant Cell Physiol 45(4):481–489

    Article  PubMed  CAS  Google Scholar 

  • Liu Z, Shen J, Carbrey JM, Mukhopadhyay R, Agre P et al (2002) Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9. Proc Natl Acad Sci USA 99(9):6053–6058

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25(4):402–408

    Article  PubMed  CAS  Google Scholar 

  • Ma JF, Yamaji N (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci 11(8):392–397

    Article  PubMed  CAS  Google Scholar 

  • Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S et al (2006) A silicon transporter in rice. Nature 440(7084):688–691

    Article  PubMed  CAS  Google Scholar 

  • Ma JF, Yamaji N, Mitani N, Xu X, Su Y et al (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci USA 105(29):9931–9935

    Article  PubMed  CAS  Google Scholar 

  • Meharg AA (2004) Arsenic in rice—understanding a new disaster for south-east Asia. Trends Plant Sci 9(9):415–417

    Article  PubMed  CAS  Google Scholar 

  • Meharg AA, Macnair MR (1992) Suppression of the high affinity phosphate uptake system: a mechanism of arsenate tolerance in Holcus lanatus L. J Exp Bot 43(4):519–524

    Article  CAS  Google Scholar 

  • Meharg AA, Rahman MM (2003) Arsenic contamination of bangladesh paddy field soils: implications for rice contribution to arsenic consumption. Environ Sci Technol 37(2):229–234

    Article  PubMed  CAS  Google Scholar 

  • Meharg AA, Williams PN, Adomako E, Lawgali YY, Deacon C et al (2009) Geographical variation in total and inorganic arsenic content of polished (white) rice. Environ Sci Technol 43(5):1612–1617

    Article  PubMed  CAS  Google Scholar 

  • Meng Y, Liu Z, Rosen BP (2004) As(III) and sb(III) uptake by GlpF and efflux by ArsB in escherichia coli. J Biol Chem 279(18):18334–18341

    Article  PubMed  CAS  Google Scholar 

  • Miwa K, Kamiya T, Fujiwara T (2009) Homeostasis of the structurally important micronutrients, B and si. Curr Opin Plant Biol 12(3):307–311

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plantarum 15(3):473–497

    Article  CAS  Google Scholar 

  • Ravenscroft P, Brammer H, Richards KS (2009) Arsenic pollution: a global synthesis. Wiley-Blackwell, UK

    Book  Google Scholar 

  • Rosen BP (2002) Biochemistry of arsenic detoxification. FEBS Lett 529(1):86–92

    Article  PubMed  CAS  Google Scholar 

  • Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol 46(9):1568–1577

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24):4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Weig A, Deswarte C, Chrispeels MJ (1997) The major intrinsic protein family of arabidopsis has 23 members that form three distinct groups with functional aquaporins in each group. Plant Physiol 114(4):1347–1357

    Article  PubMed  CAS  Google Scholar 

  • Williams PN, Villada A, Deacon C, Raab A, Figuerola J et al (2007) Greatly enhanced arsenic shoot assimilation in rice leads to elevated grain levels compared to wheat and barley. Environ Sci Technol 41(19):6854–6859

    Article  PubMed  CAS  Google Scholar 

  • Wysocki R, Chéry CC, Wawrzycka D, Van Hulle M, Cornelis R et al (2001) The glycerol channel Fps1p mediates the uptake of arsenite and antimonite in saccharomyces cerevisiae. Mol Microbiol 40(6):1391–1401

    Article  PubMed  CAS  Google Scholar 

  • Yu X, Peng YH, Zhang MH, Shao YJ, Su WA, Tang ZC (2006) Water relations and an expression analysis of plasma membrane intrinsic proteins in sensitive and tolerant rice during chilling and recovery. Cell Res 16(6):599–608

    Article  PubMed  Google Scholar 

  • Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytol 181(4):777–794

    Article  PubMed  CAS  Google Scholar 

  • Zhao F, Ago Y, Mitani N, Li R, Su Y et al (2010a) The role of the rice aquaporin Lsi1 in arsenite efflux from roots. New Phytol 186(2):392–399

    Article  PubMed  CAS  Google Scholar 

  • Zhao F, McGrath SP, Meharg AA (2010b) Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Annu Rev Plant Biol 61(1):535–559

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This work was supported by a grant (#S18990000000001) from the Ministry of Higher Education and Scientific Research in Egypt through the Egyptian Cultural and Educational Bureau, Washington, DC to OPD and KAM (GM: 714) and partially by a grant (#GO12026, under Department of Energy prime agreement: DE-FG36-02 GO12026) from the consortium of Plant Biotech Research (CPBR) to OPD. Authors wish to thank Dr. Elsbeth Walker and Dr. M. K. Kandasamy for their critical reading of the manuscript and suggestions.

Author information

Authors and Affiliations

  1. Department of Plant, Soil and Insect Sciences, University of Massachusetts, 202 French Hall, Amherst, MA, 01003, USA

    Kareem A. Mosa, Kundan Kumar, Sudesh Chhikara & Om Parkash Dhankher

  2. Department of Biological Sciences, Oakland University, Rochester, MI, 48309, USA

    Joseph Mcdermott & Zijuan Liu

  3. Department of Analytical Chemistry, The Connecticut Agricultural Experiment Station, New Haven, CT, 06504-1106, USA

    Craig Musante & Jason C. White

  4. Department of Biotechnology, Faculty of Agriculture, Al-Azhar University, Cairo, Egypt

    Kareem A. Mosa

Authors
  1. Kareem A. Mosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kundan Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sudesh Chhikara
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joseph Mcdermott
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zijuan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Craig Musante
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jason C. White
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Om Parkash Dhankher
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Om Parkash Dhankher.

Additional information

Kareem A. Mosa, Kundan Kumar contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 16 kb)

Supplementary material 2 (PDF 516 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mosa, K.A., Kumar, K., Chhikara, S. et al. Members of rice plasma membrane intrinsic proteins subfamily are involved in arsenite permeability and tolerance in plants. Transgenic Res 21, 1265–1277 (2012). https://doi.org/10.1007/s11248-012-9600-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11248-012-9600-8

Keywords

Search

Navigation