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Monoubiquitin-dependent endocytosis of the Iron-Regulated Transporter 1 (IRT1) transporter controls iron uptake in plants

Marie Barberon, Eenric Zelazny, Stephanie Robert UGent, Geneviève Conejero, Cathy Curie, Jiri Friml UGent and Grégory Vert (2011) PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 108(32). p.E450-E458
abstract
Plants take up iron from the soil using the IRON-REGULATED TRANSPORTER 1 (IRT1) high-affinity iron transporter at the root surface. Sophisticated regulatory mechanisms allow plants to tightly control the levels of IRT1, ensuring optimal absorption of essential but toxic iron. Here, we demonstrate that overexpression of Arabidopsis thaliana IRT1 leads to constitutive IRT1 protein accumulation, metal overload, and oxidative stress. IRT1 is unexpectedly found in trans-Golgi network/early endosomes of root hair cells, and its levels and localization are unaffected by iron nutrition. Using pharmacological approaches, we show that IRT1 cycles to the plasma membrane to perform iron and metal uptake at the cell surface and is sent to the vacuole for proper turnover. We also prove that IRT1 is monoubiquitinated on several cytosol-exposed residues in vivo and that mutation of two putative monoubiquitination target residues in IRT1 triggers stabilization at the plasma membrane and leads to extreme lethality. Together, these data suggest a model in which monoubiquitin-dependent internalization/sorting and turnover keep the plasma membrane pool of IRT1 low to ensure proper iron uptake and to prevent metal toxicity. More generally, our work demonstrates the existence of monoubiquitin-dependent trafficking to lytic vacuoles in plants and points to proteasome-independent turnover of plasma membrane proteins.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
E3 UBIQUITIN LIGASE, PLASMA-MEMBRANE, YEAST, RECEPTOR, THALIANA, GENE, ubiquitin, protein dynamic, plant cell biology, INTRACELLULAR TRAFFICKING, ARABIDOPSIS METAL TRANSPORTER, PROTEIN, CELL-SURFACE
journal title
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Proc. Natl. Acad. Sci. U. S. A.
volume
108
issue
32
pages
E450 - E458
Web of Science type
Article
Web of Science id
000293691400009
JCR category
MULTIDISCIPLINARY SCIENCES
JCR impact factor
9.681 (2011)
JCR rank
3/54 (2011)
JCR quartile
1 (2011)
ISSN
0027-8424
DOI
10.1073/pnas.1100659108
language
English
UGent publication?
yes
classification
A1
additional info
The 2-page author summary is published in Proc. Natl. Acad. Sci. USA 108, 12985-12986.
copyright statement
I have transferred the copyright for this publication to the publisher
id
1896834
handle
http://hdl.handle.net/1854/LU-1896834
date created
2011-09-02 10:16:42
date last changed
2012-04-01 00:30:39
@article{1896834,
  abstract     = {Plants take up iron from the soil using the IRON-REGULATED TRANSPORTER 1 (IRT1) high-affinity iron transporter at the root surface. Sophisticated regulatory mechanisms allow plants to tightly control the levels of IRT1, ensuring optimal absorption of essential but toxic iron. Here, we demonstrate that overexpression of Arabidopsis thaliana IRT1 leads to constitutive IRT1 protein accumulation, metal overload, and oxidative stress. IRT1 is unexpectedly found in trans-Golgi network/early endosomes of root hair cells, and its levels and localization are unaffected by iron nutrition. Using pharmacological approaches, we show that IRT1 cycles to the plasma membrane to perform iron and metal uptake at the cell surface and is sent to the vacuole for proper turnover. We also prove that IRT1 is monoubiquitinated on several cytosol-exposed residues in vivo and that mutation of two putative monoubiquitination target residues in IRT1 triggers stabilization at the plasma membrane and leads to extreme lethality. Together, these data suggest a model in which monoubiquitin-dependent internalization/sorting and turnover keep the plasma membrane pool of IRT1 low to ensure proper iron uptake and to prevent metal toxicity. More generally, our work demonstrates the existence of monoubiquitin-dependent trafficking to lytic vacuoles in plants and points to proteasome-independent turnover of plasma membrane proteins.},
  author       = {Barberon, Marie and Zelazny, Eenric and Robert, Stephanie and Conejero, Genevi{\`e}ve and Curie, Cathy and Friml, Jiri and Vert, Gr{\'e}gory},
  issn         = {0027-8424},
  journal      = {PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA},
  keyword      = {E3 UBIQUITIN LIGASE,PLASMA-MEMBRANE,YEAST,RECEPTOR,THALIANA,GENE,ubiquitin,protein dynamic,plant cell biology,INTRACELLULAR TRAFFICKING,ARABIDOPSIS METAL TRANSPORTER,PROTEIN,CELL-SURFACE},
  language     = {eng},
  number       = {32},
  pages        = {E450--E458},
  title        = {Monoubiquitin-dependent endocytosis of the Iron-Regulated Transporter 1 (IRT1) transporter controls iron uptake in plants},
  url          = {http://dx.doi.org/10.1073/pnas.1100659108},
  volume       = {108},
  year         = {2011},
}

Chicago
Barberon, Marie, Eenric Zelazny, Stephanie Robert, Geneviève Conejero, Cathy Curie, Jiri Friml, and Grégory Vert. 2011. “Monoubiquitin-dependent Endocytosis of the Iron-Regulated Transporter 1 (IRT1) Transporter Controls Iron Uptake in Plants.” Proceedings of the National Academy of Sciences of the United States of America 108 (32): E450–E458.
APA
Barberon, M., Zelazny, E., Robert, S., Conejero, G., Curie, C., Friml, J., & Vert, G. (2011). Monoubiquitin-dependent endocytosis of the Iron-Regulated Transporter 1 (IRT1) transporter controls iron uptake in plants. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 108(32), E450–E458.
Vancouver
1.
Barberon M, Zelazny E, Robert S, Conejero G, Curie C, Friml J, et al. Monoubiquitin-dependent endocytosis of the Iron-Regulated Transporter 1 (IRT1) transporter controls iron uptake in plants. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2011;108(32):E450–E458.
MLA
Barberon, Marie, Eenric Zelazny, Stephanie Robert, et al. “Monoubiquitin-dependent Endocytosis of the Iron-Regulated Transporter 1 (IRT1) Transporter Controls Iron Uptake in Plants.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 108.32 (2011): E450–E458. Print.