An arabidopsis basic helix-loop-helix leucine zipper protein modulates metal homeostasis and auxin conjugate responsiveness

Rebekah A. Rampey, Andrew W. Woodward, Brianne N. Hobbs, Megan P. Tierney, Brett Lahner, David E. Salt, Bonnie Bartel

Research output: Contribution to journalArticle

66 Citations (Scopus)

Abstract

The plant hormone auxin can be regulated by formation and hydrolysis of amide-linked indole-3-acetic acid (IAA) conjugates. Here, we report the characterization of the dominant Arabidopsis iaa-leucine resistant3 (ilr3-1) mutant, which has reduced sensitivity to IAA-Leu and IAA-Phe, while retaining wild-type responses to free LAA. The gene defective in ilr3-1 encodes a basic helix-loop-helix leucine zipper protein, bHLH105, and the ilr3-1 lesion results in a truncated product. Overexpressing ilr3-1 in wild-type plants recapitulates certain ilr3-1 mutant phenotypes. In contrast, the loss-of-function ilr3-2 allele has increased IAA-Leu sensitivity compared to wild type, indicating that the ilr3-1 allele confers a gain of function. Microarray and quantitative real-time PCR analyses revealed five downregulated genes in ilr3-1, including three encoding putative membrane proteins similar to the yeast iron and manganese transporter Ccc1p. Transcript changes are accompanied by reciprocally misregulated metal accumulation in ilr3-1 and ilr3-2 mutants. Further, ilr3-1 seedlings are less sensitive than wild type to manganese, and auxin conjugate response phenotypes are dependent on exogenous metal concentration in ilr3 mutants. These data suggest a model in which the ILR3/bHLH105 transcription factor regulates expression of metal transporter genes, perhaps indirectly modulating IAA-conjugate hydrolysis by controlling the availability of metals previously shown to influence IAA-amino acid hydrolase protein activity.

Original languageEnglish
Pages (from-to)1841-1857
Number of pages17
JournalGenetics
Volume174
Issue number4
Early online date8 Oct 2006
DOIs
Publication statusPublished - Dec 2006

Keywords

  • transcriptional activation domains
  • iron-deficiency
  • indoleacetic-acid
  • factor family
  • gene family
  • genome-wide
  • thaliana
  • transporter
  • sensitivity
  • mutants

Cite this

An arabidopsis basic helix-loop-helix leucine zipper protein modulates metal homeostasis and auxin conjugate responsiveness. / Rampey, Rebekah A.; Woodward, Andrew W.; Hobbs, Brianne N.; Tierney, Megan P.; Lahner, Brett; Salt, David E.; Bartel, Bonnie.

In: Genetics, Vol. 174, No. 4, 12.2006, p. 1841-1857.

Research output: Contribution to journalArticle

Rampey, Rebekah A. ; Woodward, Andrew W. ; Hobbs, Brianne N. ; Tierney, Megan P. ; Lahner, Brett ; Salt, David E. ; Bartel, Bonnie. / An arabidopsis basic helix-loop-helix leucine zipper protein modulates metal homeostasis and auxin conjugate responsiveness. In: Genetics. 2006 ; Vol. 174, No. 4. pp. 1841-1857.
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abstract = "The plant hormone auxin can be regulated by formation and hydrolysis of amide-linked indole-3-acetic acid (IAA) conjugates. Here, we report the characterization of the dominant Arabidopsis iaa-leucine resistant3 (ilr3-1) mutant, which has reduced sensitivity to IAA-Leu and IAA-Phe, while retaining wild-type responses to free LAA. The gene defective in ilr3-1 encodes a basic helix-loop-helix leucine zipper protein, bHLH105, and the ilr3-1 lesion results in a truncated product. Overexpressing ilr3-1 in wild-type plants recapitulates certain ilr3-1 mutant phenotypes. In contrast, the loss-of-function ilr3-2 allele has increased IAA-Leu sensitivity compared to wild type, indicating that the ilr3-1 allele confers a gain of function. Microarray and quantitative real-time PCR analyses revealed five downregulated genes in ilr3-1, including three encoding putative membrane proteins similar to the yeast iron and manganese transporter Ccc1p. Transcript changes are accompanied by reciprocally misregulated metal accumulation in ilr3-1 and ilr3-2 mutants. Further, ilr3-1 seedlings are less sensitive than wild type to manganese, and auxin conjugate response phenotypes are dependent on exogenous metal concentration in ilr3 mutants. These data suggest a model in which the ILR3/bHLH105 transcription factor regulates expression of metal transporter genes, perhaps indirectly modulating IAA-conjugate hydrolysis by controlling the availability of metals previously shown to influence IAA-amino acid hydrolase protein activity.",
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AU - Rampey, Rebekah A.

