Towards the systems biology of auxin-transport-mediated patterning.

Polar auxin transport intimately connects plant cell polarity and multicellular patterning. Through the transport of the small molecule indole-3-acetic acid, plant cells integrate their polarities and communicate the degree of their polarization. In this way, they generate an apical-basal axis that serves as a positional reference anchoring subsequent patterning events. Research in recent years has brought the molecular mechanisms underlying auxin perception and auxin transport to light. This knowledge has been used to derive spectacular molecular visualization tools and animated computer simulations, which are now allied in a joint systems biology effort towards a mathematical description of auxin-transport-mediated patterning processes.

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

[2]  Ben Scheres,et al.  Polar PIN Localization Directs Auxin Flow in Plants , 2006, Science.

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

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

[5]  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.

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

[7]  H. Meinhardt,et al.  Biological pattern formation: fmm basic mechanisms ta complex structures , 1994 .

[8]  E. Meyerowitz,et al.  Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana , 2004, Development.

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

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

[11]  L Wolpert,et al.  One hundred years of positional information. , 1996, Trends in genetics : TIG.

[12]  T. Sachs,et al.  Collective specification of cellular development. , 2003, BioEssays : news and reviews in molecular, cellular and developmental biology.

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

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

[15]  E. C. Jeffrey Die Phylogenie der Pflanzen , 1930 .

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

[17]  Martin Frenz,et al.  Microsurgical and laser ablation analysis of interactions between the zones and layers of the tomato shoot apical meristem , 2003, Development.

[18]  Graeme Mitchison,et al.  The dynamics of auxin transport , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[19]  N. Chua,et al.  Auxin Polar Transport Is Essential for the Establishment of Bilateral Symmetry during Early Plant Embryogenesis. , 1993, The Plant cell.

[20]  C. Kuhlemeier,et al.  Auxin Regulates the Initiation and Radial Position of Plant Lateral Organs , 2000, Plant Cell.

[21]  P. Prusinkiewicz,et al.  A plausible model of phyllotaxis , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Wenzislava Ckurshumova,et al.  Auxin Signaling in Arabidopsis Leaf Vascular Development1 , 2003, Plant Physiology.

[23]  R. F. Lyndon Plant Development: The Cellular Basis , 1990 .

[24]  E. Mjolsness,et al.  An auxin-driven polarized transport model for phyllotaxis , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

[26]  Y. Iwasa,et al.  Self-organization of the vascular system in plant leaves: inter-dependent dynamics of auxin flux and carrier proteins. , 2005, Journal of theoretical biology.

[27]  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.

[28]  L. Wolpert Positional information and the spatial pattern of cellular differentiation. , 1969, Journal of theoretical biology.

[29]  E. Kramer,et al.  How Far Can a Molecule of Weak Acid Travel in the Apoplast or Xylem?1[W] , 2006, Plant Physiology.

[30]  L. Held,et al.  Models for embryonic periodicity. , 1992, Monographs in developmental biology.

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

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

[33]  T. Sachs Integrating cellular and organismic aspects of vascular differentiation. , 2000, Plant & cell physiology.

[34]  G. Mitchison,et al.  The polar transport of auxin and vein patterns in plants , 1981 .

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

[36]  C. Hardtke,et al.  The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development , 1998, The EMBO journal.

[37]  Hironori Fujita,et al.  Pattern formation of leaf veins by the positive feedback regulation between auxin flow and auxin efflux carrier. , 2006, Journal of theoretical biology.

[38]  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.

[39]  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 .

[40]  M. Estelle,et al.  Arabidopsis AXR6 encodes CUL1 implicating SCF E3 ligases in auxin regulation of embryogenesis , 2003, The EMBO journal.

[41]  G. Hagen,et al.  ARF1, a transcription factor that binds to auxin response elements. , 1997, Science.

[42]  P. Prusinkiewicz,et al.  Reviewing models of auxin canalization in the context of leaf vein pattern formation in Arabidopsis. , 2005, The Plant journal : for cell and molecular biology.

[43]  G. Hagen,et al.  Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4 , 2004, Development.

[44]  T. Sachs The Control of the Differentiation of Vascular Networks , 1975 .

