Physcomitrium patens PpRIC, an ancestral CRIB-domain ROP effector, inhibits auxin-induced differentiation of apical initial cells

Summary: RHO guanosine triphosphatases are important eukaryotic regulators of cell differentiation and behavior. Plant ROP (RHO of plant) family members activate specific, incompletely characterized downstream signaling. The structurally simple land plant Physcomitrium patens is missing homologs of...

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Main Authors: Maria Ntefidou, D. Magnus Eklund, Aude Le Bail, Sylwia Schulmeister, Franziska Scherbel, Lisa Brandl, Wolfgang Dörfler, Chantal Eichstädt, Anna Bannmüller, Karin Ljung, Benedikt Kost
Format: Article
Language:English
Published: Elsevier 2023-02-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124723001419
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author Maria Ntefidou
D. Magnus Eklund
Aude Le Bail
Sylwia Schulmeister
Franziska Scherbel
Lisa Brandl
Wolfgang Dörfler
Chantal Eichstädt
Anna Bannmüller
Karin Ljung
Benedikt Kost
author_facet Maria Ntefidou
D. Magnus Eklund
Aude Le Bail
Sylwia Schulmeister
Franziska Scherbel
Lisa Brandl
Wolfgang Dörfler
Chantal Eichstädt
Anna Bannmüller
Karin Ljung
Benedikt Kost
author_sort Maria Ntefidou
collection DOAJ
description Summary: RHO guanosine triphosphatases are important eukaryotic regulators of cell differentiation and behavior. Plant ROP (RHO of plant) family members activate specific, incompletely characterized downstream signaling. The structurally simple land plant Physcomitrium patens is missing homologs of key animal and flowering plant RHO effectors but contains a single CRIB (CDC42/RAC interactive binding)-domain-containing RIC (ROP-interacting CRIB-containing) protein (PpRIC). Protonemal P. patens filaments elongate based on regular division and PpROP-dependent tip growth of apical initial cells, which upon stimulation by the hormone auxin differentiate caulonemal characteristics. PpRIC interacts with active PpROP1, co-localizes with this protein at the plasma membrane at the tip of apical initial cells, and accumulates in the nucleus. Remarkably, PpRIC is not required for tip growth but is targeted to the nucleus to block caulonema differentiation downstream of auxin-controlled gene expression. These observations establish functions of PpRIC in mediating crosstalk between ROP and auxin signaling, which contributes to the maintenance of apical initial cell identity.
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spelling doaj.art-02731ffad1514f0194da232bc8c9487a2023-02-16T04:18:07ZengElsevierCell Reports2211-12472023-02-01422112130Physcomitrium patens PpRIC, an ancestral CRIB-domain ROP effector, inhibits auxin-induced differentiation of apical initial cellsMaria Ntefidou0D. Magnus Eklund1Aude Le Bail2Sylwia Schulmeister3Franziska Scherbel4Lisa Brandl5Wolfgang Dörfler6Chantal Eichstädt7Anna Bannmüller8Karin Ljung9Benedikt Kost10Cell Biology, Department of Biology, University Erlangen-Nuremberg, 91058 Erlangen, GermanyPhysiology and Environmental Toxicology, Department of Organismal Biology, Uppsala University, 75236 Uppsala, SwedenCell Biology, Department of Biology, University Erlangen-Nuremberg, 91058 Erlangen, GermanyCell Biology, Department of Biology, University Erlangen-Nuremberg, 91058 Erlangen, GermanyCell Biology, Department of Biology, University Erlangen-Nuremberg, 91058 Erlangen, GermanyCell Biology, Department of Biology, University Erlangen-Nuremberg, 91058 Erlangen, GermanyCell Biology, Department of Biology, University Erlangen-Nuremberg, 91058 Erlangen, GermanyCell Biology, Department of Biology, University Erlangen-Nuremberg, 91058 Erlangen, GermanyCell Biology, Department of Biology, University Erlangen-Nuremberg, 91058 Erlangen, GermanyUmeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 90183 Umeå, SwedenCell Biology, Department of Biology, University Erlangen-Nuremberg, 91058 Erlangen, Germany; Corresponding authorSummary: RHO guanosine triphosphatases are important eukaryotic regulators of cell differentiation and behavior. Plant ROP (RHO of plant) family members activate specific, incompletely characterized downstream signaling. The structurally simple land plant Physcomitrium patens is missing homologs of key animal and flowering plant RHO effectors but contains a single CRIB (CDC42/RAC interactive binding)-domain-containing RIC (ROP-interacting CRIB-containing) protein (PpRIC). Protonemal P. patens filaments elongate based on regular division and PpROP-dependent tip growth of apical initial cells, which upon stimulation by the hormone auxin differentiate caulonemal characteristics. PpRIC interacts with active PpROP1, co-localizes with this protein at the plasma membrane at the tip of apical initial cells, and accumulates in the nucleus. Remarkably, PpRIC is not required for tip growth but is targeted to the nucleus to block caulonema differentiation downstream of auxin-controlled gene expression. These observations establish functions of PpRIC in mediating crosstalk between ROP and auxin signaling, which contributes to the maintenance of apical initial cell identity.http://www.sciencedirect.com/science/article/pii/S2211124723001419CP: PlantsCP: Developmental biology
spellingShingle Maria Ntefidou
D. Magnus Eklund
Aude Le Bail
Sylwia Schulmeister
Franziska Scherbel
Lisa Brandl
Wolfgang Dörfler
Chantal Eichstädt
Anna Bannmüller
Karin Ljung
Benedikt Kost
Physcomitrium patens PpRIC, an ancestral CRIB-domain ROP effector, inhibits auxin-induced differentiation of apical initial cells
Cell Reports
CP: Plants
CP: Developmental biology
title Physcomitrium patens PpRIC, an ancestral CRIB-domain ROP effector, inhibits auxin-induced differentiation of apical initial cells
title_full Physcomitrium patens PpRIC, an ancestral CRIB-domain ROP effector, inhibits auxin-induced differentiation of apical initial cells
title_fullStr Physcomitrium patens PpRIC, an ancestral CRIB-domain ROP effector, inhibits auxin-induced differentiation of apical initial cells
title_full_unstemmed Physcomitrium patens PpRIC, an ancestral CRIB-domain ROP effector, inhibits auxin-induced differentiation of apical initial cells
title_short Physcomitrium patens PpRIC, an ancestral CRIB-domain ROP effector, inhibits auxin-induced differentiation of apical initial cells
title_sort physcomitrium patens ppric an ancestral crib domain rop effector inhibits auxin induced differentiation of apical initial cells
topic CP: Plants
CP: Developmental biology
url http://www.sciencedirect.com/science/article/pii/S2211124723001419
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