Vectorial Information for Arabidopsis Planar Polarity Is Mediated by Combined AUX1, EIN2, and GNOM Activity

Cell polarity is commonly coordinated within the plane of a single tissue layer (planar polarity), and hair positioning has been exploited as a simple marker for planar polarization of animal epithelia . The root epidermis of the plant Arabidopsis similarly reveals planar polarity of hair localization close to root tip-oriented (basal) ends of hair-forming cells . Hair position is directed toward a concentration maximum of the hormone auxin in the root tip , but mechanisms driving this plant-specific planar polarity remain elusive. Here, we report that combinatorial action of the auxin influx carrier AUX1, ETHYLENE-INSENSITIVE2 (EIN2) , and GNOM genes mediates the vector for coordinate hair positioning. In aux1;ein2;gnom eb triple mutant roots, hairs display axial (apical or basal) instead of coordinate polar (basal) position, and recruitment of Rho-of-Plant (ROP) GTPases to the hair initiation site reveals the same polar-to-axial switch. The auxin concentration gradient is virtually abolished in aux1;ein2;gnom eb roots, where locally applied auxin can coordinate hair positioning. Moreover, auxin overproduction in sectors of wild-type roots enhances planar ROP and hair polarity over long and short distances. Hence, auxin may provide vectorial information for planar polarity that requires combinatorial AUX1, EIN2, and GNOM activity upstream of ROP positioning.

[1]  Michael Sauer,et al.  Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis , 2003, Nature.

[2]  H. Strutt,et al.  Long‐range coordination of planar polarity in Drosophila , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[3]  B. Sundberg,et al.  A Microscale Technique for Gas Chromatography-Mass Spectrometry Measurements of Picogram Amounts of Indole-3-Acetic Acid in Plant Tissues , 1995, Plant physiology.

[4]  Ying Fu,et al.  The Arabidopsis Rop2 GTPase Is a Positive Regulator of Both Root Hair Initiation and Tip Growth Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010359. , 2002, The Plant Cell Online.

[5]  Anna N. Stepanova,et al.  A Link between Ethylene and Auxin Uncovered by the Characterization of Two Root-Specific Ethylene-Insensitive Mutants in Arabidopsis , 2005, The Plant Cell Online.

[6]  J. Ecker,et al.  EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. , 1999, Science.

[7]  J. Friml,et al.  Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth , 2001, The EMBO journal.

[8]  Klaus Palme,et al.  AtPIN2 defines a locus of Arabidopsis for root gravitropism control , 1998, The EMBO journal.

[9]  A. Nakano,et al.  The Arabidopsis GNOM ARF-GEF Mediates Endosomal Recycling, Auxin Transport, and Auxin-Dependent Plant Growth , 2003, Cell.

[10]  M. Grebe.  Ups and downs of tissue and planar polarity in plants , 2004, BioEssays : news and reviews in molecular, cellular and developmental biology.

[11]  Klaus Palme,et al.  A PINOID-Dependent Binary Switch in Apical-Basal PIN Polar Targeting Directs Auxin Efflux , 2004, Science.

[12]  David A. Morris,et al.  Auxin inhibits endocytosis and promotes its own efflux from cells , 2005, Nature.

[13]  K. Koizumi,et al.  A series of novel mutants of Arabidopsis thaliana that are defective in the formation of continuous vascular network: calling the auxin signal flow canalization hypothesis into question. , 2000, Development.

[14]  O. Leyser,et al.  AXR3 and SHY2 interact to regulate root hair development , 2003, Development.

[15]  M. Caboche,et al.  Sur2 mutations of Arabidopsis thaliana define a new locus involved in the control of auxin homeostasis. , 1998, The Plant journal : for cell and molecular biology.

[16]  A. Müller,et al.  Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. , 1998, Science.

[17]  M. Busch,et al.  Molecular analysis of theArabidopsis pattern formation geneGNOM: gene structure and intragenic complementation , 1996, Molecular and General Genetics MGG.

[18]  H. Tsukaya,et al.  The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves. , 2001, Development.

[19]  Joseph R. Ecker,et al.  CTR1, a negative regulator of the ethylene response pathway in arabidopsis, encodes a member of the Raf family of protein kinases , 1993, Cell.

[20]  Gerrit T. S. Beemster,et al.  Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal , 2005, Nature Cell Biology.

[21]  M. Estelle,et al.  The axr6 mutants of Arabidopsis thaliana define a gene involved in auxin response and early development. , 2000, Development.

[22]  Masashi Yamada,et al.  Sites and Regulation of Auxin Biosynthesis in Arabidopsis Roots , 2005, The Plant Cell Online.

[23]  K. Ljung,et al.  Cell Polarity Signaling in Arabidopsis Involves a BFA-Sensitive Auxin Influx Pathway , 2002, Current Biology.

[24]  J. Schiefelbein,et al.  The rhd6 Mutation of Arabidopsis thaliana Alters Root-Hair Initiation through an Auxin- and Ethylene-Associated Process , 1994, Plant physiology.

[25]  J. Guern,et al.  Comparison of mechanisms controlling uptake and accumulation of 2,4-dichlorophenoxy acetic acid, naphthalene-1-acetic acid, and indole-3-acetic acid in suspension-cultured tobacco cells , 1996, Planta.

[26]  Alan Marchant,et al.  The Arabidopsis AUX1 gene: a model system to study mRNA processing in plants , 1998, Plant Molecular Biology.

[27]  G. Jürgens,et al.  Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. , 1999, Science.

[28]  R. Wepf,et al.  Roles for Rac1 and Cdc42 in planar polarization and hair outgrowth in the wing of Drosophila , 1996, The Journal of cell biology.

[29]  Ottoline Leyser,et al.  An Auxin-Dependent Distal Organizer of Pattern and Polarity in the Arabidopsis Root , 1999, Cell.

[30]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[31]  Klaus Palme,et al.  The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots , 2005, Nature.

[32]  B. Scheres,et al.  Mosaic analyses using marked activation and deletion clones dissect Arabidopsis SCARECROW action in asymmetric cell division. , 2004, Genes & development.

[33]  T. Vernoux,et al.  Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. , 2002, Development.

[34]  Alan Marchant,et al.  AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues , 1999, The EMBO journal.

[35]  D. Schachtman,et al.  High-Affinity Auxin Transport by the AUX1 Influx Carrier Protein , 2006, Current Biology.