An intracellular partitioning-based framework for tissue cell polarity in plants and animals

Development (Cambridge)

Volumn 140, Issue 10, 2013, Pages 2061-2074

  Abley, Katie ^a   Barbier de Reuille, Pierre ^a,b,c   Strutt, David ^d   Bangham, Andrew ^b   Prusinkiewicz, Przemyslaw ^c   Marée, Athanasius F M ^a   Grieneisen, Verônica A ^a   Coen, Enrico ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^c UNIVERSITY OF CALGARY   (Canada)

^d UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Auxin; Organiser; Pcp; PIN; Polarity

Indexed keywords

ARTICLE; CELL DIVISION; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL POLARITY; CELL WALL; COMPUTER SIMULATION; DROSOPHILA; NONHUMAN; PLANT; PLANT CELL; PLANT TISSUE; PRIORITY JOURNAL; THICKNESS;

ANIMALS; BIOLOGICAL TRANSPORT; CELL COMMUNICATION; CELL POLARITY; CYTOSOL; DROSOPHILA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INDOLEACETIC ACIDS; MORPHOGENESIS; PLANT PHYSIOLOGICAL PHENOMENA; PLANTS; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 84876990939     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.062984     Document Type: Article

References (64)

1. Adler, P. N., Krasnow, R. E. and Liu, J. (1997). Tissue polarity points from cells that have higher Frizzled levels towards cells that have lower Frizzled levels. Curr. Biol. 7, 940-949.
2. Aida, M. and Tasaka, M. (2006). Morphogenesis and patterning at the organ boundaries in the higher plant shoot apex. Plant Mol. Biol. 60, 915-928.
3. Aida, M., Beis, D., Heidstra, R., Willemsen, V., Blilou, I., Galinha, C., Nussaume, L., Noh, Y. S., Amasino, R. and Scheres, B. (2004). The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119, 109-120.
4. Aigouy, B., Farhadifar, R., Staple, D. B., Sagner, A., Röper, J. C., Jülicher, F. and Eaton, S. (2010). Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila. Cell 142, 773-786.
5. Ambegaonkar, A. A., Pan, G., Mani, M., Feng, Y. and Irvine, K. D. (2012). Propagation of Dachsous-Fat planar cell polarity. Curr. Biol. 22, 1302-1308.
6. Amonlirdviman, K., Khare, N. A., Tree, D. R., Chen, W. S., Axelrod, J. D. and Tomlin, C. J. (2005). Mathematical modeling of planar cell polarity to understand domineering nonautonomy. Science 307, 423-426.
7. Bayer, E. M., Smith, R. S., Mandel, T., Nakayama, N., Sauer, M., Prusinkiewicz, P. and Kuhlemeier, C. (2009). Integration of transport-based models for phyllotaxis and midvein formation. Genes Dev. 23, 373-384.
8. Benková, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertová, D., Jürgens, G. and Friml, J. (2003). Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591-602.
9. Blilou, I., Xu, J., Wildwater, M., Willemsen, V., Paponov, I., Friml, J., Heidstra, R., Aida, M., Palme, K. and Scheres, B. (2005). The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39-44.
10. Boutté, Y., Crosnier, M. T., Carraro, N., Traas, J. and Satiat-Jeunemaitre, B. (2006). The plasma membrane recycling pathway and cell polarity in plants: studies on PIN proteins. J. Cell Sci. 119, 1255-1265.
11. Brittle, A. L., Repiso, A., Casal, J., Lawrence, P. A. and Strutt, D. (2010). Fourjointed modulates growth and planar polarity by reducing the affinity of dachsous for fat. Curr. Biol. 20, 803-810.
12. Brittle, A., Thomas, C. and Strutt, D. (2012). Planar polarity specification through asymmetric subcellular localization of Fat and Dachsous. Curr. Biol. 22, 907-914.
13. Burak, Y. and Shraiman, B. I. (2009). Order and stochastic dynamics in Drosophila planar cell polarity. PLoS Comput. Biol. 5, e1000628.
14. Casal, J., Lawrence, P. A. and Struhl, G. (2006). Two separate molecular systems, Dachsous/Fat and Starry night/Frizzled, act independently to confer planar cell polarity. Development 133, 4561-4572.
15. Classen, A. K., Anderson, K. I., Marois, E. and Eaton, S. (2005). Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway. Dev. Cell 9, 805-817.
16. Fu, Y., Gu, Y., Zheng, Z., Wasteneys, G. and Yang, Z. (2005). Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 120, 687-700.
