A rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution.

Development in multicellular organisms depends on the ability of individual cells to coordinate their behavior by means of small signaling molecules to form correctly patterned tissues. In plants, a unique mechanism of directional transport of the signaling molecule auxin between cells connects cell...

Full description

Bibliographic Details
Main Authors: Ora Hazak, Daria Bloch, Limor Poraty, Hasana Sternberg, Jing Zhang, Jirí Friml, Shaul Yalovsky
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2010-01-01
Series:PLoS Biology
Online Access:http://europepmc.org/articles/PMC2808208?pdf=render
id doaj-4e764d3a43fb4f8fb1c9226d73364fb2
record_format Article
spelling doaj-4e764d3a43fb4f8fb1c9226d73364fb22021-07-02T07:41:29ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852010-01-0181e100028210.1371/journal.pbio.1000282A rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution.Ora HazakDaria BlochLimor PoratyHasana SternbergJing ZhangJirí FrimlShaul YalovskyDevelopment in multicellular organisms depends on the ability of individual cells to coordinate their behavior by means of small signaling molecules to form correctly patterned tissues. In plants, a unique mechanism of directional transport of the signaling molecule auxin between cells connects cell polarity and tissue patterning and thus is required for many aspects of plant development. Direction of auxin flow is determined by polar subcellular localization of PIN auxin efflux transporters. Dynamic PIN polar localization results from the constitutive endocytic cycling to and from the plasma membrane, but it is not well understood how this mechanism connects to regulators of cell polarity. The Rho family small GTPases ROPs/RACs are master regulators of cell polarity, however their role in regulating polar protein trafficking and polar auxin transport has not been established. Here, by analysis of mutants and transgenic plants, we show that the ROP interactor and polarity regulator scaffold protein ICR1 is required for recruitment of PIN proteins to the polar domains at the plasma membrane. icr1 mutant embryos and plants display an a array of severe developmental aberrations that are caused by compromised differential auxin distribution. ICR1 functions at the plasma membrane where it is required for exocytosis but does not recycle together with PINs. ICR1 expression is quickly induced by auxin but is suppressed at the positions of stable auxin maxima in the hypophysis and later in the embryonic and mature root meristems. Our results imply that ICR1 is part of an auxin regulated positive feedback loop realized by a unique integration of auxin-dependent transcriptional regulation into ROP-mediated modulation of cell polarity. Thus, ICR1 forms an auxin-modulated link between cell polarity, exocytosis, and auxin transport-dependent tissue patterning.http://europepmc.org/articles/PMC2808208?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Ora Hazak
Daria Bloch
Limor Poraty
Hasana Sternberg
Jing Zhang
Jirí Friml
Shaul Yalovsky
spellingShingle Ora Hazak
Daria Bloch
Limor Poraty
Hasana Sternberg
Jing Zhang
Jirí Friml
Shaul Yalovsky
A rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution.
PLoS Biology
author_facet Ora Hazak
Daria Bloch
Limor Poraty
Hasana Sternberg
Jing Zhang
Jirí Friml
Shaul Yalovsky
author_sort Ora Hazak
title A rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution.
title_short A rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution.
title_full A rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution.
title_fullStr A rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution.
title_full_unstemmed A rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution.
title_sort rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution.
publisher Public Library of Science (PLoS)
series PLoS Biology
issn 1544-9173
1545-7885
publishDate 2010-01-01
description Development in multicellular organisms depends on the ability of individual cells to coordinate their behavior by means of small signaling molecules to form correctly patterned tissues. In plants, a unique mechanism of directional transport of the signaling molecule auxin between cells connects cell polarity and tissue patterning and thus is required for many aspects of plant development. Direction of auxin flow is determined by polar subcellular localization of PIN auxin efflux transporters. Dynamic PIN polar localization results from the constitutive endocytic cycling to and from the plasma membrane, but it is not well understood how this mechanism connects to regulators of cell polarity. The Rho family small GTPases ROPs/RACs are master regulators of cell polarity, however their role in regulating polar protein trafficking and polar auxin transport has not been established. Here, by analysis of mutants and transgenic plants, we show that the ROP interactor and polarity regulator scaffold protein ICR1 is required for recruitment of PIN proteins to the polar domains at the plasma membrane. icr1 mutant embryos and plants display an a array of severe developmental aberrations that are caused by compromised differential auxin distribution. ICR1 functions at the plasma membrane where it is required for exocytosis but does not recycle together with PINs. ICR1 expression is quickly induced by auxin but is suppressed at the positions of stable auxin maxima in the hypophysis and later in the embryonic and mature root meristems. Our results imply that ICR1 is part of an auxin regulated positive feedback loop realized by a unique integration of auxin-dependent transcriptional regulation into ROP-mediated modulation of cell polarity. Thus, ICR1 forms an auxin-modulated link between cell polarity, exocytosis, and auxin transport-dependent tissue patterning.
url http://europepmc.org/articles/PMC2808208?pdf=render
work_keys_str_mv AT orahazak arhoscaffoldintegratesthesecretorysystemwithfeedbackmechanismsinregulationofauxindistribution
AT dariabloch arhoscaffoldintegratesthesecretorysystemwithfeedbackmechanismsinregulationofauxindistribution
AT limorporaty arhoscaffoldintegratesthesecretorysystemwithfeedbackmechanismsinregulationofauxindistribution
AT hasanasternberg arhoscaffoldintegratesthesecretorysystemwithfeedbackmechanismsinregulationofauxindistribution
AT jingzhang arhoscaffoldintegratesthesecretorysystemwithfeedbackmechanismsinregulationofauxindistribution
AT jirifriml arhoscaffoldintegratesthesecretorysystemwithfeedbackmechanismsinregulationofauxindistribution
AT shaulyalovsky arhoscaffoldintegratesthesecretorysystemwithfeedbackmechanismsinregulationofauxindistribution
AT orahazak rhoscaffoldintegratesthesecretorysystemwithfeedbackmechanismsinregulationofauxindistribution
AT dariabloch rhoscaffoldintegratesthesecretorysystemwithfeedbackmechanismsinregulationofauxindistribution
AT limorporaty rhoscaffoldintegratesthesecretorysystemwithfeedbackmechanismsinregulationofauxindistribution
AT hasanasternberg rhoscaffoldintegratesthesecretorysystemwithfeedbackmechanismsinregulationofauxindistribution
AT jingzhang rhoscaffoldintegratesthesecretorysystemwithfeedbackmechanismsinregulationofauxindistribution
AT jirifriml rhoscaffoldintegratesthesecretorysystemwithfeedbackmechanismsinregulationofauxindistribution
AT shaulyalovsky rhoscaffoldintegratesthesecretorysystemwithfeedbackmechanismsinregulationofauxindistribution
_version_ 1721335692661882880