[45]  G. Mitchison A model for vein formation in higher plants , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[46]  Patrick Laufs,et al.  In Vivo Analysis of Cell Division, Cell Growth, and Differentiation at the Shoot Apical Meristem in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.017962. , 2004, The Plant Cell Online.

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

[48]  O. Leyser,et al.  Plant Development: Auxin in Loops , 2005, Current Biology.

[49]  Michael Sauer,et al.  A Molecular Framework for Plant Regeneration , 2006, Science.

[50]  Scott F. Gilbert,et al.  Developmental Biology, 6th edition , 2000 .

[51]  T. Sachs,et al.  Polarity and the Induction of Organized Vascular Tissues , 1969 .

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

[53]  L. Sieburth,et al.  Auxin is required for leaf vein pattern in Arabidopsis. , 1999, Plant physiology.

[54]  E. Kramer,et al.  PIN and AUX/LAX proteins: their role in auxin accumulation. , 2004, Trends in plant science.

[55]  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.

[56]  T. Steeves,et al.  Patterns in plant development: Subject index , 1972 .

[57]  A. M. Turing,et al.  The chemical basis of morphogenesis , 1952, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[58]  R. Amasino,et al.  The PLETHORA Genes Mediate Patterning of the Arabidopsis Root Stem Cell Niche , 2004, Cell.

[59]  P. Prusinkiewicz,et al.  Modeling and visualization of leaf venation patterns , 2005, SIGGRAPH 2005.

[60]  O. Leyser,et al.  Something on the Side: Axillary Meristems and Plant Development , 2006, Plant Molecular Biology.

[61]  G. Jürgens,et al.  The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. , 2002, Genes & development.

[62]  G. Neuhaus,et al.  Auxin-induced developmental patterns in Brassica juncea embryos. , 1998, Development.

[63]  Ottoline Leyser,et al.  Auxin Distribution and Plant Pattern Formation: How Many Angels Can Dance on the Point of PIN? , 2005, Cell.

[64]  Ben Scheres,et al.  Polar auxin transport and patterning: grow with the flow. , 2006, Genes & development.

[65]  Pavel Dimitrov,et al.  A constant production hypothesis guides leaf venation patterning. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[66]  Markus Langhans,et al.  Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis , 2003, Planta.

[67]  P. J. Davies Plant hormones : physiology, biochemistry and molecular biology , 1995 .

[68]  P. Benfey,et al.  Intercellular movement of the putative transcription factor SHR in root patterning , 2001, Nature.

[69]  Klaus Palme,et al.  Auxin transport inhibitors block PIN1 cycling and vesicle trafficking , 2001, Nature.

[70]  Charlie Chang,et al.  Functional Genomic Analysis of the AUXIN RESPONSE FACTOR Gene Family Members in Arabidopsis thaliana: Unique and Overlapping Functions of ARF7 and ARF19w⃞ , 2005, The Plant Cell Online.

[71]  H. Meinhardt,et al.  A theory of biological pattern formation , 1972, Kybernetik.

[72]  H. Meinhardt Models of biological pattern formation , 1982 .

[73]  G. Muday,et al.  Polar auxin transport: controlling where and how much. , 2001, Trends in plant science.

[74]  Yoh Iwasa,et al.  How canalization can make loops: a new model of reticulated leaf vascular pattern formation. , 2006, Journal of theoretical biology.

[75]  Pierre Barbier de Reuille,et al.  Computer simulations reveal novel properties of the cell-cell signaling network at the shoot apex in /Arabidopsis , 2005 .

[76]  M. Estelle,et al.  Auxin receptors: a new role for F-box proteins. , 2006, Current opinion in cell biology.

[77]  J. Bowman,et al.  Establishment of polarity in angiosperm lateral organs. , 2002, Trends in genetics : TIG.

[78]  T. Berleth,et al.  Responses of plant vascular systems to auxin transport inhibition. , 1999, Development.

[79]  R. Racusen,et al.  Microsurgery reveals regional capabilities for pattern reestablishment in somatic carrot embryos. , 1990, Developmental biology.

[80]  Ottoline Leyser,et al.  Dynamic Integration of Auxin Transport and Signalling , 2006, Current Biology.