1932

Abstract

Development is remarkably reproducible, producing organs with the same size, shape, and function repeatedly from individual to individual. For example, every flower on the stalk has the same snapping dragon mouth. This reproducibility has allowed taxonomists to classify plants and animals according to their morphology. Yet these reproducible organs are composed of highly variable cells. For example, neighboring cells grow at different rates in leaves, sepals, and shoot apical meristems. This cellular variability occurs in normal, wild-type organisms, indicating that cellular heterogeneity (or diversity in a characteristic such as growth rate) is either actively maintained or, at a minimum, not entirely suppressed. In fact, cellular heterogeneity can contribute to producing invariant organs. Here, we focus on how plant organs are reproducibly created during development from these highly variable cells.

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2018-04-29
2024-05-01
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Literature Cited

  1. Abley K, Barbier de Reuille P, Strutt D, Bangham A, Prusinkiewicz P. 1.  et al. 2013. An intracellular partitioning-based framework for tissue cell polarity in plants and animals. Development 140:102061–74 [Google Scholar]
  2. Abley K, Locke JCW, Leyser HMO. 2.  2016. Developmental mechanisms underlying variable, invariant and plastic phenotypes. Ann. Bot. 117:5733–48 [Google Scholar]
  3. Abley K, Sauret-Güeto S, Marée AF, Coen ES. 3.  2016. Formation of polarity convergences underlying shoot outgrowths. eLife 5:e18165 [Google Scholar]
  4. Adamski NM, Anastasiou E, Eriksson S, O'Neill CM, Lenhard M. 4.  2009. Local maternal control of seed size by KLUH/CYP78A5-dependent growth signaling. PNAS 106:4720115–20 [Google Scholar]
  5. Ali O, Traas J. 5.  2016. Force-driven polymerization and turgor-induced wall expansion. Trends Plant Sci 21:5398–409 [Google Scholar]
  6. Allard JF, Wasteneys GO, Cytrynbaum EN. 6.  2010. Mechanisms of self-organization of cortical microtubules in plants revealed by computational simulations. Mol. Biol. Cell 21:2278–86 [Google Scholar]
  7. Amir A.7.  2017. Is cell size a spandrel?. eLife 6:e22186 [Google Scholar]
  8. Anastasiou E, Kenz S, Gerstung M, MacLean D, Timmer J. 8.  et al. 2007. Control of plant organ size by KLUH/CYP78A5-dependent intercellular signaling. Dev. Cell 13:6843–56 [Google Scholar]
  9. Andriankaja M, Dhondt S, De Bodt S Vanhaeren H, Coppens F. 9.  et al. 2012. Exit from proliferation during leaf development in Arabidopsis thaliana: a not-so-gradual process. Dev. Cell 22:164–78 [Google Scholar]
  10. Avery GS.10.  1933. Structure and development of the tobacco leaf. Am. J. Bot. 20:9565 [Google Scholar]
  11. Balduzzi M, Binder BM, Bucksch A, Chang C, Hong L. 11.  et al. 2017. Reshaping plant biology: qualitative and quantitative descriptors for plant morphology. Front. Plant Sci. 8:117 [Google Scholar]
  12. Barbier de Reuille P, Routier-Kierzkowska AL, Kierzkowski D, Bassel GW, Schüpbach T. 12.  et al. 2015. MorphoGraphX: a platform for quantifying morphogenesis in 4D. eLife 4:e05864 [Google Scholar]
  13. Bassel GW, Stamm P, Mosca G, Barbier de Reuille P, Gibbs DJ. 13.  et al. 2014. Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo. PNAS 111:238685–90 [Google Scholar]
  14. Beauzamy L, Derr J, Boudaoud A. 14.  2015. Quantifying hydrostatic pressure in plant cells by using indentation with an atomic force microscope. Biophys. J. 108:102448–56 [Google Scholar]
  15. Beauzamy L, Fourquin C, Dubrulle N, Boursiac Y, Boudaoud A, Ingram G. 15.  2016. Endosperm turgor pressure decreases during early Arabidopsis seed development. Development 143:183295–99 [Google Scholar]
  16. Beauzamy L, Louveaux M, Hamant O, Boudaoud A. 16.  2015. Mechanically, the shoot apical meristem of Arabidopsis behaves like a shell inflated by a pressure of about 1 MPa. Front. Plant Sci. 6:1038 [Google Scholar]
  17. Beauzamy L, Nakayama N, Boudaoud A. 17.  2014. Flowers under pressure: ins and outs of turgor regulation in development. Ann. Bot. 114:71517–33 [Google Scholar]
  18. Besson S, Dumais J. 18.  2011. Universal rule for the symmetric division of plant cells. PNAS 108:156294–99 [Google Scholar]
  19. Bezanilla M, Perroud PF. 19.  2009. Tip growth in the moss Physcomitrella patens. Annu. Plant Rev 36:143–66 [Google Scholar]
  20. Bhalerao RP, Bennett MJ. 20.  2003. The case for morphogens in plants. Nat. Cell Biol. 5:11939–43 [Google Scholar]
