Distance Maps and Plant Development #2: Facilitated Transport and Uniform Gradient

The principles underlying plant development are extended to allow a more molecular mechanism to elaborate the schema by which ground cells dierentiate into vascular cells. Biophysical considerations dictate that linear dynamics are not sucent to capture facilitated auxin transport (e.g., through PIN). We group these transport facilitators into a non-linear model under the assumption that they attempt to minimize certain dierences of auxin concentration. This Constant Gradient Hypothesis greatly increases the descriptive power of our model to include complex dynamical behaviour. Specically, we show how the early pattern of PIN1 expression appears in the embryo, how the leaf primordium emerges, how convergence points arise on the leaf margin, how the rst loop is formed, and how the intricate pattern of PIN shifts during the early establishment of vein patterns in incipient leaves of Arabidopsis. Given our results, we submit that the model provides evidence that many of the salient structural characteristics that have been described at various stages of plant development can arise from the uniform application of a small number of abstract principles.

[1]  A. Sheldrake,et al.  Effect of pH and surface charge on cell uptake of auxin. , 1973, Nature: New biology.

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

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

[4]  Ross C. Bean,et al.  Permeability of Lipid Bilayer Membranes to Organic Solutes , 1968, The Journal of general physiology.

[5]  A. Murphy,et al.  Multidrug Resistance–like Genes of Arabidopsis Required for Auxin Transport and Auxin-Mediated Development Article, publication date, and citation information can be found at www.aspb.org/cgi/doi/10.1105/tpc.010350. , 2001, The Plant Cell Online.

[6]  M. Bennett,et al.  Regulation of phyllotaxis by polar auxin transport , 2003, Nature.

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

[8]  A. Murphy,et al.  Flavonoids act as negative regulators of auxin transport in vivo in arabidopsis. , 2001, Plant physiology.

[9]  Klaus Palme,et al.  Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis , 2002, Nature.

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

[11]  J. Chory,et al.  BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. , 2001, Genes & development.

[12]  G. Sandberg,et al.  AXR4 Is Required for Localization of the Auxin Influx Facilitator AUX1 , 2006, Science.

[13]  Rob Phillips,et al.  A First Exposure to Statistical Mechanics for Life Scientists , 2007, 0708.1899.

[14]  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.

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

[16]  N. Provart,et al.  Embryogenesis: Pattern Formation from a Single Cell , 2009, The arabidopsis book.

[17]  A. Murphy,et al.  Enhanced gravi- and phototropism in plant mdr mutants mislocalizing the auxin efflux protein PIN1 , 2003, Nature.

[18]  D. Koshland,et al.  An amplified sensitivity arising from covalent modification in biological systems. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[19]  M. Bennett,et al.  New insight into the biochemical mechanisms regulating auxin transport in plants. , 2007, The Biochemical journal.

[20]  J. Changeux,et al.  ON THE NATURE OF ALLOSTERIC TRANSITIONS: A PLAUSIBLE MODEL. , 1965, Journal of molecular biology.

[21]  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.

[22]  W. J. Lucas,et al.  Plasmodesmata as a supracellular control network in plants , 2004, Nature Reviews Molecular Cell Biology.

[23]  J. Friml,et al.  Polar auxin transport – old questions and new concepts? , 2002, Plant Molecular Biology.

[24]  Zerihun Tadele,et al.  PIN Proteins Perform a Rate-Limiting Function in Cellular Auxin Efflux , 2006, Science.

[25]  John A. Raven,et al.  TRANSPORT OF INDOLEACETIC ACID IN PLANT CELLS IN RELATION TO pH AND ELECTRICAL POTENTIAL GRADIENTS, AND ITS SIGNIFICANCE FOR POLAR IAA TRANSPORT , 1975 .

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

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

[28]  Tom Beeckman,et al.  Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression , 2005, Development.

[29]  J. O´Rourke,et al.  Computational Geometry in C: Arrangements , 1998 .

[30]  A. Murphy,et al.  Auxin transport. , 2005, Current opinion in plant biology.

[31]  A. Sheldrake,et al.  Carrier-mediated auxin transport , 1974, Planta.

[32]  J. Friml,et al.  Control of leaf vascular patterning by polar auxin transport. , 2006, Genes & development.

[33]  Klaus Palme,et al.  AtPIN4 Mediates Sink-Driven Auxin Gradients and Root Patterning in Arabidopsis , 2002, Cell.

[34]  Gerald R. Fink,et al.  Post-transcriptional control of the Arabidopsis auxin efflux carrier EIR1 requires AXR1 , 2000, Current Biology.

[35]  Jiří Friml,et al.  Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism , 2006, Nature Cell Biology.

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

[37]  D. Tosteson,et al.  Diffusion of Weak Acids across Lipid Bilayer Membranes: Effects of Chemical Reactions in the Unstirred Layers , 1973, Science.

[38]  Gordon F. Royle,et al.  Algebraic Graph Theory , 2001, Graduate texts in mathematics.

[39]  T. Sachs The Control of the Patterned Differentiation of Vascular Tissues , 1981 .

[40]  B. Scheres,et al.  Non-cell-autonomous rescue of anaphase-promoting complex function revealed by mosaic analysis of HOBBIT, an Arabidopsis CDC27 homolog , 2006, Proceedings of the National Academy of Sciences.

[41]  Mark Ptashne,et al.  A Genetic Switch, Phage Lambda Revisited , 2004 .

[42]  Joseph O'Rourke,et al.  Computational Geometry in C. , 1995 .

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

[44]  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.

[45]  John Gutknecht,et al.  Transport of auxin (indoleacetic acid) through lipid bilayer membranes , 1980, The Journal of Membrane Biology.

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

[47]  N. Biggs Algebraic Graph Theory: COLOURING PROBLEMS , 1974 .

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

[49]  A. Murphy,et al.  Regulation of auxin transport by aminopeptidases and endogenous flavonoids , 2000, Planta.

[50]  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.

[51]  M. Martin,et al.  Mathematical analysis of the chemosmotic polar diffusion of auxin through plant tissues. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Diana Santelia,et al.  MDR‐like ABC transporter AtPGP4 is involved in auxin‐mediated lateral root and root hair development , 2005, FEBS letters.

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

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