Phosphate Availability Alters Lateral Root Development in Arabidopsis by Modulating Auxin Sensitivity via a Mechanism Involving the TIR1 Auxin Receptor[C][W][OA]

The survival of plants, as sessile organisms, depends on a series of postembryonic developmental events that determine the final architecture of plants and allow them to contend with a continuously changing environment. Modulation of cell differentiation and organ formation by environmental signals has not been studied in detail. Here, we report that alterations in the pattern of lateral root (LR) formation and emergence in response to phosphate (Pi) availability is mediated by changes in auxin sensitivity in Arabidopsis thaliana roots. These changes alter the expression of auxin-responsive genes and stimulate pericycle cells to proliferate. Modulation of auxin sensitivity by Pi was found to depend on the auxin receptor TRANSPORT INHIBITOR RESPONSE1 (TIR1) and the transcription factor AUXIN RESPONSE FACTOR19 (ARF19). We determined that Pi deprivation increases the expression of TIR1 in Arabidopsis seedlings and causes AUXIN/INDOLE-3-ACETIC ACID (AUX/IAA) auxin response repressors to be degraded. Based on our results, we propose a model in which auxin sensitivity is enhanced in Pi-deprived plants by an increased expression of TIR1, which accelerates the degradation of AUX/IAA proteins, thereby unshackling ARF transcription factors that activate/repress genes involved in LR formation and emergence.

[1]  B. Lahner,et al.  The Effect of Iron on the Primary Root Elongation of Arabidopsis during Phosphate Deficiency1[W][OA] , 2008, Plant Physiology.

[2]  M. Todesco,et al.  Target mimicry provides a new mechanism for regulation of microRNA activity , 2007, Nature Genetics.

[3]  L. Dolan,et al.  Ethylene Modulates Stem Cell Division in the Arabidopsis thaliana Root , 2007, Science.

[4]  Laurent Nussaume,et al.  Root tip contact with low-phosphate media reprograms plant root architecture , 2007, Nature Genetics.

[5]  T. Guilfoyle.  Plant biology: Sticking with auxin , 2007, Nature.

[6]  A. Murphy,et al.  Differential Effects of Sucrose and Auxin on Localized Phosphate Deficiency-Induced Modulation of Different Traits of Root System Architecture in Arabidopsis1[C][W][OA] , 2007, Plant Physiology.

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

[8]  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.

[9]  Christian Hermans,et al.  How do plants respond to nutrient shortage by biomass allocation? , 2006, Trends in plant science.

[10]  J. G. Dubrovsky,et al.  Mutations in the Diageotropica (Dgt) gene uncouple patterned cell division during lateral root initiation from proliferative cell division in the pericycle. , 2006, The Plant journal : for cell and molecular biology.

[11]  L. Herrera-Estrella,et al.  Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Jonathan D. G. Jones,et al.  A Plant miRNA Contributes to Antibacterial Resistance by Repressing Auxin Signaling , 2006, Science.

[13]  L. Herrera-Estrella,et al.  Characterization of low phosphorus insensitive Mutants Reveals a Crosstalk between Low Phosphorus-Induced Determinate Root Development and the Activation of Genes Involved in the Adaptation of Arabidopsis to Phosphorus Deficiency1 , 2006, Plant Physiology.

[14]  S. Somerville,et al.  A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Bertrand Muller,et al.  A Role for Auxin Redistribution in the Responses of the Root System Architecture to Phosphate Starvation in Arabidopsis1 , 2005, Plant Physiology.

[16]  Masashi Yamada,et al.  Plant development is regulated by a family of auxin receptor F box proteins. , 2005, Developmental cell.

[17]  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.

[18]  M. Estelle,et al.  The F-box protein TIR1 is an auxin receptor , 2005, Nature.

[19]  Ottoline Leyser,et al.  The Arabidopsis F-box protein TIR1 is an auxin receptor , 2005, Nature.

[20]  B. Bartel,et al.  Auxin: regulation, action, and interaction. , 2005, Annals of botany.

[21]  L. Herrera-Estrella,et al.  An Auxin Transport Independent Pathway Is Involved in Phosphate Stress-Induced Root Architectural Alterations in Arabidopsis. Identification of BIG as a Mediator of Auxin in Pericycle Cell Activation1 , 2005, Plant Physiology.

[22]  L. Herrera-Estrella,et al.  Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. , 2005, Plant & cell physiology.

[23]  C. Ticconi,et al.  Short on phosphate: plant surveillance and countermeasures. , 2004, Trends in plant science.

[24]  M. Estelle,et al.  Auxin signaling and regulated protein degradation. , 2004, Trends in plant science.

[25]  Mark Stitt,et al.  Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. , 2004, The Plant journal : for cell and molecular biology.