  21. Biot E, Cortizo M, Burguet J, Kiss A, Oughou M. 21.  et al. 2016. Multiscale quantification of morphodynamics: MorphoLeaf software for 2D shape analysis. Development 143:3417–28 [Google Scholar]
  22. Bonett DG.22.  2006. Confidence interval for a coefficient of quartile variation. Comput. Stat. Data Anal. 50:112953–57 [Google Scholar]
  23. Boonstra J, Post JA. 23.  2004. Molecular events associated with reactive oxygen species and cell cycle progression in mammalian cells. Gene 337:1–13 [Google Scholar]
  24. Bosch M, Hepler PK. 24.  2005. Pectin methylesterases and pectin dynamics in pollen tubes. Plant Cell 17:123219–26 [Google Scholar]
  25. Boudaoud A, Burian A, Borowska-Wykręt D, Uyttewaal M, Wrzalik R. 25.  et al. 2014. FibrilTool, an ImageJ plug-in to quantify fibrillar structures in raw microscopy images. Nat. Protoc. 9:2457–63 [Google Scholar]
  26. Boukhibar LM, Barkoulas M. 26.  2016. The developmental genetics of biological robustness. Ann. Bot. 117:5699–707 [Google Scholar]
  27. Braam J.27.  2005. In touch: plant responses to mechanical stimuli. New Phytol 165:2373–89 [Google Scholar]
  28. Braidwood L, Breuer C, Sugimoto K. 28.  2013. My body is a cage: mechanisms and modulation of plant cell growth. New Phytol 201:2388–402 [Google Scholar]
  29. Bringmann M, Li E, Sampathkumar A, Kocabek T, Hauser M-T, Persson S. 29.  2012. POM-POM2/CELLULOSE SYNTHASE INTERACTING1 is essential for the functional association of cellulose synthase and microtubules in Arabidopsis. Plant Cell 24:1163–77 [Google Scholar]
  30. Burian A, Ludynia M, Uyttewaal M, Traas J, Boudaoud A. 30.  et al. 2013. A correlative microscopy approach relates microtubule behaviour, local organ geometry, and cell growth at the Arabidopsis shoot apical meristem. J. Exp. Bot. 64:185753–67 [Google Scholar]
  31. Chitwood DH, Nogueira FTS, Howell MD, Montgomery TA, Carrington JC, Timmermans MCP. 31.  2009. Pattern formation via small RNA mobility. Genes Dev 23:5549–54 [Google Scholar]
  32. Coen ES, Rolland-Lagan A-G, Matthews M, Bangham JA, Prusinkiewicz P. 32.  2004. The genetics of geometry. PNAS 101:144728–35 [Google Scholar]
  33. Corson F, Hamant O, Bohn S, Traas J, Boudaoud A. 33.  et al. 2009. Turning a plant tissue into a living cell froth through isotropic growth. PNAS 106:218453–58 [Google Scholar]
  34. Cosgrove DJ.34.  2016. Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes. J. Exp. Bot. 67:2463–76 [Google Scholar]
  35. Das Gupta M, Nath U. 35.  2015. Divergence in patterns of leaf growth polarity is associated with the expression divergence of miR396. Plant Cell 27:2785–99Shows the miR396-GRF module correlates with the proximodistal patterning of leaf growth whether basipetal, acropetal, or bipolar. [Google Scholar]
  36. Dello Ioio R, Nakamura K, Moubayidin L, Perilli S, Taniguchi M. 36.  et al. 2008. A genetic framework for the control of cell division and differentiation in the root meristem. Science 322:59061380–84 [Google Scholar]
  37. de Souza A, Hull PA, Gille S, Pauly M. 37.  2014. Identification and functional characterization of the distinct plant pectin esterases PAE8 and PAE9 and their deletion mutants. Planta 240:51123–38 [Google Scholar]
  38. De Veylder L, Larkin JC, Schnittger A. 38.  2011. Molecular control and function of endoreplication in development and physiology. Trends Plant Sci 16:11624–34 [Google Scholar]
  39. Deinum EE, Tindemans SH, Lindeboom JJ, Mulder BM. 39.  2017. How selective severing by katanin promotes order in the plant cortical microtubule array. PNAS 114:276942–47 [Google Scholar]
  40. Di Talia S, Skotheim JM, Bean JM, Siggia ED, Cross FR. 40.  2007. The effects of molecular noise and size control on variability in the budding yeast cell cycle. Nature 448:7156947–51 [Google Scholar]
  41. Dixit R, Cyr R. 41.  2004. The cortical microtubule array: from dynamics to organization. Plant Cell 16:102546–52 [Google Scholar]
  42. Dumais J, Kwiatkowska D. 42.  2002. Analysis of surface growth in shoot apices. Plant J 31:2229–41 [Google Scholar]
  43. Dupuy L, Mackenzie J, Haseloff J. 43.  2010. Coordination of plant cell division and expansion in a simple morphogenetic system. PNAS 107:62711–16 [Google Scholar]
  44. Dyer JM, Savage NS, Jin M, Zyla TR, Elston TC, Lew DJ. 44.  2013. Tracking shallow chemical gradients by actin-driven wandering of the polarization site. Curr. Biol. 23:132–41 [Google Scholar]
  45. Dyson RJ, Vizcay-Barrena G, Band LR, Fernandes AN, French AP. 45.  et al. 2014. Mechanical modelling quantifies the functional importance of outer tissue layers during root elongation and bending. New Phytol 202:41212–22 [Google Scholar]