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AU - Hobbs, Brianne N.

AU - Tierney, Megan P.

AU - Lahner, Brett

AU - Salt, David E.

AU - Bartel, Bonnie

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N2 - The plant hormone auxin can be regulated by formation and hydrolysis of amide-linked indole-3-acetic acid (IAA) conjugates. Here, we report the characterization of the dominant Arabidopsis iaa-leucine resistant3 (ilr3-1) mutant, which has reduced sensitivity to IAA-Leu and IAA-Phe, while retaining wild-type responses to free LAA. The gene defective in ilr3-1 encodes a basic helix-loop-helix leucine zipper protein, bHLH105, and the ilr3-1 lesion results in a truncated product. Overexpressing ilr3-1 in wild-type plants recapitulates certain ilr3-1 mutant phenotypes. In contrast, the loss-of-function ilr3-2 allele has increased IAA-Leu sensitivity compared to wild type, indicating that the ilr3-1 allele confers a gain of function. Microarray and quantitative real-time PCR analyses revealed five downregulated genes in ilr3-1, including three encoding putative membrane proteins similar to the yeast iron and manganese transporter Ccc1p. Transcript changes are accompanied by reciprocally misregulated metal accumulation in ilr3-1 and ilr3-2 mutants. Further, ilr3-1 seedlings are less sensitive than wild type to manganese, and auxin conjugate response phenotypes are dependent on exogenous metal concentration in ilr3 mutants. These data suggest a model in which the ILR3/bHLH105 transcription factor regulates expression of metal transporter genes, perhaps indirectly modulating IAA-conjugate hydrolysis by controlling the availability of metals previously shown to influence IAA-amino acid hydrolase protein activity.

AB - The plant hormone auxin can be regulated by formation and hydrolysis of amide-linked indole-3-acetic acid (IAA) conjugates. Here, we report the characterization of the dominant Arabidopsis iaa-leucine resistant3 (ilr3-1) mutant, which has reduced sensitivity to IAA-Leu and IAA-Phe, while retaining wild-type responses to free LAA. The gene defective in ilr3-1 encodes a basic helix-loop-helix leucine zipper protein, bHLH105, and the ilr3-1 lesion results in a truncated product. Overexpressing ilr3-1 in wild-type plants recapitulates certain ilr3-1 mutant phenotypes. In contrast, the loss-of-function ilr3-2 allele has increased IAA-Leu sensitivity compared to wild type, indicating that the ilr3-1 allele confers a gain of function. Microarray and quantitative real-time PCR analyses revealed five downregulated genes in ilr3-1, including three encoding putative membrane proteins similar to the yeast iron and manganese transporter Ccc1p. Transcript changes are accompanied by reciprocally misregulated metal accumulation in ilr3-1 and ilr3-2 mutants. Further, ilr3-1 seedlings are less sensitive than wild type to manganese, and auxin conjugate response phenotypes are dependent on exogenous metal concentration in ilr3 mutants. These data suggest a model in which the ILR3/bHLH105 transcription factor regulates expression of metal transporter genes, perhaps indirectly modulating IAA-conjugate hydrolysis by controlling the availability of metals previously shown to influence IAA-amino acid hydrolase protein activity.

KW - transcriptional activation domains

KW - iron-deficiency

KW - indoleacetic-acid

KW - factor family

KW - gene family

KW - genome-wide

KW - thaliana

KW - transporter

KW - sensitivity

KW - mutants

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DO - 10.1534/genetics.106.061044

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EP - 1857

JO - Genetics

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SN - 0016-6731

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ER -