[26]  L. Herrera-Estrella,et al.  Improving transformation efficiency ofArabidopsis thaliana by modifying the floral dip method , 2004, Plant Molecular Biology Reporter.

[27]  François Tardieu,et al.  Temporal responses of Arabidopsis root architecture to phosphate starvation: evidence for the involvement of auxin signalling , 2003 .

[28]  L. Herrera-Estrella,et al.  The role of nutrient availability in regulating root architecture. , 2003, Current opinion in plant biology.

[29]  G. Sandberg,et al.  Dissecting Arabidopsis lateral root development. , 2003, Trends in plant science.

[30]  C. Vance,et al.  Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. , 2003, The New phytologist.

[31]  Dirk Inzé,et al.  Auxin-Mediated Cell Cycle Activation during Early Lateral Root Initiation Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.004960. , 2002, The Plant Cell Online.

[32]  A. Karthikeyan,et al.  Regulated Expression of Arabidopsis Phosphate Transporters1 , 2002, Plant Physiology.

[33]  Luis Herrera-Estrella,et al.  Phosphate Availability Alters Architecture and Causes Changes in Hormone Sensitivity in the Arabidopsis Root System1 , 2002, Plant Physiology.

[34]  G. Neumann,et al.  Cluster roots--an underground adaptation for survival in extreme environments. , 2002, Trends in plant science.

[35]  G. Hagen,et al.  AUX/IAA Proteins Are Active Repressors, and Their Stability and Activity Are Modulated by Auxin Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010289. , 2001, The Plant Cell Online.

[36]  Ottoline Leyser,et al.  Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins , 2001, Nature.

[37]  J. Callis,et al.  Auxin modulates the degradation rate of Aux/IAA proteins , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[38]  H. Leyser,et al.  Phosphate availability regulates root system architecture in Arabidopsis. , 2001, Plant physiology.

[39]  D. Inzé,et al.  Auxin Transport Promotes Arabidopsis Lateral Root Initiation , 2001, Plant Cell.

[40]  A. Theologis,et al.  IAA17/AXR3: Biochemical Insight into an Auxin Mutant Phenotype , 2001, Plant Cell.

[41]  A. Karthikeyan,et al.  LEPS2, a phosphorus starvation-induced novel acid phosphatase from tomato. , 2001, Plant physiology.

[42]  C. Vance,et al.  Proteoid Root Development of Phosphorus Deficient Lupin is Mimicked by Auxin and Phosphonate , 2000 .

[43]  N. Fedoroff,et al.  Genetic ablation of root cap cells in Arabidopsis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Travis W. Banks,et al.  Identification of an SCF ubiquitin-ligase complex required for auxin response in Arabidopsis thaliana. , 1999, Genes & development.

[45]  P W Barlow,et al.  Dual pathways for regulation of root branching by nitrate. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[46]  G. Muday,et al.  Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. , 1998, Plant physiology.

[47]  A. Theologis,et al.  age Mutants of Arabidopsis Exhibit Altered Auxin-Regulated Gene Expression , 1998, Plant Cell.

[48]  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.

[49]  M. Estelle,et al.  The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast grr1p. , 1998, Genes & development.

[50]  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.

[51]  J. Lynch,et al.  Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability , 1996 .

[52]  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.

[53]  H. Nusbaum,et al.  Formation of lateral root meristems is a two-stage process. , 1995, Development.

[54]  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.

[55]  J. Floris,et al.  An inflatable minirhizotron system for root observations with improved soil/tube contact , 1991, Plant and Soil.

[56]  P. Colowit,et al.  Experimental Studies on Lateral Root Formation in Radish Seedling Roots: II. Analysis of the Dose-Response to Exogenous Auxin. , 1988, Plant physiology.

[57]  J. Torrey.  THE INDUCTION OF LATERAL ROOTS BY INDOLEACETIC ACID AND ROOT DECAPITATION , 1950 .

[58]  J. Malamy,et al.  Intrinsic and environmental response pathways that regulate root system architecture. , 2005, Plant, cell & environment.

[59]  A. Karthikeyan,et al.  Phosphate Acquisition , 2004, Plant and Soil.

[60]  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.

[61]  M. Estelle,et al.  Access the most recent version at doi: 10.1101/gad.12.2.198 References , 2022 .

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

[63]  I. C. R. Holford,et al.  Soil phosphorus: its measurement, and its uptake by plants , 1997 .

[64]  S. Gallagher.  3 – Quantitation of GUS Activity by Fluorometry , 1992 .

[65]  S. Gallagher.  GUS protocols: using the GUS gene as a reporter of gene expression. , 1992 .

[66]  N. Claassen,et al.  II. Significance of root radius, root hairs and cation-anion balance for phosphorus influx in seven plant species , 1991 .