  46. Efron B.46.  1979. Bootstrap methods: another look at the jackknife. Ann. Stat. 7:1–26 [Google Scholar]
  47. Elsner J, Michalski M, Kwiatkowska D. 47.  2012. Spatiotemporal variation of leaf epidermal cell growth: a quantitative analysis of Arabidopsis thaliana wild-type and triple cyclinD3 mutant plants. Ann. Bot. 109:5897–910 [Google Scholar]
  48. Erdmann T, Howard M, ten Wolde PR. 48.  2009. Role of spatial averaging in the precision of gene expression patterns. Phys. Rev. Lett. 103:25258101 [Google Scholar]
  49. Eren EC, Gautam N, Dixit R. 49.  2012. Computer simulation and mathematical models of the noncentrosomal plant cortical microtubule cytoskeleton. Cytoskeleton 69:3144–54 [Google Scholar]
  50. Eriksson S, Stransfeld L, Adamski NM, Breuninger H, Lenhard M. 50.  2010. KLUH/CYP78A5-dependent growth signaling coordinates floral organ growth in Arabidopsis. Curr. Biol 20:6527–32 [Google Scholar]
  51. Errera L.51.  1886. Sur une condition fondamentale d'équilibre des cellules vivantes. [On a fundamental condition of equilibrium for living cells.]. C. R. Hebd. Seances Acad. Sci. 103:822–24 (in French) [Google Scholar]
  52. Forouzesh E, Goel A, Mackenzie SA, Turner JA. 52.  2013. In vivo extraction of Arabidopsis cell turgor pressure using nanoindentation in conjunction with finite element modeling. Plant J 73:3509–20 [Google Scholar]
  53. Franck AD, Powers AF, Gestaut DR, Gonen T, Davis TN, Asbury CL. 53.  2007. Tension applied through the Dam1 complex promotes microtubule elongation providing a direct mechanism for length control in mitosis. Nat. Cell Biol. 9:7832–37 [Google Scholar]
  54. Fry SC.54.  2004. Oxidative coupling of tyrosine and ferulic acid residues: intra- and extra-protoplasmic occurrence, predominance of trimers and larger products, and possible role in inter-polymeric cross-linking. Phytochem. Rev. 3:1–297–111 [Google Scholar]
  55. Gázquez A, Beemster GTS. 55.  2017. What determines organ size differences between species? A meta-analysis of the cellular basis. New Phytol 215:1299–308 [Google Scholar]
  56. Geitmann A.56.  2006. Experimental approaches used to quantify physical parameters at cellular and subcellular levels. Am. J. Bot. 93:101380 [Google Scholar]
  57. Glass M, Barkwill S, Unda F, Mansfield SD. 57.  2015. Endo-β-1,4-glucanases impact plant cell wall development by influencing cellulose crystallization. J. Integr. Plant Biol. 57:4396–410 [Google Scholar]
  58. Gonzalez N, Pauwels L, Baekelandt A, De Milde L, Van Leene J. 58.  et al. 2015. A repressor protein complex regulates leaf growth in Arabidopsis. Plant Cell 27:82273–87 [Google Scholar]
  59. Gonzalez N, Vanhaeren H, Inzé D. 59.  2012. Leaf size control: complex coordination of cell division and expansion. Trends Plant Sci 17:6332–40 [Google Scholar]
  60. Granier C, Tardieu F. 60.  1998. Spatial and temporal analyses of expansion and cell cycle in sunflower leaves: a common pattern of development for all zones of a leaf and different leaves of a plant. Plant Physiol 116:3991–1001 [Google Scholar]
  61. Grebe M.61.  2012. The patterning of epidermal hairs in Arabidopsis—updated. Curr. Opin. Plant Biol. 15:131–37 [Google Scholar]
  62. Green AA, Kennaway JR, Hanna AI, Bangham JA, Coen ES. 62.  2010. Genetic control of organ shape and tissue polarity. PLOS Biol 8:11e1000537 [Google Scholar]
  63. Green PB.63.  1962. Mechanism for plant cellular morphogenesis. Science 138:35481404–5 [Google Scholar]
  64. Green PB.64.  1968. Growth physics in Nitella: a method for continuous in vivo analysis of extensibility based on a micro-manometer technique for turgor pressure. Plant Physiol 43:81169–84 [Google Scholar]
  65. Green PB, King A. 65.  1966. A mechanism for the origin of specifically oriented textures in development with special reference to Nitella wall texture. Aust. J. Biol. Sci. 19:421–37 [Google Scholar]
  66. Green RH.66.  1966. Measurement of non-randomness in spatial distributions. Res. Popul. Ecol. 8:11–7 [Google Scholar]
  67. Grieneisen VA, Scheres B. 67.  2012. Morphogengineering roots: comparing mechanisms of morphogen gradient formation. BMC Syst. Biol. 6:37 [Google Scholar]
  68. Hamant O, Heisler MG, Jönsson H, Krupinski P, Uyttewaal M. 68.  et al. 2008. Developmental patterning by mechanical signals in Arabidopsis. Science 322:59081650–55 [Google Scholar]
  69. Hanada K, Higuchi-Takeuchi M. 69.  2013. Small open reading frames associated with morphogenesis are hidden in plant genomes. PNAS 110:62395–2400 [Google Scholar]
