AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues

Plants employ a specialized transport system composed of separate influx and efflux carriers to mobilize the plant hormone auxin between its site(s) of synthesis and action. Mutations within the permease‐like AUX1 protein significantly reduce the rate of carrier‐mediated auxin uptake within Arabidopsis roots, conferring an agravitropic phenotype. We are able to bypass the defect within auxin uptake and restore the gravitropic root phenotype of aux1 by growing mutant seedlings in the presence of the membrane‐permeable synthetic auxin, 1‐naphthaleneacetic acid. We illustrate that AUX1 expression overlaps that previously described for the auxin efflux carrier, AtPIN2, using transgenic lines expressing an AUX1 promoter::uidA (GUS) gene. Finally, we demonstrate that AUX1 regulates gravitropic curvature by acting in unison with the auxin efflux carrier to co‐ordinate the localized redistribution of auxin within the Arabidopsis root apex. Our results provide the first example of a developmental role for the auxin influx carrier within higher plants and supply new insight into the molecular basis of gravitropic signalling.

[1]  G. Fink,et al.  EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. , 1998, Genes & development.

[2]  D. Söll,et al.  A mutation in protein phosphatase 2A regulatory subunit A affects auxin transport in Arabidopsis. , 1996, The EMBO journal.

[3]  B. Scheres,et al.  Cellular organisation of the Arabidopsis thaliana root. , 1993, Development.

[4]  M. Evans.  What remains of the Cholodny-Went theory? , 1992, Plant, cell & environment.

[5]  D. Morris,et al.  Effects of Inhibitors of Protein Synthesis on Transmembrane Auxin Transport in Cucurbita pepo L. Hypocotyl Segments , 1991 .

[6]  M. Evans,et al.  Gravitropism: interaction of sensitivity modulation and effector redistribution. , 1991, Plant physiology.

[7]  D. Morris,et al.  A Microautoradiographic Study of Auxin Transport in the Stem of Intact Pea Seedlings (Pisum sativum L.) , 1978 .

[8]  R Chen,et al.  Arabidopsis thalianaのAGRAVITROPIC 1遺伝子は極性オーキシン輸送の流出キャリアの構成員をコード化する , 1998 .

[9]  B. Pickard,et al.  Auxin asymmetry during gravitropism by tomato hypocotyls. , 1989, Plant physiology.

[10]  M. Evans,et al.  Correlations between gravitropic curvature and auxin movement across gravistimulated roots of Zea mays. , 1990, Plant physiology.

[11]  M. Iino.  Mediation of tropisms by lateral translocation of endogenous indole‐3‐acetic acid in maize coleoptiles , 1991 .

[12]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[13]  O. Leyser,et al.  Changes in auxin response from mutations in an AUX/IAA gene. , 1998, Science.

[14]  J. Ellis,et al.  In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants , 1993 .

[15]  Allison K. Wilson,et al.  The aux1 Mutation of Arabidopsis Confers Both Auxin and Ethylene Resistance. , 1990, Plant physiology.

[16]  K. Feldmann,et al.  T-DNA Insertion Mutagenesis in Arabidopsis: Prospects and Perspectives , 1992 .

[17]  K. Feldmann,et al.  Arabidopsis AUX1 Gene: A Permease-Like Regulator of Root Gravitropism , 1996, Science.

[18]  N. Graham,et al.  Cell marking in Arabidopsis thaliana and its application to patch-clamp studies. , 1998, The Plant journal : for cell and molecular biology.

[19]  E. Blancaflor,et al.  Mapping the functional roles of cap cells in the response of Arabidopsis primary roots to gravity. , 1998, Plant physiology.

[20]  S. Tsurumi,et al.  Transport of 14C-lableled indoleacetic acid in Vicia root segments , 1978 .

[21]  A. Theologis,et al.  The PS-IAA4/5-like family of early auxin-inducible mRNAs in Arabidopsis thaliana. , 1995, Journal of molecular biology.

[22]  J. Ecker,et al.  Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. , 1995, Genetics.

[23]  S. May,et al.  Going the distance with auxin: unravelling the molecular basis of auxin transport. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[24]  W. Briggs,et al.  Transport of Indole-3-Acetic Acid during Gravitropism in Intact Maize Coleoptiles. , 1990, Plant physiology.

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

[26]  J. Suttle.  Effect of Ethylene Treatment on Polar IAA Transport, Net IAA Uptake and Specific Binding of N-1-Naphthylphthalamic Acid in Tissues and Microsomes Isolated from Etiolated Pea Epicotyls. , 1988, Plant physiology.

[27]  B. Forde,et al.  Efficient transformation of Agrobacterium spp. by high voltage electroporation. , 1989, Nucleic acids research.

[28]  M. Estelle,et al.  Reduced naphthylphthalamic acid binding in the tir3 mutant of Arabidopsis is associated with a reduction in polar auxin transport and diverse morphological defects. , 1997, The Plant cell.

[29]  B. André,et al.  Amino acid transport in plants , 1998 .

[30]  P. Masson,et al.  The arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[31]  T Hashimoto,et al.  Agr, an Agravitropic locus of Arabidopsis thaliana, encodes a novel membrane-protein family member. , 1998, Plant & cell physiology.

[32]  D. Rayle,et al.  Effect of asymmetric auxin application on Helianthus hypocotyl curvature. , 1989, Plant physiology.

[33]  W. Briggs,et al.  Transport of indoleacetic Acid in intact corn coleoptiles. , 1990, Plant physiology.

[34]  F. B. Pickett,et al.  Mutations in the AXR3 gene of Arabidopsis result in altered auxin response including ectopic expression from the SAUR-AC1 promoter. , 1996, The Plant journal : for cell and molecular biology.

[35]  M. Bevan,et al.  GUS fusions: beta‐glucuronidase as a sensitive and versatile gene fusion marker in higher plants. , 1987, The EMBO journal.

[36]  M. Goldsmith,et al.  The Polar Transport of Auxin , 1977 .

[37]  C. Bell,et al.  Requirement of the Auxin Polar Transport System in Early Stages of Arabidopsis Floral Bud Formation. , 1991, The Plant cell.

[38]  A. Trewavas.  What remains of the Cholodny-Went theory? Introduction. , 1992, Plant, cell & environment.

[39]  G. F. Katekar,et al.  Auxin Transport Inhibitors: III. Chemical Requirements of a Class of Auxin Transport Inhibitors. , 1977, Plant physiology.

[40]  D. Morris,et al.  Targeting of auxin carriers to the plasma membrane: differential effects of brefeldin A on the traffic of auxin uptake and efflux carriers , 1998, Planta.

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