NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana

Takehiro Kamiya, Mayuki Tanaka, Namiki Mitani, Jian Feng Ma, Masayoshi Maeshima, Toru Fujiwara

Research output: Contribution to journalArticle

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Abstract

Arsenite [As(III)] is highly toxic to organisms, including plants. Very recently, transporters in rice responsible for As(III) transport have been described (Ma, J. F., Yamaji, N., Mitani, N., Xu, X. Y., Su, Y. H., McGrath, S. P., and Zhao, F. J. (2008) Proc. Natl. Acad. Sci. U. S. A. 105, 9931-9935), but little is known about As(III) tolerance. In this study, three independent As(III)-tolerant mutants were isolated from ethyl methanesulfonate-mutagenized M2 seeds of Arabidopsis thaliana. All three mutants carried independent mutations in Nodulin 26-like intrinsic protein 1;1 (NIP1;1), a homolog of an aquaporin. Two independent transgenic lines carrying T-DNA in NIP1;1 were highly tolerant to As(III), establishing that NIP1;1 is the causal gene of As(III) tolerance. Because an aquaglyceroporin is able to transport As(III), we measured As(III) transport activity. When expressed in Xenopus oocytes, NIP1;1 was capable of transporting As(III). As content in the mutant plants was 30% lower than in wild-type plants. Promoter β-glucuronidase and real-time PCR analysis showed that NIP1;1 is highly expressed in roots, and GFP-NIP1;1 is localized to the plasma membrane. These data show that NIP1;1 is involved in As(III) uptake into roots and that disruption of NIP1;1 function confers As(III) tolerance to plants. NIP1;2 and NIP5;1, closely related homologs of NIP1;1, were also permeable to As(III). Although the disruption of these genes reduced the As content in plants, As(III) tolerance was not observed in nip1;2 and nip5;1 mutants. This indicates that As(III) tolerance cannot be simply explained by decreased As contents in plants.

Original languageEnglish
Pages (from-to)2114-2120
Number of pages7
JournalJournal of Biological Chemistry
Volume284
Issue number4
DOIs
Publication statusPublished - Jan 23 2009

Fingerprint

Aquaporin 1
Arabidopsis
Proteins
Aquaglyceroporins
Genes
Ethyl Methanesulfonate
nodulin
arsenite
Aquaporins
Poisons
Glucuronidase
Cell membranes
Xenopus
Oocytes
Seed
Real-Time Polymerase Chain Reaction
Seeds
Cell Membrane

ASJC Scopus subject areas

  • Biochemistry
  • Cell Biology
  • Molecular Biology

Cite this

NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana. / Kamiya, Takehiro; Tanaka, Mayuki; Mitani, Namiki; Ma, Jian Feng; Maeshima, Masayoshi; Fujiwara, Toru.

In: Journal of Biological Chemistry, Vol. 284, No. 4, 23.01.2009, p. 2114-2120.

Research output: Contribution to journalArticle

Kamiya, Takehiro ; Tanaka, Mayuki ; Mitani, Namiki ; Ma, Jian Feng ; Maeshima, Masayoshi ; Fujiwara, Toru. / NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana. In: Journal of Biological Chemistry. 2009 ; Vol. 284, No. 4. pp. 2114-2120.
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abstract = "Arsenite [As(III)] is highly toxic to organisms, including plants. Very recently, transporters in rice responsible for As(III) transport have been described (Ma, J. F., Yamaji, N., Mitani, N., Xu, X. Y., Su, Y. H., McGrath, S. P., and Zhao, F. J. (2008) Proc. Natl. Acad. Sci. U. S. A. 105, 9931-9935), but little is known about As(III) tolerance. In this study, three independent As(III)-tolerant mutants were isolated from ethyl methanesulfonate-mutagenized M2 seeds of Arabidopsis thaliana. All three mutants carried independent mutations in Nodulin 26-like intrinsic protein 1;1 (NIP1;1), a homolog of an aquaporin. Two independent transgenic lines carrying T-DNA in NIP1;1 were highly tolerant to As(III), establishing that NIP1;1 is the causal gene of As(III) tolerance. Because an aquaglyceroporin is able to transport As(III), we measured As(III) transport activity. When expressed in Xenopus oocytes, NIP1;1 was capable of transporting As(III). As content in the mutant plants was 30{\%} lower than in wild-type plants. Promoter β-glucuronidase and real-time PCR analysis showed that NIP1;1 is highly expressed in roots, and GFP-NIP1;1 is localized to the plasma membrane. These data show that NIP1;1 is involved in As(III) uptake into roots and that disruption of NIP1;1 function confers As(III) tolerance to plants. NIP1;2 and NIP5;1, closely related homologs of NIP1;1, were also permeable to As(III). Although the disruption of these genes reduced the As content in plants, As(III) tolerance was not observed in nip1;2 and nip5;1 mutants. This indicates that As(III) tolerance cannot be simply explained by decreased As contents in plants.",
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AU - Fujiwara, Toru

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