17. Goodrich, L. V. and Strutt, D. (2011). Principles of planar polarity in animal development. Development 138, 1877-1892.
18. Greb, T., Clarenz, O., Schafer, E., Muller, D., Herrero, R., Schmitz, G. and Theres, K. (2003). Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes Dev. 17, 1175-1187.
19. Green, A. A., Kennaway, J. R., Hanna, A. I., Bangham, J. A. and Coen, E. (2010). Genetic control of organ shape and tissue polarity. PLoS Biol. 8, e1000537.
20. Heisler, M. G., Ohno, C., Das, P., Sieber, P., Reddy, G. V., Long, J. A. and Meyerowitz, E. M. (2005). Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol. 15, 1899-1911.
21. Heisler, M. G., Hamant, O., Krupinski, P., Uyttewaal, M., Ohno, C., Jönsson, H., Traas, J. and Meyerowitz, E. M. (2010). Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biol. 8, e1000516.
22. Jilkine, A., Marée, A. F. and Edelstein-Keshet, L. (2007). Mathematical model for spatial segregation of the Rho-family GTPases based on inhibitory crosstalk. Bull. Math. Biol. 69, 1943-1978.
23. Johnson, J. M., Jin, M. and Lew, D. J. (2011). Symmetry breaking and the establishment of cell polarity in budding yeast. Curr. Opin. Genet. Dev. 21, 740-746.
24. Jönsson, H., Heisler, M. G., Shapiro, B. E., Meyerowitz, E. M. and Mjolsness, E. (2006). An auxin-driven polarized transport model for phyllotaxis. Proc. Natl. Acad. Sci. USA 103, 1633-1638.
25. Kramer, E. M., Frazer, N. L. and Baskin, T. I. (2007). Measurement of diffusion within the cell wall in living roots of Arabidopsis thaliana. J. Exp. Bot. 58, 3005-3015.
26. Křeček, P., Skůpa, P., Libus, J., Naramoto, S., Tejos, R., Friml, J. and Zažímalová, E. (2009). The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol. 10, 249.
27. Lawrence, P. A., Casal, J. and Struhl, G. (2004). Cell interactions and planar polarity in the abdominal epidermis of Drosophila. Development 131, 4651-4664.
28. Lawrence, P. A., Struhl, G. and Casal, J. (2007). Planar cell polarity: one or two pathways? Nat. Rev. Genet. 8, 555-563.
29. Le Garrec, J. F., Lopez, P. and Kerszberg, M. (2006). Establishment and maintenance of planar epithelial cell polarity by asymmetric cadherin bridges: a computer model. Dev. Dyn. 235, 235-246.
30. Ludwig-Müller, J. (2011). Auxin conjugates: their role for plant development and in the evolution of land plants. J. Exp. Bot. 62, 1757-1773.
31. Ma, D., Amonlirdviman, K., Raffard, R. L., Abate, A., Tomlin, C. J. and Axelrod, J. D. (2008). Cell packing influences planar cell polarity signaling. Proc. Natl. Acad. Sci. USA 105, 18800-18805.
32. Majer, C. and Hochholdinger, F. (2011). Defining the boundaries: structure and function of LOB domain proteins. Trends Plant Sci. 16, 47-52.
33. Marée, A. F., Jilkine, A., Dawes, A., Grieneisen, V. A. and Edelstein-Keshet, L. (2006). Polarization and movement of keratocytes: a multiscale modelling approach. Bull. Math. Biol. 68, 1169-1211.
34. Marée, A. F., Grieneisen, V. A. and Edelstein-Keshet, L. (2012). How cells integrate complex stimuli: the effect of feedback from phosphoinositides and cell shape on cell polarization and motility. PLoS Comput. Biol. 8, e1002402.
35. Meinhardt, H. (2007). Computational modelling of epithelial patterning. Curr. Opin. Genet. Dev. 17, 272-280.
36. Merks, R. M. H., Van de Peer, Y., Inze, D. and Beemster, G. T. S. (2007). Canalization without flux sensors: a traveling-wave hypothesis. Trends Plant Sci. 12, 384-390.
37. Mitchison, G. (1980). A model for vein formation in higher plants. Proc. R. Soc. B 207, 79-109.
38. Mogilner, A., Allard, J. and Wollman, R. (2012). Cell polarity: quantitative modeling as a tool in cell biology. Science 336, 175-179.
39. Oda, Y. and Fukuda, H. (2012). Initiation of cell wall pattern by a Rho- and microtubule-driven symmetry breaking. Science 337, 1333-1336.
40. Postma, M. and Van Haastert, P. J. (2001). A diffusion-translocation model for gradient sensing by chemotactic cells. Biophys. J. 81, 1314-1323.
