Mechanical induction of lateral root initiation in Arabidopsis thaliana

Lateral roots are initiated postembryonically in response to environmental cues, enabling plants to explore efficiently their underground environment. However, the mechanisms by which the environment determines the position of lateral root formation are unknown. In this study, we demonstrate that in Arabidopsis thaliana lateral root initiation can be induced mechanically by either gravitropic curvature or by the transient bending of a root by hand. The plant hormone auxin accumulates at the site of lateral root induction before a primordium starts to form. Here we describe a subcellular relocalization of PIN1, an auxin transport protein, in a single protoxylem cell in response to gravitropic curvature. This relocalization precedes auxin-dependent gene transcription at the site of a new primordium. Auxin-dependent nuclear signaling is necessary for lateral root formation; arf7/19 double knock-out mutants normally form no lateral roots but do so upon bending when the root tip is removed. Signaling through arf7/19 can therefore be bypassed by root bending. These data support a model in which a root-tip-derived signal acts on downstream signaling molecules that specify lateral root identity.

[1]  S. Sabatini,et al.  SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. , 2003, Genes & development.

[2]  A. Theologis,et al.  ARF7 and ARF19 Regulate Lateral Root Formation via Direct Activation of LBD/ASL Genes in Arabidopsis[W] , 2007, The Plant Cell Online.

[3]  D. Inzé,et al.  Lateral Root Initiation or the Birth of a New Meristem , 2006, Plant Molecular Biology.

[4]  G. Hagen,et al.  Auxin Response Factors , 2001, Journal of Plant Growth Regulation.

[5]  M. Evans,et al.  Gravity-regulated differential auxin transport from columella to lateral root cap cells , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[6]  G. Jürgens,et al.  Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation , 2003, Cell.

[7]  E. Meyerowitz,et al.  Patterns of Auxin Transport and Gene Expression during Primordium Development Revealed by Live Imaging of the Arabidopsis Inflorescence Meristem , 2005, Current Biology.

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

[9]  Joseph R Ecker,et al.  NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. , 2005, The Plant journal : for cell and molecular biology.

[10]  P. Schopfer,et al.  Physical strain-mediated microtubule reorientation in the epidermis of gravitropically or phototropically stimulated maize coleoptiles. , 1998, The Plant journal : for cell and molecular biology.

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

[12]  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.

[13]  R Swarup,et al.  Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. , 2001, Genes & development.

[14]  E. Scarpella,et al.  Stage-specific markers define early steps of procambium development in Arabidopsis leaves and correlate termination of vein formation with mesophyll differentiation , 2004, Development.

[15]  R. Hellens,et al.  pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation , 2000, Plant Molecular Biology.

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

[17]  Tom Beeckman,et al.  Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis , 2007, Development.

[18]  N. Geldner,et al.  The plant endosomal system—its structure and role in signal transduction and plant development , 2004, Planta.

[19]  G. Hagen,et al.  Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. , 1997, The Plant cell.

[20]  M. Lenhard,et al.  Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers , 2007, Nature.

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

[22]  Tom Beeckman,et al.  The auxin influx carrier LAX3 promotes lateral root emergence , 2008, Nature Cell Biology.

[23]  Xiang Li,et al.  Cytokinin-mediated cell cycling arrest of pericycle founder cells in lateral root initiation of Arabidopsis. , 2006, Plant & cell physiology.

[24]  P. Benfey,et al.  Organization and cell differentiation in lateral roots of Arabidopsis thaliana. , 1997, Development.

[25]  Fabio Paolicchi,et al.  A turanose-insensitive mutant suggests a role for WOX5 in auxin homeostasis in Arabidopsis thaliana. , 2005, The Plant journal : for cell and molecular biology.

[26]  K. Ljung,et al.  Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. , 2002, The Plant journal : for cell and molecular biology.

[27]  H. Fukaki,et al.  Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. , 2002, The Plant journal : for cell and molecular biology.

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

[29]  G. Sandberg,et al.  AUX1 Promotes Lateral Root Formation by Facilitating Indole-3-Acetic Acid Distribution between Sink and Source Tissues in the Arabidopsis Seedling , 2002, The Plant Cell Online.

[30]  A. Theologis,et al.  Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 alters lateral root development in Arabidopsis. , 2005, The Plant journal : for cell and molecular biology.