Stochasticity in plant cellular growth and patterning

Frontiers in Plant Science

Volumn 5, Issue SEP, 2014, Pages

  Meyer, Heather M ^a   Roeder, Adrienne H K ^a  

^a School of Integrative Plant Sciences   (United States)

Author keywords

Arabidopsis; Cell division; Development; Robustness; Variability

Indexed keywords

EID: 84908192701     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00420     Document Type: Review

References (79)

1. Allard, J. F., Wasteneys, G. O., and Cytrynbaum, E. N. (2010). Mechanisms of self organization of cortical microtubules in plants revealed by computational simulations. Mol. Biol. Cell 21, 278-286. doi: 10.1091/mbc.E09-07-0579
2. Allen, T. D., and Potten, C. S. (1974). Fine-structural identification and organization of the epidermal proliferative unit. J. Cell Sci. 15, 291-319.
3. Bar-Even, A., Paulsson, J., Maheshri, N., Carmi, M., O'Shea, E., Pilpel, Y., et al. (2006). Noise in protein expression scales with natural protein abundance. Nat. Genet. 38, 636-643. doi: 10.1038/ng1807
4. Bender, A., and Pringle, J. R. (1989). Multicopy suppression of the cdc24 budding defect in yeast by CDC42 and three newly identified genes including the ras-related gene RSR1. Proc. Natl. Acad. Sci. U.S.A. 86, 9976-9980.
5. Benítez, M., Espinosa-Soto, C., Padilla-Longoria, P., and Alvarez-Buylla, E. R. (2008). Interlinked nonlinear subnetworks underlie the formation of robust cellular patterns in Arabidopsis epidermis: a dynamic spatial model. BMC Syst. Biol. 2:98. doi: 10.1186/1752-0509-2-98
6. Benítez, M., Espinosa-Soto, C., Padilla-Longoria, P., Díaz, J., and Alvarez-Buylla, E. R. (2007). Equivalent genetic regulatory networks in different contexts recover contrasting spatial cell patterns that resemble those in Arabidopsis root and leaf epidermis: a dynamic model. Int. J. Dev. Biol. 51, 139-155. doi: 10.1387/ijdb.062183mb
7. Besnard, F., Refahi, Y., Morin, V., Marteaux, B., Brunoud, G., Chambrier, P., et al. (2014). Cytokinin signalling inhibitory fields provide robustness to phyllotaxis. Nature 505, 417-421. doi: 10.1038/nature12791
8. Besson, S., and Dumais, J. (2011). Universal rule for the symmetric division of plant cells. Proc. Natl. Acad. Sci. U.S.A. 108, 6294-6299. doi: 10.1073/pnas.1011866108
9. Blake, W. J., Kærn, M., Cantor, C. R., and Collins, J. J. (2003). Noise in eukaryotic gene expression. Nature 422, 633-637. doi: 10.1038/nature01546
10. Bouyer, D., Geier, F., Kragler, F., Schnittger, A., Pesch, M., Wester, K., et al. (2008). Two-dimensional patterning by a trapping/depletion mechanism: the role of TTG1 and GL3 in Arabidopsis trichome formation. PLoS Biol. 6:e141. doi: 10.1371/journal.pbio.0060141
11. Clayton, E., Doupé, D. P., Klein, A. M., Winton, D. J., Simons, B. D., and Jones, P. H. (2007). A single type of progenitor cell maintains normal epidermis. Nature 446, 185-189. doi: 10.1038/nature05574
12. Dar, R. D., Hosmane, N. N., Arkin, M. R., Siliciano, R. F., and Weinberger, L. S. (2014). Screening for noise in gene expression identifies drug synergies. Science 344, 1392-1396. doi: 10.1126/science.1250220
13. del Álamo, D., Rouault, H., and Schweisguth, F. (2011). Mechanism and significance of cis-inhibition in Notch signalling. Curr. Biol. 21, R40-R47. doi: 10.1016/j.cub.2010.10.034
14. Dong, J., MacAlister, C. A., and Bergmann, D. C. (2009). BASL controls asymmetric cell division in Arabidopsis. Cell137, 1320-1330. doi: 10.1016/j.cell.2009.04.018
15. Doupé, D. P., Klein, A. M., Simons, B. D., and Jones, P. H. (2010). The ordered architecture of murine ear epidermis is maintained by progenitor cells with random fate. Dev. Cell 18, 317-323. doi: 10.1016/j.devcel.2009.12.016
16. Dupuy, L., MacKenzie, J., and Haseloff, J. (2010). Coordination of plant cell division and expansion in a simple morphogenetic system. Proc. Natl. Acad. Sci. U.S.A. 107, 2711-2716. doi: 10.1073/pnas.0906322107