41. Postma, M., Bosgraaf, L., Loovers, H. M., and Van Haastert, P. J. (2004). Chemotaxis: signalling modules join hands at front and tail. EMBO Rep. 5, 35-40.
42. Rolland-Lagan, A. G. and Prusinkiewicz, P. (2005). Reviewing models of auxin canalization in the context of leaf vein pattern formation in Arabidopsis. Plant J. 44, 854-865.
43. Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J., Benfey, P., Leyser, O., Bechtold, N., Weisbeek, P. et al. (1999). An auxindependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463-472.
44. Sachs, T. (1981). The controls of the patterned differentiation of vascular tissues. Adv. Bot. Res. 9, 151-262.
45. Sahlin, P., Söderberg, B. and Jönsson, H. (2009). Regulated transport as a mechanism for pattern generation: capabilities for phyllotaxis and beyond. J. Theor. Biol. 258, 60-70.
46. Sauer, M. and Kleine-Vehn, J. (2011). AUXIN BINDING PROTEIN1: the outsider. Plant Cell 23, 2033-2043.
47. Simon, M. A. (2004). Planar cell polarity in the Drosophila eye is directed by graded Four-jointed and Dachsous expression. Development 131, 6175-6184.
48. Simon, M. A., Xu, A., Ishikawa, H. O. and Irvine, K. D. (2010). Modulation of fat:dachsous binding by the cadherin domain kinase four-jointed. Curr. Biol. 20, 811-817.
49. Smith, C., Prusinkiewicz, P. and Samavati, F. (2003). Local specification of surface subdivision algorithms (Applications of Graph Transformations with Industrial Relevance (AGTIVE 2003)). Lecture Notes Comp. Sci. 3062, 313-327.
50. Smith, R. S., Guyomarc'h, S., Mandel, T., Reinhardt, D., Kuhlemeier, C. and Prusinkiewicz, P. (2006). A plausible model of phyllotaxis. Proc. Natl. Acad. Sci. USA 103, 1301-1306.
51. Spemann, H. and Mangold, H. (1924). Uber Induktion von Embryonalanlagen durch Implantation artfremder Organisatoren. Arch. Mikr. Anat. und Entw. Mech. 100, 599-638.
52. Stoma, S., Lucas, M., Chopard, J., Schaedel, M., Traas, J. and Godin, C. (2008). Flux-based transport enhancement as a plausible unifying mechanism for auxin transport in meristem development. PLoS Comput. Biol. 4, e1000207.
53. Strutt, D. and Strutt, H. (2007). Differential activities of the core planar polarity proteins during Drosophila wing patterning. Dev. Biol. 302, 181-194.
54. Strutt, H. and Strutt, D. (2009). Asymmetric localisation of planar polarity proteins: Mechanisms and consequences. Semin. Cell Dev. Biol. 20, 957-963.
55. Usui, T., Shima, Y., Shimada, Y., Hirano, S., Burgess, R. W., Schwarz, T. L., Takeichi, M. and Uemura, T. (1999). Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98, 585-595.
56. Venema, D. R., Zeev-Ben-Mordehai, T. and Auld, V. J. (2004). Transient apical polarization of Gliotactin and Coracle is required for parallel alignment of wing hairs in Drosophila. Dev. Biol. 275, 301-314.
57. Verkhovsky, A. B., Svitkina, T. M. and Borisy, G. G. (1999). Self-polarization and directional motility of cytoplasm. Curr. Biol. 9, 11-20.
58. Wabnik, K., Kleine-Vehn, J., Balla, J., Sauer, M., Naramoto, S., Reinöhl, V., Merks, R. M., Govaerts, W. and Friml, J. (2010). Emergence of tissue polarization from synergy of intracellular and extracellular auxin signaling. Mol. Syst. Biol. 6, 447.
59. Wedlich-Soldner, R. and Li, R. (2003). Spontaneous cell polarization: undermining determinism. Nat. Cell Biol. 5, 267-270.
60. Wong, L. L. and Adler, P. N. (1993). Tissue polarity genes of Drosophila regulate the subcellular location for prehair initiation in pupal wing cells. J. Cell Biol. 123, 209-221.
61. Xu, T., Wen, M., Nagawa, S., Fu, Y., Chen, J. G., Wu, M. J., Perrot- Rechenmann, C., Friml, J., Jones, A. M. and Yang, Z. (2010). Cell surfaceand rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143, 99-110.
62. Yang, Z. (2008). Cell polarity signaling in Arabidopsis. Annu. Rev. Cell Dev. Biol. 24, 551-575.
63. Yang, Y., Hammes, U. Z., Taylor, C. G., Schachtman, D. P. and Nielsen, E. (2006). High-affinity auxin transport by the AUX1 influx carrier protein. Curr. Biol. 16, 1123-1127.
64. Zhao, Y. (2010). Auxin biosynthesis and its role in plant development. Annu. Rev. Plant Biol. 61, 49-64.