  70. He F, Saunders TE, Wen Y, Cheung D, Jiao R. 70.  et al. 2010. Shaping a morphogen gradient for positional precision. Biophys. J. 99:3697–707 [Google Scholar]
  71. Heisler MG, Hamant O, Krupinski P, Uyttewaal M, Ohno C. 71.  et al. 2010. Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLOS Biol 8:10e1000516 [Google Scholar]
  72. Hejnowicz Z, Rusin A, Rusin T. 72.  2000. Tensile tissue stress affects the orientation of cortical microtubules in the epidermis of sunflower hypocotyl. J. Plant Growth Regul. 19:131–44 [Google Scholar]
  73. Hepler PK, Vidali L, Cheung AY. 73.  2001. Polarized cell growth in higher plants. Annu. Rev. Cell Dev. Biol. 17:159–87 [Google Scholar]
  74. Hepworth J, Lenhard M. 74.  2014. Regulation of plant lateral-organ growth by modulating cell number and size. Curr. Opin. Plant Biol. 17:36–42 [Google Scholar]
  75. Hervieux N, Dumond M, Sapala A, Routier-Kierzkowska A-L, Kierzkowski D. 75.  et al. 2016. A mechanical feedback restricts sepal growth and shape in Arabidopsis. Curr. Biol 26:1019–28Shows how a mechanical conflict in growing sepals between slow-growing tip and fast-growing base restricts lateral growth of the tip, contributing to final organ shape. [Google Scholar]
  76. Higaki T, Kutsuna N, Sano T, Kondo N, Hasezawa S. 76.  2010. Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells. Plant J 61:1156–65 [Google Scholar]
  77. Hong L, Brown J, Segerson NA, Rose JKC, Roeder AHK. 77.  2017. CUTIN SYNTHASE 2 maintains progressively developing cuticular ridges in Arabidopsis sepals. Mol. Plant 10:4560–74 [Google Scholar]
  78. Hong L, Dumond M, Tsugawa S, Sapala A, Routier-Kierzkowska A-L. 78.  et al. 2016. Variable cell growth yields reproducible organ development through spatiotemporal averaging. Dev. Cell 38:15–32Shows that variability in cell growth is averaged over space and time (spatiotemporal averaging) to produce regular organs. [Google Scholar]
  79. Hong L, Roeder AHK. 79.  2017. Plant development: differential growth rates in distinct zones shape an ancient plant form. Curr. Biol. 27:1R19–21 [Google Scholar]
  80. Houchmandzadeh B, Wieschaus E, Leibler S. 80.  2002. Establishment of developmental precision and proportions in the early Drosophila embryo. Nature 415:6873798–802 [Google Scholar]
  81. Imai KK, Ohashi Y, Tsuge T, Yoshizumi T, Matsui M. 81.  et al. 2006. The A-type cyclin CYCA2;3 is a key regulator of ploidy levels in Arabidopsis endoreduplication. Plant Cell 18:2382–96 [Google Scholar]
  82. Jacques E, Buytaert J, Wells DM, Lewandowski M, Bennett MJ. 82.  et al. 2013. MicroFilament Analyzer, an image analysis tool for quantifying fibrillar orientation, reveals changes in microtubule organization during gravitropism. Plant J 74:61045–58 [Google Scholar]
  83. Jones AR, Forero-Vargas M, Withers SP, Smith RS, Traas J. 83.  et al. 2017. Cell-size dependent progression of the cell cycle creates homeostasis and flexibility of plant cell size. Nat. Commun. 8:15060 [Google Scholar]
  84. Jönsson H, Heisler MG, Shapiro BE, Meyerowitz EM, Mjolsness E. 84.  2006. An auxin-driven polarized transport model for phyllotaxis. PNAS 103:51633–38 [Google Scholar]
  85. Kalve S, De Vos D, Beemster GTS. 85.  2014. Leaf development: a cellular perspective. Front. Plant Sci. 5:362 [Google Scholar]
  86. Kaplan DR.86.  1992. The relationship of cells to organisms in plants: problem and implications of an organismal perspective. Int. J. Plant Sci. 153:3S28–37 [Google Scholar]
  87. Kaplan DR, Hagemann W. 87.  1991. The relationship of cell and organism in vascular plants. BioScience 41:10693–703 [Google Scholar]
  88. Karidas P, Challa KR, Nath U. 88.  2015. The tarani mutation alters surface curvature in Arabidopsis leaves by perturbing the patterns of surface expansion and cell division. J. Exp. Bot. 66:72107–22 [Google Scholar]
  89. Katagiri Y, Hasegawa J, Fujikura U, Hoshino R, Matsunaga S, Tsukaya H. 89.  2016. The coordination of ploidy and cell size differs between cell layers in leaves. Development 143:71120–25 [Google Scholar]
  90. Kennaway R, Coen ES, Green A, Bangham A. 90.  2011. Generation of diverse biological forms through combinatorial interactions between tissue polarity and growth. PLOS Comput. Biol. 7:6e1002071 [Google Scholar]
  91. Kha H, Tuble SC, Kalyanasundaram S, Williamson RE. 91.  2010. WallGen, software to construct layered cellulose–hemicellulose networks and predict their small deformation mechanics. Plant Physiol 152:2774–86 [Google Scholar]
