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ROTUNDA3 function in plant development by phosphatase 2A-mediated regulation of auxin transporter recycling

Michail Karampelias, Pia Neyt UGent, Steven De Groeve UGent, Stijn Aesaert UGent, Griet Coussens UGent, Jakub Rolčik, Leonardo Bruno, Nancy De Winne UGent, Annemie Van Minnebruggen, Marc Van Montagu UGent, et al. (2016) PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 113(10). p.2768-2773
abstract
The shaping of organs in plants depends on the intercellular flow of the phytohormone auxin, of which the directional signaling is determined by the polar subcellular localization of PIN-FORMED (PIN) auxin transport proteins. Phosphorylation dynamics of PIN proteins are affected by the protein phosphatase 2A (PP2A) and the PINOID kinase, which act antagonistically to mediate their apical-basal polar delivery. Here, we identified the ROTUNDA3 (RON3) protein as a regulator of the PP2A phosphatase activity in Arabidopsis thaliana. The RON3 gene was map-based cloned starting from the ron3-1 leaf mutant and found to be a unique, plant-specific gene coding for a protein with high and dispersed proline content. The ron3-1 and ron3-2 mutant phenotypes [i.e., reduced apical dominance, primary root length, lateral root emergence, and growth; increased ectopic stages II, IV, and V lateral root primordia; decreased auxin maxima in indole-3-acetic acid (IAA)-treated root apical meristems; hypergravitropic root growth and response; increased IAA levels in shoot apices; and reduced auxin accumulation in root meristems] support a role for RON3 in auxin biology. The affinity-purified PP2A complex with RON3 as bait suggested that RON3 might act in PIN transporter trafficking. Indeed, pharmacological interference with vesicle trafficking processes revealed that single ron3-2 and double ron3-2 rcn1 mutants have altered PIN polarity and endocytosis in specific cells. Our data indicate that RON3 contributes to auxin-mediated development by playing a role in PIN recycling and polarity establishment through regulation of the PP2A complex activity.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
MERISTEM, CARRIERS, PROTEINS, POLARITY, EFFLUX, ARABIDOPSIS, LEAF MORPHOGENESIS, plant development, PIN PHOSPHORYLATION, auxin, PP2A, PIN recycling, Arabidopsis
journal title
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Proc. Natl. Acad. Sci. USA
volume
113
issue
10
pages
2768 - 2773
Web of Science type
Article
Web of Science id
000372013300055
JCR category
MULTIDISCIPLINARY SCIENCES
JCR impact factor
9.661 (2016)
JCR rank
4/64 (2016)
JCR quartile
1 (2016)
ISSN
0027-8424
DOI
10.1073/pnas.1501343112
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
7186338
handle
http://hdl.handle.net/1854/LU-7186338
date created
2016-04-18 11:46:36
date last changed
2016-12-19 15:47:27
@article{7186338,
  abstract     = {The shaping of organs in plants depends on the intercellular flow of the phytohormone auxin, of which the directional signaling is determined by the polar subcellular localization of PIN-FORMED (PIN) auxin transport proteins. Phosphorylation dynamics of PIN proteins are affected by the protein phosphatase 2A (PP2A) and the PINOID kinase, which act antagonistically to mediate their apical-basal polar delivery. Here, we identified the ROTUNDA3 (RON3) protein as a regulator of the PP2A phosphatase activity in Arabidopsis thaliana. The RON3 gene was map-based cloned starting from the ron3-1 leaf mutant and found to be a unique, plant-specific gene coding for a protein with high and dispersed proline content. The ron3-1 and ron3-2 mutant phenotypes [i.e., reduced apical dominance, primary root length, lateral root emergence, and growth; increased ectopic stages II, IV, and V lateral root primordia; decreased auxin maxima in indole-3-acetic acid (IAA)-treated root apical meristems; hypergravitropic root growth and response; increased IAA levels in shoot apices; and reduced auxin accumulation in root meristems] support a role for RON3 in auxin biology. The affinity-purified PP2A complex with RON3 as bait suggested that RON3 might act in PIN transporter trafficking. Indeed, pharmacological interference with vesicle trafficking processes revealed that single ron3-2 and double ron3-2 rcn1 mutants have altered PIN polarity and endocytosis in specific cells. Our data indicate that RON3 contributes to auxin-mediated development by playing a role in PIN recycling and polarity establishment through regulation of the PP2A complex activity.},
  author       = {Karampelias, Michail and Neyt, Pia and De Groeve, Steven and Aesaert, Stijn and Coussens, Griet and Rol\v{c}ik, Jakub and Bruno, Leonardo and De Winne, Nancy and Van Minnebruggen, Annemie and Van Montagu, Marc and Ponce, Mar{\'i}a Rosa and Micol, Jos{\'e} Luis and Friml, Jiri and De Jaeger, Geert and Van Lijsebettens, Maria},
  issn         = {0027-8424},
  journal      = {PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA},
  keyword      = {MERISTEM,CARRIERS,PROTEINS,POLARITY,EFFLUX,ARABIDOPSIS,LEAF MORPHOGENESIS,plant development,PIN PHOSPHORYLATION,auxin,PP2A,PIN recycling,Arabidopsis},
  language     = {eng},
  number       = {10},
  pages        = {2768--2773},
  title        = {ROTUNDA3 function in plant development by phosphatase 2A-mediated regulation of auxin transporter recycling},
  url          = {http://dx.doi.org/10.1073/pnas.1501343112},
  volume       = {113},
  year         = {2016},
}

Chicago
Karampelias, Michail, Pia Neyt, Steven De Groeve, Stijn Aesaert, Griet Coussens, Jakub Rolčik, Leonardo Bruno, et al. 2016. “ROTUNDA3 Function in Plant Development by Phosphatase 2A-mediated Regulation of Auxin Transporter Recycling.” Proceedings of the National Academy of Sciences of the United States of America 113 (10): 2768–2773.
APA
Karampelias, M., Neyt, P., De Groeve, S., Aesaert, S., Coussens, G., Rolčik, J., Bruno, L., et al. (2016). ROTUNDA3 function in plant development by phosphatase 2A-mediated regulation of auxin transporter recycling. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 113(10), 2768–2773.
Vancouver
1.
Karampelias M, Neyt P, De Groeve S, Aesaert S, Coussens G, Rolčik J, et al. ROTUNDA3 function in plant development by phosphatase 2A-mediated regulation of auxin transporter recycling. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2016;113(10):2768–73.
MLA
Karampelias, Michail, Pia Neyt, Steven De Groeve, et al. “ROTUNDA3 Function in Plant Development by Phosphatase 2A-mediated Regulation of Auxin Transporter Recycling.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 113.10 (2016): 2768–2773. Print.