17. Dupuy, L., MacKenzie, J., Rudge, T., and Haseloff, J. (2008). A system for modelling cell-cell interactions during plant morphogenesis. Ann. Bot. 101, 1255-1265. doi: 10.1093/aob/mcm235
18. Elowitz, M. B., Levine, A. J., Siggia, E. D., and Swain, P. S. (2002). Stochastic gene expression in a single cell. Science297, 1183-1186. doi: 10.1126/science.1070919
19. Elsner, J., Michalski, M., and Kwiatkowska, D. (2012). Spatiotemporal variation of leaf epidermal cell growth: a quantitative analysis of Arabidopsis thaliana wild-type and triple cyclinD3 mutant plants. Ann. Bot. 109, 897-910. doi: 10.1093/aob/mcs005
20. Eren, E. C., Dixit, R., and Gautam, N. (2010). A three-dimensional computer simulation model reveals the mechanisms for self-organization of pant cortical microtubules into oblique arrays. Mol. Biol. Cell 21, 2674-2684. doi: 10.1091/mbc.E10-02-0136
21. Fillmore, C. M., and Kuperwasser, C. (2008). Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res. 10, R25. doi: 10.1186/bcr1982
22. Góra, P. F. (2006). "The theory of Brownian motion: a hundred years' anniversary," in The 19th Marian Smoluchowski Symposium on Statistical Physics (Kraków), 52-57.
23. Goryachev, A. B., and Pokhilko, A. V. (2008). Dynamics of Cdc42 network embodies a Turing-type mechanism of yeast cell polarity. FEBS Lett. 582, 1437-1443. doi: 10.1016/j.febslet.2008.03.029
24. Gupta, P. B., Fillmore, C. M., Jiang, G., Shapira, S. D., Tao, K., Kuperwasser, C., et al. (2011). Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 146, 633-644. doi: 10.1016/j.cell.2011.07.026
25. Hamant, O., Heisler, M. G., Jönsson, H., Krupinski, P., Uyttewaal, M., Bokov, P., et al. (2008). Developmental patterning by mechanical signals in Arabidopsis. Science 322, 1650-1655. doi: 10.1126/science.1165594
26. Holy, T. E., and Leibler, S. (1994). Dynamic instability of microtubules as an efficient way to search in space. Proc. Natl. Acad. Sci. U.S.A. 91, 5682-5685
27. Howell, A. S., Jin, M., Wu, C.-F., Zyla, T. R., Elston, T. C., and Lew, D. J. (2012). Negative feedback enhances robustness in the yeast polarity establishment circuit. Cell 149, 322-333. doi: 10.1016/j.cell.2012.03.012
28. Howell, A. S., Savage, N. S., Johnson, S. A., Bose, I., Wagner, A. W., Zyla, T. R., et al. (2009). Singularity in polarization: rewiring yeast cells to make two buds. Cell 139, 731-743. doi: 10.1016/j.cell.2009.10.024
29. Hülskamp, M. (2004). Plant trichomes: a model for cell differentiation. Nat. Rev. Mol. Cell Biol. 5, 471-480. doi: 10.1038/nrm1404
30. Hülskamp, M., and Schnittger, A. (1998). Spatial regulation of trichome formation in Arabidopsis thaliana. Semin. Cell Dev. Biol. 9, 213-220. doi: 10.1006/scdb.1997.0209
31. Irazoqui, J. E., Gladfelter, A. S., and Lew, D. J. (2003). Scaffold-mediated symmetry breaking by Cdc42p. Nat. Cell Biol. 5, 1062-1070. doi: 10.1038/ncb1068
32. Jeune, B., and Barabé, D. (2006). A stochastic approach to phyllotactic patterns analysis. J. Theor. Biol. 238, 52-59. doi: 10.1016/j.jtbi.2005.05.036
33. Johnston, R. J. Jr., and Desplan, C. (2010). Stochastic mechanisms of cell fate specification that yield random or robust outcomes. Annu. Rev. Cell Dev. Biol. 26, 689-719. doi: 10.1146/annurev-cellbio-100109-104113
34. 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. U.S.A. 103, 1633-1638. doi: 10.1073/pnas.0509839103
35. Kierzkowski, D., Nakayama, N., Routier-Kierzkowska, A.-L., Weber, A., Bayer, E., Schorderet, M., et al. (2012). Elastic domains regulate growth and organogenesis in the plant shoot apical meristem. Science 335, 1096-1099. doi: 10.1126/science.1213100
36. Kozubowski, L., Saito, K., Johnson, J. M., Howell, A. S., Zyla, T. R., and Lew, D. J. (2008). Symmetry-breaking polarization driven by a Cdc42p GEF-PAK complex. Curr. Biol. 18, 1719-1726. doi: 10.1016/j.cub.2008.09.060
37. Kubu, C. J., Orimoto, K., Morrison, S. J., Weinmaster, G., Anderson, D. J., and Verdi, J. M. (2002). Developmental changes in Notch1 and numb expression mediated by local cell-cell interactions underlie progressively increasing delta sensitivity in neural crest stem cells. Dev. Biol. 244, 199-214. doi: 10.1006/dbio.2002.0568