  92. Kierzkowski D, Nakayama N, Routier-Kierzkowska AL, Weber A, Bayer E. 92.  et al. 2012. Elastic domains regulate growth and organogenesis in the plant shoot apical meristem. Science 335:60721096–99 [Google Scholar]
  93. Kroeger J, Geitmann A. 93.  2012. The pollen tube paradigm revisited. Curr. Opin. Plant Biol. 15:6618–24 [Google Scholar]
  94. Kuchen EE, Fox S, Barbier de Reuille P, Kennaway R, Bensmihen S. 94.  et al. 2012. Generation of leaf shape through early patterns of growth and tissue polarity. Science 335:60721092–96 [Google Scholar]
  95. Kwiatkowska D.95.  2004. Surface growth at the reproductive shoot apex of Arabidopsis thaliana pin-formed 1 and wild type. J. Exp. Bot. 55:3991021–32 [Google Scholar]
  96. Landrein B, Hamant O. 96.  2013. How mechanical stress controls microtubule behavior and morphogenesis in plants: history, experiments and revisited theories. Plant J 75:2324–38 [Google Scholar]
  97. Lindeboom JJ, Nakamura M, Hibbel A, Shundyak K, Gutierrez R. 97.  et al. 2013. A mechanism for reorientation of cortical microtubule arrays driven by microtubule severing. Science 342:61631245533 [Google Scholar]
  98. Lintilhac PM, Vesecky TB. 98.  1984. Stress-induced alignment of division plane in plant tissues grown in vitro. Nature 307:5949363–64 [Google Scholar]
  99. Liu Y-B, Lu S-M, Zhang J-F, Liu S, Lu Y-T. 99.  2007. A xyloglucan endotransglucosylase/hydrolase involves in growth of primary root and alters the deposition of cellulose in Arabidopsis. Planta 226:61547–60 [Google Scholar]
  100. Livanos P, Galatis B, Apostolakos P. 100.  2016. Deliberate ROS production and auxin synergistically trigger the asymmetrical division generating the subsidiary cells in Zea mays stomatal complexes. Protoplasma 253:1081–99 [Google Scholar]
  101. Louveaux M, Julien J-D, Mirabet V, Boudaoud A, Hamant O. 101.  2016. Cell division plane orientation based on tensile stress in Arabidopsis thaliana. PNAS 113:30E4294–303Argues that the cell division plane is determined by mechanical stress, which accounts for previous rules based on the geometry of the cell. [Google Scholar]
  102. Lu D, Wang T, Persson S, Mueller-Roeber B, Schippers JHM. 102.  2014. Transcriptional control of ROS homeostasis by KUODA1 regulates cell expansion during leaf development. Nat. Commun. 5:3767 [Google Scholar]
  103. Ludevid D, Höfte H, Himelblau E, Chrispeels MJ. 103.  1992. The expression pattern of the tonoplast intrinsic protein γ-TIP in Arabidopsis thaliana is correlated with cell enlargement. Plant Physiol 100:41633–39 [Google Scholar]
  104. Lynch TM, Lintilhac PM. 104.  1997. Mechanical signals in plant development: a new method for single cell studies. Dev. Biol. 181:2246–56 [Google Scholar]
  105. Marquez JP.105.  2006. Fourier analysis and automated measurement of cell and fiber angular orientation distributions. Int. J. Solids Struct. 43:216413–23 [Google Scholar]
  106. Marshall WF, Young KD, Swaffer M, Wood E, Nurse P. 106.  et al. 2012. What determines cell size?. BMC Biol 10:1101 [Google Scholar]
  107. Martinez P, Luo A, Sylvester A, Rasmussen CG. 107.  2017. Proper division plane orientation and mitotic progression together allow normal growth of maize. PNAS 114:102759–64 [Google Scholar]
  108. Melaragno JE, Mehrotra B, Coleman AW. 108.  1993. Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5:111661–68 [Google Scholar]
  109. Meyer HM, Roeder AHK. 109.  2014. Stochasticity in plant cellular growth and patterning. Front. Plant Sci. 5:420 [Google Scholar]
  110. Meyer HM, Teles J, Formosa-Jordan P, Refahi Y, San-Bento R. 110.  et al. 2017. Fluctuations of the transcription factor ATML1 generate the pattern of giant cells in the Arabidopsis sepal. eLife 6:e19131 [Google Scholar]
  111. Miedes E, Suslov D, Vandenbussche F, Kenobi K, Ivakov A. 111.  et al. 2013. Xyloglucan endotransglucosylase/hydrolase (XTH) overexpression affects growth and cell wall mechanics in etiolated Arabidopsis hypocotyls. J. Exp. Bot. 64:82481–97 [Google Scholar]
  112. Milani P, Braybrook SA, Boudaoud A. 112.  2013. Shrinking the hammer: micromechanical approaches to morphogenesis. J. Exp. Bot. 64:154651–62 [Google Scholar]
  113. Milani P, Gholamirad M, Traas J, Arnéodo A, Boudaoud A. 113.  et al. 2011. In vivo analysis of local wall stiffness at the shoot apical meristem in Arabidopsis using atomic force microscopy. Plant J 67:61116–23 [Google Scholar]
  114. Milani P, Mirabet V, Cellier C, Rozier F, Hamant O. 114.  et al. 2014. Matching patterns of gene expression to mechanical stiffness at cell resolution through quantitative tandem epifluorescence and nanoindentation. Plant Physiol 165:41399–1408 [Google Scholar]
