A Vacuolar Arsenite Transporter Necessary for Arsenic Tolerance in the Arsenic Hyperaccumulating Fern Pteris vittata Is Missing in Flowering Plants

Emily Indriolo, GunNam Na, Danielle Ellis, David E. Salt, Jo Ann Banks

Research output: Contribution to journalArticle

129 Citations (Scopus)

Abstract

The fern Pteris vittata tolerates and hyperaccumulates exceptionally high levels of the toxic metalloid arsenic, and this trait appears unique to the Pteridaceae. Once taken up by the root, arsenate is reduced to arsenite as it is transported to the lamina of the frond, where it is stored in cells as free arsenite. Here, we describe the isolation and characterization of two P. vittata genes, ACR3 and ACR3;1, which encode proteins similar to the ACR3 arsenite effluxer of yeast. Pv ACR3 is able to rescue the arsenic-sensitive phenotypes of yeast deficient for ACR3. ACR3 transcripts are upregulated by arsenic in sporophyte roots and gametophytes, tissues that directly contact soil, whereas ACR3;1 expression is unaffected by arsenic. Knocking down the expression of ACR3, but not ACR3;1, in the gametophyte results in an arsenite-sensitive phenotype, indicating that ACR3 plays a necessary role in arsenic tolerance in the gametophyte. We show that ACR3 localizes to the vacuolar membrane in gametophytes, indicating that it likely effluxes arsenite into the vacuole for sequestration. Whereas single-copy ACR3 genes are present in moss, lycophytes, other ferns, and gymnosperms, none are present in angiosperms. The duplication of ACR3 in P. vittata and the loss of ACR3 in angiosperms may explain arsenic tolerance in this unusual group of ferns while precluding the same trait in angiosperms.

Original languageEnglish
Pages (from-to)2045-2057
Number of pages13
JournalThe Plant Cell
Volume22
Issue number6
DOIs
Publication statusPublished - Jun 2010

Keywords

  • specificity tyrosine-phosphatase
  • saccharomyces-cerevisiae
  • arabidopsis-thaliana
  • contaminated soils
  • membrane-proteins
  • high-throughput
  • holcus-lanatus
  • phytochelatin complexes
  • topology prediction
  • Southern China

Cite this

A Vacuolar Arsenite Transporter Necessary for Arsenic Tolerance in the Arsenic Hyperaccumulating Fern Pteris vittata Is Missing in Flowering Plants. / Indriolo, Emily; Na, GunNam; Ellis, Danielle; Salt, David E.; Banks, Jo Ann.

In: The Plant Cell, Vol. 22, No. 6, 06.2010, p. 2045-2057.

Research output: Contribution to journalArticle

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AB - The fern Pteris vittata tolerates and hyperaccumulates exceptionally high levels of the toxic metalloid arsenic, and this trait appears unique to the Pteridaceae. Once taken up by the root, arsenate is reduced to arsenite as it is transported to the lamina of the frond, where it is stored in cells as free arsenite. Here, we describe the isolation and characterization of two P. vittata genes, ACR3 and ACR3;1, which encode proteins similar to the ACR3 arsenite effluxer of yeast. Pv ACR3 is able to rescue the arsenic-sensitive phenotypes of yeast deficient for ACR3. ACR3 transcripts are upregulated by arsenic in sporophyte roots and gametophytes, tissues that directly contact soil, whereas ACR3;1 expression is unaffected by arsenic. Knocking down the expression of ACR3, but not ACR3;1, in the gametophyte results in an arsenite-sensitive phenotype, indicating that ACR3 plays a necessary role in arsenic tolerance in the gametophyte. We show that ACR3 localizes to the vacuolar membrane in gametophytes, indicating that it likely effluxes arsenite into the vacuole for sequestration. Whereas single-copy ACR3 genes are present in moss, lycophytes, other ferns, and gymnosperms, none are present in angiosperms. The duplication of ACR3 in P. vittata and the loss of ACR3 in angiosperms may explain arsenic tolerance in this unusual group of ferns while precluding the same trait in angiosperms.

KW - specificity tyrosine-phosphatase

KW - saccharomyces-cerevisiae

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KW - contaminated soils

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KW - high-throughput

KW - holcus-lanatus

KW - phytochelatin complexes

KW - topology prediction

KW - Southern China

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