APSR1, a novel gene required for meristem maintenance, is negatively regulated by low phosphate availability.

Proper root growth is crucial for anchorage, exploration, and exploitation of the soil substrate. Root growth is highly sensitive to a variety of environmental cues, among them water and nutrient availability have a great impact on root development. Phosphorus (P) availability is one of the most limiting nutrients that affect plant growth and development under natural and agricultural environments. Root growth in the direction of the long axis proceeds from the root tip and requires the coordinated activities of cell proliferation, cell elongation and cell differentiation. Here we report a novel gene, APSR1 (Altered Phosphate Starvation Response1), involved in root meristem maintenance. The loss of function mutant apsr1-1 showed a reduction in primary root length and root apical meristem size, short differentiated epidermal cells and long root hairs. Expression of APSR1 gene decreases in response to phosphate starvation and apsr1-1 did not show the typical progressive decrease of undifferentiated cells at root tip when grown under P limiting conditions. Interestingly, APSR1 expression pattern overlaps with root zones of auxin accumulation. Furthermore, apsr1-1 showed a clear decrease in the level of the auxin transporter PIN7. These data suggest that APSR1 is required for the coordination of cell processes necessary for correct root growth in response to phosphate starvation conceivably by direct or indirect modulation of PIN7. We also propose, based on its nuclear localization and structure, that APSR1 may potentially be a member of a novel group of transcription factors.

[1]  B. Bartel,et al.  Ethylene directs auxin to control root cell expansion. , 2010, The Plant journal : for cell and molecular biology.

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

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

[4]  A. Karthikeyan,et al.  Ethylene signalling is involved in regulation of phosphate starvation-induced gene expression and production of acid phosphatases and anthocyanin in Arabidopsis. , 2011, The New phytologist.

[5]  P. Doerner,et al.  Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. , 1999, The Plant journal : for cell and molecular biology.

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

[7]  D. Jones,et al.  Through form to function: root hair development and nutrient uptake. , 2000, Trends in plant science.

[8]  A. Murphy,et al.  Vesicular cycling mechanisms that control auxin transport polarity. , 2003, Trends in plant science.

[9]  D. Schachtman,et al.  Nutrient sensing and signaling: NPKS. , 2007, Annual review of plant biology.

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

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

[12]  C. Ticconi,et al.  Phosphate sensing in higher plants. , 2002, Physiologia plantarum.

[13]  K. Ljung,et al.  Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. , 2002, The Plant journal : for cell and molecular biology.

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

[15]  Steffen Vanneste,et al.  Auxin: A Trigger for Change in Plant Development , 2009, Cell.

[16]  N. Goto,et al.  Auxin and Ethylene Response Interactions during Arabidopsis Root Hair Development Dissected by Auxin Influx Modulators , 2002, Plant Physiology.

[17]  P. Benfey,et al.  Signaling in and out: control of cell division and differentiation in the shoot and root. , 2002, The Plant cell.

[18]  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.

[19]  M. McManus,et al.  Regulation of root growth by auxin and ethylene is influenced by phosphate supply in white clover (Trifolium repens L.) , 2012, Plant Growth Regulation.

[20]  J. Friml,et al.  Auxin transport - shaping the plant. , 2003, Current opinion in plant biology.

[21]  G. Muday,et al.  Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. , 2010, The Plant journal : for cell and molecular biology.

[22]  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.

[23]  J. Alonso,et al.  Multilevel Interactions between Ethylene and Auxin in Arabidopsis Roots[W] , 2007, The Plant Cell Online.

[24]  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.

[25]  Dong Liu,et al.  The Arabidopsis gene hypersensitive to phosphate starvation 3 encodes ethylene overproduction 1. , 2012, Plant & cell physiology.

[26]  L. Dolan,et al.  Cell expansion in roots. , 2004, Current opinion in plant biology.

[27]  G. Fink,et al.  A pathway for lateral root formation in Arabidopsis thaliana. , 1995, Genes & development.

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

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

[30]  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.

[31]  L. Herrera-Estrella,et al.  Phosphate Availability Alters Lateral Root Development in Arabidopsis by Modulating Auxin Sensitivity via a Mechanism Involving the TIR1 Auxin Receptor[C][W][OA] , 2008, The Plant Cell Online.

[32]  W. Lukowitz,et al.  Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you. , 2000, Plant physiology.

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

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

[35]  H. Bohnert,et al.  SIZ1 Regulation of Phosphate Starvation-Induced Root Architecture Remodeling Involves the Control of Auxin Accumulation1[C][W][OA] , 2010, Plant Physiology.

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

[37]  L. Herrera-Estrella,et al.  Global expression pattern comparison between low phosphorus insensitive 4 and WT Arabidopsis reveals an important role of reactive oxygen species and jasmonic acid in the root tip response to phosphate starvation , 2011, Plant signaling & behavior.

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

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

[40]  Daniel R. Lewis,et al.  Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers , 2011, Development.

[41]  R. Last,et al.  Arabidopsis Map-Based Cloning in the Post-Genome Era , 2002, Plant Physiology.

[42]  J. Friml,et al.  Spatiotemporal asymmetric auxin distribution: a means to coordinate plant development , 2006, Cellular and Molecular Life Sciences CMLS.

[43]  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.

[44]  N. Tuteja,et al.  Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. , 2010, Plant physiology and biochemistry : PPB.

[45]  Claire S. Grierson,et al.  Clonal relationships and cell patterning in the root epidermis of Arabidopsis , 1994 .