  115. Miyoshi K, Ahn B-O, Kawakatsu T, Ito Y, Itoh J-I. 115.  et al. 2004. PLASTOCHRON1, a timekeeper of leaf initiation in rice, encodes cytochrome P450. PNAS 101:3875–80 [Google Scholar]
  116. Mizukami Y.116.  2001. A matter of size: developmental control of organ size in plants. Curr. Opin. Plant Biol. 4:533–39 [Google Scholar]
  117. Mosca G, Sapala A, Strauss S, Routier-Kierzkowska A-L, Smith RS. 117.  2017. On the micro-indentation of plant cells in a tissue context. Phys. Biol. 14:1015003 [Google Scholar]
  118. Nakayama N, Smith RS, Mandel T, Robinson S, Kimura S. 118.  et al. 2012. Mechanical regulation of auxin-mediated growth. Curr. Biol. 22:161468–76 [Google Scholar]
  119. Nath U, Crawford BCW, Carpenter R, Coen ES. 119.  2003. Genetic control of surface curvature. Science 299:56111404–7 [Google Scholar]
  120. Nelissen H, Rymen B, Jikumaru Y, Demuynck K, Van Lijsebettens M. 120.  et al. 2012. A local maximum in gibberellin levels regulates maize leaf growth by spatial control of cell division. Curr. Biol. 22:131183–87 [Google Scholar]
  121. Paredez AR, Somerville CR, Ehrhardt DW. 121.  2006. Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:57791491–95 [Google Scholar]
  122. Paulsson J.122.  2005. Models of stochastic gene expression. Phys. Life Rev. 2:2157–75 [Google Scholar]
  123. Peaucelle A, Braybrook SA, Le Guillou L Bron E, Kuhlemeier C, Höfte H. 123.  2011. Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Curr. Biol 21:201720–26 [Google Scholar]
  124. Peaucelle A, Louvet R, Johansen JN, Höfte H, Laufs P. 124.  et al. 2008. Arabidopsis phyllotaxis is controlled by the methyl-esterification status of cell-wall pectins. Curr. Biol. 18:241943–48 [Google Scholar]
  125. Peaucelle A, Wightman R, Höfte H. 125.  2015. The control of growth symmetry breaking in the Arabidopsis hypocotyl. Curr. Biol. 25:131746–52 [Google Scholar]
  126. Péret B, Li G, Zhao J, Band LR, Voss U. 126.  et al. 2012. Auxin regulates aquaporin function to facilitate lateral root emergence. Nat. Cell Biol. 14:10991–98 [Google Scholar]
  127. Plavskin Y, Nagashima A, Perroud P-F, Hasebe M, Quatrano RS. 127.  et al. 2016. Ancient trans-acting siRNAs confer robustness and sensitivity onto the auxin response. Dev. Cell 36:3276–89 [Google Scholar]
  128. Ralph J, Bunzel M, Marita JM, Hatfield RD, Lu F. 128.  et al. 2004. Peroxidase-dependent cross-linking reactions of P-hydroxycinnamates in plant cell walls. Phytochem. Rev. 3:1–279–96 [Google Scholar]
  129. Ranjan A, Townsley BT, Ichihashi Y, Sinha NR, Chitwood DH. 129.  2015. An intracellular transcriptomic atlas of the giant coenocyte Caulerpa taxifolia. PLOS Genet 11:1e1004900 [Google Scholar]
  130. Rasmussen CG, Humphries JA, Smith LG. 130.  2011. Determination of symmetric and asymmetric division planes in plant cells. Annu. Rev. Plant Biol. 62:387–409 [Google Scholar]
  131. Rebocho AB, Southam P, Kennaway JR, Bangham JA, Coen ES. 131.  2017. Generation of shape complexity through tissue conflict resolution. eLife 6:e20156Uses models to analyze how mechanical tissue conflicts generate bending and buckling of tissue, and contribute to final organ shapes. [Google Scholar]
  132. Rodríguez AA, Grunberg KA, Taleisnik EL. 132.  2002. Reactive oxygen species in the elongation zone of maize leaves are necessary for leaf extension. Plant Physiol 129:41627–32 [Google Scholar]
  133. Roeder AHK.133.  2012. When and where plant cells divide: a perspective from computational modeling. Curr. Opin. Plant Biol. 15:6638–44 [Google Scholar]
  134. Roeder AHK, Chickarmane V, Cunha A, Obara B, Manjunath BS, Meyerowitz EM. 134.  2010. Variability in the control of cell division underlies sepal epidermal patterning in Arabidopsis thaliana. PLOS Biol 8:5e1000367 [Google Scholar]
  135. Roeder AHK, Cunha A, Burl MC, Meyerowitz EM. 135.  2012. A computational image analysis glossary for biologists. Development 139:173071–80 [Google Scholar]
  136. Roeder AHK, Cunha A, Ohno CK, Meyerowitz EM. 136.  2012. Cell cycle regulates cell type in the Arabidopsis sepal. Development 139:4416–27 [Google Scholar]
  137. Rolland-Lagan AG, Remmler L, Girard-Bock C. 137.  2014. Quantifying shape changes and tissue deformation in leaf development. Plant Physiol 165:2496–505 [Google Scholar]
  138. Routier-Kierzkowska A-L, Smith RS. 138.  2013. Measuring the mechanics of morphogenesis. Curr. Opin. Plant Biol. 16:125–32 [Google Scholar]
  139. Runions A, Tsiantis M, Prusinkiewicz P. 139.  2017. A common developmental program can produce diverse leaf shapes. New Phytol 216:401–18 [Google Scholar]
