Abstract
Morphogenesis involves coordinated cell division and cellular growth. Beyond average growth rate and direction, multicellular growth can also be characterized by its variance, i.e., the level of heterogeneity between individual cells or regions. Because final shapes are usually very reproducible, this raises the question of the contribution of local variability in growth in morphogenesis. Here, we focus on the mechanical conflicts that are associated with differential growth and discuss how mechanical forces, emerging from growth heterogeneity, can serve as cues to channel morphogenesis.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abley K, Locke JCW, Leyser HMO (2016) Developmental mechanisms underlying variable, invariant and plastic phenotypes. Ann Bot 117:733–748
Aegerter-Wilmsen T, Aegerter CM, Hafen E, Basler K (2007) Model for the regulation of size in the wing imaginal disc of Drosophila. Mech Dev 124:318–326
Aigouy B, Farhadifar R, Staple DB, Sagner A, Röper J-C, Jülicher F, Eaton S (2010) Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila. Cell 142:773–786
Aliee M, Röper J-C, Landsberg KP, Pentzold C, Widmann TJ, Jülicher F, Dahmann C (2012) Physical mechanisms shaping the Drosophila dorsoventral compartment boundary. Curr Biol CB 22:967–976
Barbier de Reuille P, Routier-Kierzkowska A-L, Kierzkowski D, Bassel GW, Schüpbach T, Tauriello G, Bajpai N, Strauss S, Weber A, Kiss A et al (2015) MorphoGraphX: a platform for quantifying morphogenesis in 4D. eLife 4:05864
Baskin TI (2005) Anisotropic expansion of the plant cell wall. Annu Rev Cell Dev Biol 21:203–222
Bassel GW, Stamm P, Mosca G, Barbier de Reuille P, Gibbs DJ, Winter R, Janka A, Holdsworth MJ, Smith RS (2014) Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo. Proc Natl Acad Sci USA 111:8685–8690
Beauzamy L, Louveaux M, Hamant O, Boudaoud A (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
Beer FP, Johnston ER (1992) Mechanics of material. McGraw-Hill
Besson S, Dumais J (2011) Universal rule for the symmetric division of plant cells. Proc Natl Acad Sci US A 108:6294–6299
Boudon F, Chopard J, Ali O, Gilles B, Hamant O, Boudaoud A, Traas J, Godin C (2015) A computational framework for 3D mechanical modeling of plant morphogenesis with cellular resolution. PLoS Comput, Biol, p 11
Bozorg B, Krupinski P, Jönsson H (2014) Stress and strain provide positional and directional cues in development. PLoS Comput Biol 10:e1003410
Bringmann M, Landrein B, Schudoma C, Hamant O, Hauser M-T, Persson S (2012) Cracking the elusive alignment hypothesis: the microtubule-cellulose synthase nexus unraveled. Trends Plant Sci 17:666–674
Brunet T, Bouclet A, Ahmadi P, Mitrossilis D, Driquez B, Brunet A-C, Henry L, Serman F, Béalle G, Ménager C et al (2013) Evolutionary conservation of early mesoderm specification by mechanotransduction in Bilateria. Nat Commun 4:2821
Burian A, Ludynia M, Uyttewaal M, Traas J, Boudaoud A, Hamant O, Kwiatkowska D (2013) A correlative microscopy approach relates microtubule behaviour, local organ geometry, and cell growth at the Arabidopsis shoot apical meristem. J Exp Bot 64:5753–5767
Buschmann H, Lloyd CW (2008) Arabidopsis mutants and the network of microtubule-associated functions. Mol Plant 1:888–898
Castle ES (1937) Membrane tension and orientation of structure in the plant cell wall. J Cell Comp Physiol 10:113–121
Coen E, Rebocho AB (2016) Resolving conflicts: modeling genetic control of plant morphogenesis. Dev Cell 38:579–583
Corson F, Hamant O, Bohn S, Traas J, Boudaoud A, Couder Y (2009) Turning a plant tissue into a living cell froth through isotropic growth. Proc Natl Acad Sci USA 106:8453–8458
Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861
Cosgrove DJ (2016) Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes. J Exp Bot 67:463–476
Creff A, Brocard L, Ingram G (2015) A mechanically sensitive cell layer regulates the physical properties of the Arabidopsis seed coat. Nat Commun 6:6382
Durand-Smet P, Chastrette N, Guiroy A, Richert A, Berne-Dedieu A, Szecsi J, Boudaoud A, Frachisse J-M, Bendahmane M, Hamant O et al (2014) A comparative mechanical analysis of plant and animal cells reveals convergence across kingdoms. Biophys J 107:2237–2244
Elsner J, Michalski M, 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
Errera L (1886) Sur une condition fondamentale d’e´ quilibre des cellules vivantes. C R Hebd Seances Acad Sci 822–824
