Interaction of PLS and PIN and hormonal crosstalk in Arabidopsis root development

Understanding how hormones and genes interact to coordinate plant growth is a major challenge in developmental biology. The activities of auxin, ethylene, and cytokinin depend on cellular context and exhibit either synergistic or antagonistic interactions. Here we use experimentation and network construction to elucidate the role of the interaction of the POLARIS peptide (PLS) and the auxin efflux carrier PIN proteins in the crosstalk of three hormones (auxin, ethylene, and cytokinin) in Arabidopsis root development. In ethylene hypersignaling mutants such as polaris (pls), we show experimentally that expression of both PIN1 and PIN2 significantly increases. This relationship is analyzed in the context of the crosstalk between auxin, ethylene, and cytokinin: in pls, endogenous auxin, ethylene and cytokinin concentration decreases, approximately remains unchanged and increases, respectively. Experimental data are integrated into a hormonal crosstalk network through combination with information in literature. Network construction reveals that the regulation of both PIN1 and PIN2 is predominantly via ethylene signaling. In addition, it is deduced that the relationship between cytokinin and PIN1 and PIN2 levels implies a regulatory role of cytokinin in addition to its regulation to auxin, ethylene, and PLS levels. We discuss how the network of hormones and genes coordinates plant growth by simultaneously regulating the activities of auxin, ethylene, and cytokinin signaling pathways.

[1]  Sean May,et al.  Cytokinin Regulation of Auxin Synthesis in Arabidopsis Involves a Homeostatic Feedback Loop Regulated via Auxin and Cytokinin Signal Transduction[W][OA] , 2010, Plant Cell.

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

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

[4]  J. Friml,et al.  Polar targeting and endocytic recycling in auxin-dependent plant development. , 2008, Annual review of cell and developmental biology.

[5]  Alan M. Jones,et al.  Cytokinin Interplay with Ethylene, Auxin, and Glucose Signaling Controls Arabidopsis Seedling Root Directional Growth1[W][OA] , 2011, Plant Physiology.

[6]  Claire S. Grierson,et al.  Auxin transport through non-hair cells sustains root-hair development , 2008, Nature Cell Biology.

[7]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]/Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

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

[9]  K. Ljung,et al.  Ethylene Regulates Root Growth through Effects on Auxin Biosynthesis and Transport-Dependent Auxin Distribution[W] , 2007, The Plant Cell Online.

[10]  K. Ljung,et al.  Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis , 2009, Nature Cell Biology.

[11]  Reeta Prusty,et al.  Expression profiling of auxin-treated Arabidopsis roots: toward a molecular analysis of lateral root emergence. , 2006, Plant & cell physiology.

[12]  Eric Mjolsness,et al.  A plausible mechanism for auxin patterning along the developing root , 2010, BMC Systems Biology.

[13]  P. Hogeweg,et al.  Auxin transport is sufficient to generate a maximum and gradient guiding root growth , 2007, Nature.

[14]  A. Murphy,et al.  Seven things we think we know about auxin transport. , 2011, Molecular plant.

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

[16]  Keith Lindsey,et al.  The POLARIS Peptide of Arabidopsis Regulates Auxin Transport and Root Growth via Effects on Ethylene Signaling[OA] , 2006, The Plant Cell Online.

[17]  Keith Lindsey,et al.  Modelling and experimental analysis of hormonal crosstalk in Arabidopsis , 2010, Molecular systems biology.

[18]  Gerrit T. S. Beemster,et al.  Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal , 2005, Nature Cell Biology.

[19]  Keith Lindsey,et al.  The POLARIS Gene of Arabidopsis Encodes a Predicted Peptide Required for Correct Root Growth and Leaf Vascular Patterning Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.002618. , 2002, The Plant Cell Online.

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

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

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

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

[24]  Anders Nordström,et al.  Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokinin-regulated development. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Henrik Jönsson,et al.  Modeling auxin-regulated development. , 2010, Cold Spring Harbor perspectives in biology.

[26]  M. Estelle,et al.  Mechanism of auxin-regulated gene expression in plants. , 2009, Annual review of genetics.

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

[28]  L. Dolan,et al.  Ethylene is a positive regulator of root hair development in Arabidopsis thaliana. , 1995, The Plant journal : for cell and molecular biology.

[29]  J. Friml,et al.  The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells , 2010, The EMBO journal.

[30]  J. Normanly Approaching cellular and molecular resolution of auxin biosynthesis and metabolism. , 2010, Cold Spring Harbor perspectives in biology.

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

[32]  E. Benková,et al.  Hormonal interactions in the regulation of plant development. , 2012, Annual review of cell and developmental biology.

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

[34]  Michael J Holdsworth,et al.  Mathematical modeling elucidates the role of transcriptional feedback in gibberellin signaling , 2012, Proceedings of the National Academy of Sciences.

[35]  G. Sandberg,et al.  Auxin-Cytokinin Interactions in Wild-Type and Transgenic Tobacco , 1997 .

[36]  Jan Petrásek,et al.  Cytokinin regulates root meristem activity via modulation of the polar auxin transport , 2009, Proceedings of the National Academy of Sciences.

[37]  J. Molenaar,et al.  A Mathematical Model for BRASSINOSTEROID INSENSITIVE1-Mediated Signaling in Root Growth and Hypocotyl Elongation1[W] , 2012, Plant Physiology.

[38]  J. Chandler Auxin as compère in plant hormone crosstalk , 2009, Planta.

[39]  Eugenio Azpeitia,et al.  Hormone symphony during root growth and development , 2012, Developmental dynamics : an official publication of the American Association of Anatomists.

[40]  Roeland M. H. Merks,et al.  Emergence of tissue polarization from synergy of intracellular and extracellular auxin signaling , 2010, Molecular systems biology.

[41]  K. Lindsey,et al.  Promoter trap markers differentiate structural and positional components of polar development in Arabidopsis. , 1997, The Plant cell.

[42]  Christian S. Hardtke,et al.  Hormone Signalling Crosstalk in Plant Growth Regulation , 2011, Current Biology.

[43]  Yunde Zhao Auxin biosynthesis and its role in plant development. , 2010, Annual review of plant biology.

[44]  Jan Petrásek,et al.  Auxin transport routes in plant development , 2009, Development.

[45]  Renze Heidstra,et al.  Cytokinins Determine Arabidopsis Root-Meristem Size by Controlling Cell Differentiation , 2007, Current Biology.

[46]  Rishikesh Bhalerao,et al.  Ethylene Upregulates Auxin Biosynthesis in Arabidopsis Seedlings to Enhance Inhibition of Root Cell Elongation[W] , 2007, The Plant Cell Online.

[47]  Stuart A. Casson,et al.  MERISTEM-DEFECTIVE, an RS domain protein, is required for the correct meristem patterning and function in Arabidopsis. , 2009, The Plant journal : for cell and molecular biology.