38. Lee, M. M., and Schiefelbein, J. (2002). Cell pattern in the Arabidopsis root epidermis determined by lateral inhibition with feedback. Plant Cell 14, 611-618. doi: 10.3410/f.1005550.70106
39. Malliavin, P., and Thalmaier, A. (2006). Stochastic Calculus of Variations in Mathematical Finance. Berlin; Heidelberg; New York, NY: Springer-Verlag.
40. Mannello, F. (2013). Understanding breast cancer stem cell heterogeneity: time to move on to a new research paradigm. BMC Med. 11:169. doi: 10.1186/1741-7015-11-169
41. Marinari, E., Mehonic, A., Curran, S., Gale, J., Duke, T., and Baum, B. (2012). Live-cell delamination counterbalances epithelial growth to limit tissue overcrowding. Nature 484, 542-545. doi: 10.1038/nature10984
42. Martin, A. C., Kaschube, M., and Wieschaus, E. F. (2009). Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457, 495-499. doi: 10.1038/nature07522
43. Meinhardt, H., and Gierer, A. (1974). Application of a theory of biological pattern formation based on lateral inhibition. J. Cell Sci. 15, 321-346.
44. Melaragno, J. E., Mehrotra, B., and Coleman, A. W. (1993). Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5, 1661-1668. doi: 10.1105/tpc.5.11.1661
45. Mirabet, V., Besnard, F., Vernoux, T., and Boudaoud, A. (2012). Noise and robustness in phyllotaxis. PLoS Comput. Biol. 8:e1002389. doi: 10.1371/journal.pcbi.1002389.
46. Morelli, L. G., Uriu, K., Ares, S., and Oates, A. C. (2012). Computational approaches to developmental patterning. Science 336, 187-191. doi: 10.1126/science.1215478
47. Morrison, S. J., Perez, S. E., Qiao, Z., Verdi, J. M., Hicks, C., Weinmaster, G., et al. (2000). Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 101, 499-510. doi: 10.1016/S0092-8674(00)80860-0
48. Murray, J. A. H., Jones, A., Godin, C., and Traas, J. (2012). Systems analysis of shoot apical meristem growth and development: integrating hormonal and mechanical signaling. Plant Cell 24, 3907-3919. doi: 10.1105/tpc.112.102194
49. Newman, J. R. S., Ghaemmaghami, S., Ihmels, J., Breslow, D. K., Noble, M., DeRisi, J. L., et al. (2006). Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441, 840-846. doi: 10.1038/nature04785
50. Ozbudak, E. M., Thattai, M., Kurtser, I., Grossman, A. D., and van Oudenaarden, A. (2002). Regulation of noise in the expression of a single gene. Nat. Genet. 31, 69-73. doi: 10.1038/ng869
51. Paredez, A. R., Somerville, C. R., and Ehrhardt, D. W. (2006). Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491-1495. doi: 10.1126/science.1126551
52. Pedraza, J. M., and van Oudenaarden, A. (2005). Noise propagation in gene networks. Science 307, 1965-1969. doi: 10.1126/science.1109090
53. Potten, C. S. (1981). Cell replacement in epidermis (keratopoiesis) via discrete units of proliferation. Int. Rev. Cytol. 69, 271-318.
54. Pouille, P.-A., Ahmadi, P., Brunet, A.-C., and Farge, E. (2009). Mechanical signals trigger Myosin II redistribution and mesoderm invagination in Drosophila embryos. Sci. Signal. 2, ra16. doi: 10.1126/scisignal.2000098
55. Raj, A., Rifkin, S. A., Andersen, E., and van Oudenaarden, A. (2010). Variability in gene expression underlies incomplete penetrance. Nature 463, 913-918. doi: 10.1038/nature08781
56. Rao, C. V., Wolf, D. M., and Arkin, A. P. (2002). Control, exploitation and tolerance of intracellular noise. Nature420, 231-237. doi: 10.1038/nature01258
57. Raser, J. M. (2005). Noise in gene expression: origins, consequences, and control. Science 309, 2010-2013. doi: 10.1126/science.1105891
58. Raser, J. M., and O'Shea, E. K. (2004). Control of stochasticity in eukaryotic gene expression. Science 304, 1811-1814. doi: 10.1126/science.1098641
59. Robinson, S., Barbier de Reuille, P., Chan, J., Bergmann, D., Prusinkiewicz, P., and Coen, E. (2011). Generation of spatial patterns through cell polarity switching. Science 333, 1436-1440. doi: 10.1126/science.1202185