Fal K, Landrein B, Hamant O (2015) Interplay between miRNA regulation and mechanical stress for CUC gene expression at the shoot apical meristem. Plant Signal, Behav
Farge E (2003) Mechanical induction of Twist in the Drosophila foregut/stomodeal primordium. Curr Biol CB 13:1365–1377
Fernandez R, Das P, Mirabet V, Moscardi E, Traas J, Verdeil J-L, Malandain G, Godin C (2010) Imaging plant growth in 4D: robust tissue reconstruction and lineaging at cell resolution. Nat Methods 7:547–553
Fisher DD, Cyr RJ (2000) Mechanical forces in plant growth and development. Bull Publ Am Soc Gravit Space Biol. 13:67–73
Geitmann A, Hush JM, Overall RL (1997) Inhibition of ethylene biosynthesis does not block microtubule re-orientation in wounded pea roots. Protoplasma 198:135–142
Green PB (1962) Mechanism for plant cellular morphogenesis. Science 138:1404–1405
Green P, King A (1966) A mechanism for the origin of specifically oriented textures in development with special reference to Nitella wall texture. Aust J Biol Sci 421–437
Hamant O, Moulia B (2016) How do plants read their own shapes? New Phytol 212:333–337
Hamant O, Heisler MG, Jonsson H, Krupinski P, Uyttewaal M, Bokov P, Corson F, Sahlin P, Boudaoud A, Meyerowitz EM et al (2008) Developmental patterning by mechanical signals in Arabidopsis. Science 322:1650–1655
Hamant O, Traas J, Boudaoud A (2010) Regulation of shape and patterning in plant development. Curr Opin Genet Dev 20:454–459
Heath IB (1974) A unified hypothesis for the role of membrane bound enzyme complexes and microtubules in plant cell wall synthesis. J Theor Biol 48:445–449
Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol CB 15:1899–1911
Heisler MG, Hamant O, Krupinski P, Uyttewaal M, Ohno C, Jonsson H, Traas J, Meyerowitz EM (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
Hejnowicz Z, Rusin A, Rusin T (2000) Tensile tissue stress affects the orientation of cortical microtubules in the epidermis of sunflower hypocotyl. J Plant Growth Regul 19:31–44
Hervieux N, Dumond M, Sapala A, Routier-Kierzkowska A-L, Kierzkowski D, Roeder AHK, Smith RS, Boudaoud A, Hamant O (2016) A mechanical feedback restricts sepal growth and shape in arabidopsis. Curr Biol CB
Hervieux N, Tsugawa S, Fruleux A, Dumond M, Routier-Kierzkowska AL, Komatsuzaki T, Boudaoud A, Larkin JC, Smith RS, Li CB, Hamant O (2017) Mechanical shielding of rapidly growing cells buffers growth heterogeneity and contributes to organ shape reproducibility. Curr Biol 27(22):3468–3479.e4
Himmelspach R, Williamson RE, Wasteneys GO (2003) Cellulose microfibril alignment recovers from DCB-induced disruption despite microtubule disorganization. Plant J Cell Mol Biol 36:565–575
Hofmeister W (1859) Über die Beugungen saftreicher Pflanzenteile nach Erschütterung. Ber Verh Ges Wiss Leipz 175–204
Hong L, Dumond M, Tsugawa S, Sapala A, Routier-Kierzkowska A-L, Zhou Y, Chen C, Kiss A, Zhu M, Hamant O et al (2016) Variable cell growth yields reproducible organdevelopment through spatiotemporal averaging. Dev Cell 38:15–32
Hong L, Dumond M, Zhu M, Tsugawa S, Li CB, Boudaoud A, Hamant O, Roeder AHK (2018) Heterogeneity and robustness in plant morphogenesis: from cells to organs. Annu Rev Plant Biol. https://doi.org/10.1146/annurev-arplant-042817-040517
Keller PJ, Schmidt AD, Wittbrodt J, Stelzer EHK (2008) Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy. Science 322:1065–1069
Kierzkowski D, Nakayama N, Routier-Kierzkowska A-L, Weber A, Bayer E, Schorderet M, Reinhardt D, Kuhlemeier C, Smith RS (2012) Elastic domains regulate growth and organogenesis in the plant shoot apical meristem. Science 335:1096–1099
Kutschera U, Niklas KJ (2007) The epidermal-growth-control theory of stem elongation: an old and a new perspective. J Plant Physiol 164:1395–1409
Landrein B, Kiss A, Sassi M, Chauvet A, Das P, Cortizo M, Laufs P, Takeda S, Aida M, Traas J et al (2015) Mechanical stress contributes to the expression of the STM homeobox gene in Arabidopsis shoot meristems. eLife 4:e07811
Landsberg KP, Farhadifar R, Ranft J, Umetsu D, Widmann TJ, Bittig T, Said A, Jülicher F, Dahmann C (2009) Increased cell bond tension governs cell sorting at the Drosophila anteroposterior compartment boundary. Curr Biol CB 19:1950–1955
Laufs P, Grandjean O, Jonak C, Kiêu K, Traas J (1998) Cellular parameters of the shoot apical meristem in Arabidopsis. Plant Cell 10:1375–1390
Ledbetter MC, Porter KR (1963) A “microtubule” in plant cell fine structure. J Cell Biol 19:239–250
