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Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions

Pankaj Dhonukshe UGent, Hirokazu Tanaka UGent, Tatsuaki Goh, Kazuo Ebine, Ari Pekka Mähönen, Kalika Prasad, Ikram Blilou, Niko Geldner, Jian Xu and Tomohiro Uemura, et al. (2008) NATURE. 456(7224). p.962-966
abstract
Dynamically polarized membrane proteins define different cell boundaries and have an important role in intercellular communication - a vital feature of multicellular development. Efflux carriers for the signalling molecule auxin from the PIN family(1) are landmarks of cell polarity in plants and have a crucial involvement in auxin distribution- dependent development including embryo patterning, organogenesis and tropisms(2-7). Polar PIN localization determines the direction of intercellular auxin flow(8), yet the mechanisms generating PIN polarity remain unclear. Here we identify an endocytosis- dependent mechanism of PIN polarity generation and analyse its developmental implications. Real- time PIN tracking showed that after synthesis, PINs are initially delivered to the plasma membrane in a non- polar manner and their polarity is established by subsequent endocytic recycling. Interference with PIN endocytosis either by auxin or by manipulation of the Arabidopsis Rab5 GTPase pathway prevents PIN polarization. Failure of PIN polarization transiently alters asymmetric auxin distribution during embryogenesis and increases the local auxin response in apical embryo regions. This results in ectopic expression of auxin pathway- associated root- forming master regulators in embryonic leaves and promotes homeotic transformation of leaves to roots. Our results indicate a two- step mechanism for the generation of PIN polar localization and the essential role of endocytosis in this process. It also highlights the link between endocytosis- dependent polarity of individual cells and auxin distribution- dependent cell fate establishment for multicellular patterning.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
DISTINCT, ARABIDOPSIS-THALIANA, GRADIENTS, TRAFFICKING, ROOT, STEM, BIOSYNTHESIS, H+-ATPASE, TRANSPORT, EFFLUX
journal title
NATURE
Nature
volume
456
issue
7224
pages
962 - 966
Web of Science type
Article
Web of Science id
000261768300048
JCR category
MULTIDISCIPLINARY SCIENCES
JCR impact factor
31.434 (2008)
JCR rank
1/41 (2008)
JCR quartile
1 (2008)
ISSN
0028-0836
DOI
10.1038/nature07409
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
506053
handle
http://hdl.handle.net/1854/LU-506053
date created
2009-02-26 18:14:22
date last changed
2013-09-17 11:20:58
@article{506053,
  abstract     = {Dynamically polarized membrane proteins define different cell boundaries and have an important role in intercellular communication - a vital feature of multicellular development. Efflux carriers for the signalling molecule auxin from the PIN family(1) are landmarks of cell polarity in plants and have a crucial involvement in auxin distribution- dependent development including embryo patterning, organogenesis and tropisms(2-7). Polar PIN localization determines the direction of intercellular auxin flow(8), yet the mechanisms generating PIN polarity remain unclear. Here we identify an endocytosis- dependent mechanism of PIN polarity generation and analyse its developmental implications. Real- time PIN tracking showed that after synthesis, PINs are initially delivered to the plasma membrane in a non- polar manner and their polarity is established by subsequent endocytic recycling. Interference with PIN endocytosis either by auxin or by manipulation of the Arabidopsis Rab5 GTPase pathway prevents PIN polarization. Failure of PIN polarization transiently alters asymmetric auxin distribution during embryogenesis and increases the local auxin response in apical embryo regions. This results in ectopic expression of auxin pathway- associated root- forming master regulators in embryonic leaves and promotes homeotic transformation of leaves to roots. Our results indicate a two- step mechanism for the generation of PIN polar localization and the essential role of endocytosis in this process. It also highlights the link between endocytosis- dependent polarity of individual cells and auxin distribution- dependent cell fate establishment for multicellular patterning.},
  author       = {Dhonukshe, Pankaj and Tanaka, Hirokazu and Goh, Tatsuaki and Ebine, Kazuo and M{\"a}h{\"o}nen, Ari Pekka and Prasad, Kalika and Blilou, Ikram and Geldner, Niko and Xu, Jian and Uemura, Tomohiro and Chory, Joanne and Ueda, Takashi and Nakano, Akihiko and Scheres, Ben and Friml, Jiri},
  issn         = {0028-0836},
  journal      = {NATURE},
  keyword      = {DISTINCT,ARABIDOPSIS-THALIANA,GRADIENTS,TRAFFICKING,ROOT,STEM,BIOSYNTHESIS,H+-ATPASE,TRANSPORT,EFFLUX},
  language     = {eng},
  number       = {7224},
  pages        = {962--966},
  title        = {Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions},
  url          = {http://dx.doi.org/10.1038/nature07409},
  volume       = {456},
  year         = {2008},
}

Chicago
Dhonukshe, Pankaj, Hirokazu Tanaka, Tatsuaki Goh, Kazuo Ebine, Ari Pekka Mähönen, Kalika Prasad, Ikram Blilou, et al. 2008. “Generation of Cell Polarity in Plants Links Endocytosis, Auxin Distribution and Cell Fate Decisions.” Nature 456 (7224): 962–966.
APA
Dhonukshe, P., Tanaka, H., Goh, T., Ebine, K., Mähönen, A. P., Prasad, K., Blilou, I., et al. (2008). Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. NATURE, 456(7224), 962–966.
Vancouver
1.
Dhonukshe P, Tanaka H, Goh T, Ebine K, Mähönen AP, Prasad K, et al. Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. NATURE. 2008;456(7224):962–6.
MLA
Dhonukshe, Pankaj, Hirokazu Tanaka, Tatsuaki Goh, et al. “Generation of Cell Polarity in Plants Links Endocytosis, Auxin Distribution and Cell Fate Decisions.” NATURE 456.7224 (2008): 962–966. Print.