60. Roeder, A. H. K., Chickarmane, V., Cunha, A., Obara, B., Manjunath, B. S., and Meyerowitz, E. M. (2010). Variability in the control of cell division underlies sepal epidermal patterning in Arabidopsis thaliana. PLoS Biol. 8:e1000367. doi: 10.1371/journal.pbio.1000367
61. Roeder, A. H. K., Cunha, A., Ohno, C. K., and Meyerowitz, E. M. (2012). Cell cycle regulates cell type in the Arabidopsis sepal. Development 139, 4416-4427. doi: 10.1242/dev.082925
62. Rosenfeld, N. (2005). Gene regulation at the single-cell level. Science 307, 1962-1965. doi: 10.1126/science.1106914
63. Sampathkumar, A., Krupinski, P., Wightman, R., Milani, P., Berquand, A., Boudaoud, A., et al. (2014). Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. Elife 3, e01967. doi: 10.7554/eLife.01967
64. Schellmann, S., Schnittger, A., Kirik, V., Wada, T., Okada, K., Beermann, A., et al. (2002). TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J. 21, 5036-5046. doi: 10.1093/emboj/cdf524
65. Scheres, B. (2002). Plant patterning: TRY to inhibit your neighbors. Curr. Biol. 12, R804-R806. doi: 10.1016/S0960-9822(02)01313-1
66. Schiefelbein, J. (2003). Cell-fate specification in the epidermis: a common patterning mechanism in the root and shoot. Curr. Opin. Plant Biol. 6, 74-78. doi: 10.1016/S136952660200002X
67. Schiessl, K., Kausika, S., Southam, P., Bush, M., and Sablowski, R. (2012). JAGGED controls growth anisotropy and coordination between cell size and cell cycle during plant organogenesis. Curr. Biol. 22, 1739-1746. doi: 10.1016/j.cub.2012.07.020
68. Schiessl, K., Muiño, J. M., and Sablowski, R. (2014). Arabidopsis JAGGED links floral organ patterning to tissue growth by repressing Kip-related cell cycle inhibitors. Proc. Natl. Acad. Sci. U.S.A. 111, 2830-2835. doi: 10.1073/pnas.1320457111
69. 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. U.S.A. 103, 1301-1306. doi: 10.1073/pnas.0510457103
70. Solanas, G., and Benitah, S. A. (2013). Regenerating the skin: a task for the heterogeneous stem cell pool and surrounding niche. Nat. Rev. Mol. Cell Biol. 14, 737-748. doi: 10.1038/nrm3675
71. Sprinzak, D., Lakhanpal, A., Lebon, L., Santat, L. A., Fontes, M. E., Anderson, G. A., et al. (2010). Cis-interactions between Notch and Delta generate mutually exclusive signalling states. Nature 465, 86-90. doi: 10.1038/nature08959
72. 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. doi: 10.1371/journal.pcbi.1000207
73. Süel, G. M., Garcia-Ojalvo, J., Liberman, L. M., and Elowitz, M. B. (2006). An excitable gene regulatory circuit induces transient cellular differentiation. Nature 440, 545-550. doi: 10.1038/nature04588
74. Toenjes, K. A., Simpson, D., and Johnson, D. I. (2004). Separate membrane targeting and anchoring domains function in the localization of the S. cerevisiae Cdc24p guanine nucleotide exchange factor. Curr. Genet. 45, 257-264. doi: 10.1007/s00294-004-0485-9
75. Uyttewaal, M., Burian, A., Alim, K., Landrein, B., Borowska-Wykrêt, D., Dedieu, A., et al. (2012). Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis. Cell 149, 439-451. doi: 10.1016/j.cell.2012.02.048
76. Wakamatsu, Y., Maynard, T. M., and Weston, J. A. (2000). Fate determination of neural crest cells by NOTCH-mediated lateral inhibition and asymmetrical cell division during gangliogenesis. Development 127, 2811-2821.
77. Wang, W., Quan, Y., Fu, Q., Liu, Y., Liang, Y., Wu, J., et al. (2014). Dynamics between cancer cell subpopulations reveals a model coordinating with both hierarchical and stochastic concepts. PLoS ONE 9:e84654. doi: 10.1371/journal.pone.0084654
78. Wedlich-Soldner, R., Altschuler, S., Wu, L., and Li, R. (2003). Spontaneous cell polarization through actomyosin-based delivery of the Cdc42 GTPase. Science 299, 1231-1235. doi: 10.1126/science.1080944
79. Yoshida, S., Barbier de Reuille, P., Lane, B., Bassel, G. W., Prusinkiewicz, P., Smith, R. S., et al. (2014). Genetic control of plant development by overriding a geometric division rule. Dev. Cell 29, 75-87. doi: 10.1016/j.devcel.2014.02.002