  140. Rygol J, Pritchard J, Zhu JJ, Tomos AD, Zimmermann U. 140.  1993. Transpiration induces radial turgor pressure gradients in wheat and maize roots. Plant Physiol 103:2493–500 [Google Scholar]
  141. Sagner A, Briscoe J. 141.  2017. Morphogen interpretation: concentration, time, competence, and signaling dynamics. Wiley Interdiscip. Rev. Dev. Biol. 6:4e271 [Google Scholar]
  142. Sander EA, Barocas VH. 142.  2009. Comparison of 2D fiber network orientation measurement methods. J. Biomed. Mater. Res. A 88:2322–31 [Google Scholar]
  143. Sassi M, Vernoux T. 143.  2013. Auxin and self-organization at the shoot apical meristem. J. Exp. Bot. 64:92579–92 [Google Scholar]
  144. Saunders TE, Pan KZ, Angel A, Guan Y, Shah JV. 144.  et al. 2012. Noise reduction in the intracellular pom1p gradient by a dynamic clustering mechanism. Dev. Cell 22:3558–72 [Google Scholar]
  145. Sauret-Güeto S, Schiessl K, Bangham A, Sablowski R, Coen ES. 145.  2013. JAGGED controls Arabidopsis petal growth and shape by interacting with a divergent polarity field. PLOS Biol 11:4e1001550 [Google Scholar]
  146. Schaefer E, Belcram K, Uyttewaal M, Duroc Y, Goussot M. 146.  et al. 2017. The preprophase band of microtubules controls the robustness of division orientation in plants. Science 356:6334186–89Shows disrupting the preprophase band does not block cell division or affect the average division plane orientation, but instead increases the variability in orientation of new cell walls. [Google Scholar]
  147. Schiessl K, Muino JM, Sablowski R. 147.  2014. Arabidopsis JAGGED links floral organ patterning to tissue growth by repressing Kip-related cell cycle inhibitors. PNAS 111:72830–35 [Google Scholar]
  148. Schmiedel JM, Klemm SL, Zheng Y, Sahay A, Bluethgen N. 148.  et al. 2015. MicroRNA control of protein expression noise. Science 348:6230128–32 [Google Scholar]
  149. Schmoller KM, Turner JJ, Kõivomägi M, Skotheim JM. 149.  2015. Dilution of the cell cycle inhibitor Whi5 controls budding-yeast cell size. Nature 526:7572268–72 [Google Scholar]
  150. Schnyder H, Seo S, Rademacher IF, Kühbauch W. 150.  1990. Spatial distribution of growth rates and of epidermal cell lengths in the elongation zone during leaf development in Lolium perenne L. Planta 181:3423–31 [Google Scholar]
  151. Shapiro BE, Tobin C, Mjolsness E, Meyerowitz EM. 151.  2015. Analysis of cell division patterns in the Arabidopsis shoot apical meristem. PNAS 112:154815–20 [Google Scholar]
  152. Smith RS, Guyomarc'h S, Mandel T, Reinhardt D, Kuhlemeier C, Prusinkiewicz P. 152.  2006. A plausible model of phyllotaxis. PNAS 103:51301–6 [Google Scholar]
  153. Soifer I, Robert L, Amir A. 153.  2016. Single-cell analysis of growth in budding yeast and bacteria reveals a common size regulation strategy. Curr. Biol. 26:3356–61 [Google Scholar]
  154. Solly JE, Cunniffe NJ, Harrison CJ. 154.  2017. Regional growth rate differences specified by apical notch activities regulate liverwort thallus shape. Curr. Biol. 27:116–26 [Google Scholar]
  155. Somerville C, Bauer S, Brininstool G, Facette M, Hamann T. 155.  et al. 2004. Toward a systems approach to understanding plant cell walls. Science 306:57052206–11 [Google Scholar]
  156. Sugimoto-Shirasu K, Roberts K. 156.  2003. “Big it up”: endoreduplication and cell-size control in plants. Curr. Opin. Plant Biol. 6:6544–53 [Google Scholar]
  157. Sylvester AW, Smith LG. 157.  2009. Cell biology of maize leaf development. Handbook of Maize: Its Biology JL Bennetzen, SC Hake 179–203 New York: Springer [Google Scholar]
  158. Szymanski DB, Marks MD. 158.  1998. GLABROUS1 overexpression and TRIPTYCHON alter the cell cycle and trichome cell fate in Arabidopsis. Plant Cell 10:122047–62 [Google Scholar]
  159. Taheri-Araghi S, Bradde S, Sauls JT, Hill NS, Levin PA. 159.  et al. 2015. Cell-size control and homeostasis in bacteria. Curr. Biol. 25:3385–91 [Google Scholar]
  160. Tauriello G, Meyer HM, Smith RS, Koumoutsakos P, Roeder AHK. 160.  2015. Variability and constancy in cellular growth of Arabidopsis sepals. Plant Physiol 169:42342–58Analyzes variability in cell growth and finds Arabidopsis sepal cells reach a common maximum relative growth rate at different times. [Google Scholar]
  161. Traas J, Hülskamp M, Gendreau E, Höfte H. 161.  1998. Endoreduplication and development: rule without dividing?. Curr. Opin. Plant Biol. 1:6498–503 [Google Scholar]
  162. Tsimring LS.162.  2014. Noise in biology. Rep. Prog. Phys. 77:2026601 [Google Scholar]
  163. Tsugawa S, Hervieux N, Hamant O, Boudaoud A, Smith RS. 163.  et al. 2016. Extracting subcellular fibrillar alignment with error estimation: application to microtubules. Biophys. J. 110:81836–44 [Google Scholar]
  164. Tsugawa S, Hervieux N, Kierzkowski D, Routier-Kierzkowska A-L, Sapala A. 164.  et al. 2017. Clones of cells switch from reduction to enhancement of size variability in Arabidopsis sepals. Development 144:4398–405Finds clones of cells initially maintain size homeostasis before switching growth patterns to increase variability in developing Arabidopsis sepals. [Google Scholar]
  165. Tsukagoshi H, Busch W, Benfey PN. 165.  2010. Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:4606–16 [Google Scholar]
  166. Uyttewaal M, Burian A, Alim K, Landrein B, Borowska-Wykręt D. 166.  et al. 2012. Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis. Cell 149:2439–51Examines the maintenance of growth heterogeneity and suggests that strong mechanical feedback signals can maintain differences in growth rate between neighboring cells. [Google Scholar]
  167. Vogler H, Draeger C, Weber A, Felekis D, Eichenberger C. 167.  et al. 2012. The pollen tube: a soft shell with a hard core. Plant J 73:4617–27 [Google Scholar]
  168. Vogler H, Felekis D, Nelson BJ, Grossniklaus U. 168.  2015. Measuring the mechanical properties of plant cell walls. Plants 4:2167–82 [Google Scholar]
  169. Volkov V, Hachez C, Moshelion M, Draye X, Chaumont F, Fricke W. 169.  2007. Water permeability differs between growing and non-growing barley leaf tissues. J. Exp. Bot. 58:3377–90 [Google Scholar]
  170. von Dassow G Meir E, Munro EM, Odell GM. 170.  2000. The segment polarity network is a robust developmental module. Nature 406:6792188–92 [Google Scholar]
  171. Wang Z, Li N, Jiang S, Gonzalez N, Huang X. 171.  et al. 2016. SCFSAP controls organ size by targeting PPD proteins for degradation in Arabidopsis thaliana. Nat. Commun 7:11192 [Google Scholar]
  172. Weber A, Braybrook S, Huflejt M, Mosca G, Routier-Kierzkowska A-L, Smith RS. 172.  2015. Measuring the mechanical properties of plant cells by combining micro-indentation with osmotic treatments. J. Exp. Bot. 66:113229–41 [Google Scholar]
  173. White DWR.173.  2006. PEAPOD regulates lamina size and curvature in Arabidopsis. PNAS 103:3513238–43 [Google Scholar]
  174. Williamson RE.174.  1990. Alignment of cortical microtubules by anisotropic wall stresses. Aust. J. Plant Physiol. 17:6601–13 [Google Scholar]
  175. Willis L, Refahi Y, Wightman R, Landrein B, Teles J. 175.  et al. 2016. Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche. PNAS 113:51E8238–46Analyzes mechanisms for maintaining cell size homeostasis in the Arabidopsis meristem. [Google Scholar]
  176. Wisniewska J.176.  2006. Polar PIN localization directs auxin flow in plants. Science 312:5775883 [Google Scholar]
  177. Xue J, Luo D, Xu D, Zeng M, Cui X. 177.  et al. 2015. CCR1, an enzyme required for lignin biosynthesis in Arabidopsis, mediates cell proliferation exit for leaf development. Plant J 83:3375–87 [Google Scholar]
  178. Yakubov GE, Bonilla MR, Chen H, Doblin MS, Bacic A. 178.  et al. 2016. Mapping nano-scale mechanical heterogeneity of primary plant cell walls. J. Exp. Bot. 67:92799–2816 [Google Scholar]
  179. Yeoman MM, Brown R. 179.  1971. Effects of mechanical stress on the plane of cell division in developing callus cultures. Ann. Bot. 35:51102–12 [Google Scholar]
  180. Yi H, Puri VM. 180.  2012. Architecture-based multiscale computational modeling of plant cell wall mechanics to examine the hydrogen-bonding hypothesis of the cell wall network structure model. Plant Physiol 160:31281–92 [Google Scholar]
  181. Yi Q, Coppolino MG. 181.  2006. Automated classification and quantification of F-actin-containing ruffles in confocal micrographs. BioTechniques 40:6745–55 [Google Scholar]
  182. Yoshida S, Barbier de Reuille P, Lane B, Bassel GW, Prusinkiewicz P. 182.  et al. 2014. Genetic control of plant development by overriding a geometric division rule. Dev. Cell 29:175–87 [Google Scholar]
  183. Zagorski M, Tabata Y, Brandenberg N, Lutolf MP, Tkačik G. 183.  et al. 2017. Decoding of position in the developing neural tube from antiparallel morphogen gradients. Science 356:63451379–83 [Google Scholar]
  184. Zar JH.184.  2010. Biostatistical Analysis New York: Pearson. , 5th ed..
  185. Zwillinger D, Kokoska S. 185.  2000. CRC Standard Probability and Statistics Tables and Formulae Boca Raton, FL: CRC Press
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