Legoff L, Rouault H, Lecuit T (2013) A global pattern of mechanical stress polarizes cell divisions and cell shape in the growing Drosophila wing disc. Dev Camb Engl. 140:4051–4059
Lintilhac PM, Vesecky TB (1984) Stress-induced alignment of division plane in plant tissues grown in vitro. Nature 307:363–364
Louveaux M, Julien J-D, Mirabet V, Boudaoud A, Hamant O (2016) Cell division plane orientation based on tensile stress in Arabidopsis thaliana. Proc Natl Acad Sci USA 113:E4294–E4303
Maizel A, von Wangenheim D, Federici F, Haseloff J, Stelzer EHK (2011) High-resolution live imaging of plant growth in near physiological bright conditions using light sheet fluorescence microscopy. Plant J Cell Mol Biol 68:377–385
Martin AC, Kaschube M, Wieschaus EF (2009) Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457:495–499
Milani P, Gholamirad M, Traas J, Arneodo A, Boudaoud A, Argoul F, Hamant O (2011) In vivo analysis of local wall stiffness at the shoot apical meristem in Arabidopsis using atomic force microscopy. Plant J Cell Mol Biol 67:1116–1123
Milani P, Mirabet V, Cellier C, Rozier F, Hamant O, Das P, Boudaoud A (2014) Matching patterns of gene expression to mechanical stiffness at cell resolution through quantitative tandem epifluorescence and nanoindentation. Plant Physiol 165
Nakayama N, Smith RS, Mandel T, Robinson S, Kimura S, Boudaoud A, Kuhlemeier C (2012) Mechanical regulation of auxin-mediated growth. Curr Biol CB 22:1468–1476
Pan Y, Heemskerk I, Ibar C, Shraiman BI, Irvine KD (2016) Differential growth triggers mechanical feedback that elevates Hippo signaling. Proc Natl Acad Sci USA
Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:1491–1495
Peaucelle A (2014) AFM-based mapping of the elastic properties of cell walls: at tissue, cellular, and subcellular resolutions. J Vis Exp JoVE
Peaucelle A, Braybrook SA, Le Guillou L, Bron E, Kuhlemeier C, Höfte H (2011) Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Curr Biol CB 21:1720–1726
Peaucelle A, Wightman R, Höfte H (2015) The control of growth symmetry breaking in the Arabidopsis Hypocotyl. Curr Biol CB 25:1746–1752
Péret B, Li G, Zhao J, Band LR, Voß U, Postaire O, Luu D-T, Da Ines O, Casimiro I, Lucas M et al (2012) Auxin regulates aquaporin function to facilitate lateral root emergence. Nat Cell Biol 14:991–998
Peters WS, Tomos AD (1996) The history of tissue tension. Ann Bot 77:657–665
Pouille PA et al (2009) Mechanical signals trigger Myosin II redistribution and mesoderm invagination in Drosophila embryos. Sci Signal 2:ra16
Roeder AHK, Chickarmane V, Cunha A, Obara B, Manjunath BS, Meyerowitz EM (2010) Variability in the control of cell division underlies sepal epidermal patterning in Arabidopsis thaliana. PLoS Biol 8:e1000367
Routier-Kierzkowska A-L, Weber A, Kochova P, Felekis D, Nelson BJ, Kuhlemeier C, Smith RS (2012) Cellular force microscopy for in vivo measurements of plant tissue mechanics. Plant Physiol 158:1514–1522
Sachs J (1878) Über die Anordnung der Zellen in jüngsten Pflanzentheilen. Arb Bot Inst 46–104
Sampathkumar A, Krupinski P, Wightman R, Milani P, Berquand A, Boudaoud A, Hamant O, Jonsson H, Meyerowitz EM (2014) Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. eLife 3
Sassi M, Ali O, Boudon F, Cloarec G, Abad U, Cellier C, Chen X, Gilles B, Milani P, Friml J et al (2014) An auxin-mediated shift toward growth isotropy promotes organ formation at the shoot meristem in Arabidopsis. Curr Biol CB 24:2335–2342
Shraiman BI (2005) Mechanical feedback as a possible regulator of tissue growth. Proc Natl Acad Sci USA 102:3318–3323
Smith RS, Guyomarc’h S, Mandel T, Reinhardt D, Kuhlemeier C, Prusinkiewicz P (2006) A plausible model of phyllotaxis. Proc Natl Acad Sci USA 103:1301–1306
Thompson DW (1917) On growth and form. Cambridge University Press, UK
Uyttewaal M, Burian A, Alim K, Landrein B, Borowska-Wykret D, Dedieu A, Peaucelle A, Ludynia M, Traas J, Boudaoud A et al (2012) Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis. Cell 149:439–451
Vermeer JEM, von Wangenheim D, Barberon M, Lee Y, Stelzer EHK, Maizel A, Geldner N (2014) A spatial accommodation by neighboring cells is required for organ initiation in Arabidopsis. Science 343:178–183
Vlad D, Kierzkowski D, Rast MI, Vuolo F, Dello Ioio R, Galinha C, Gan X, Hajheidari M, Hay A, Smith RS et al (2014) Leaf shape evolution through duplication, regulatory diversification, and loss of a homeobox gene. Science 343:780–783
Williamson R (1990) Alignment of cortical microtubules by anisotropic wall stresses. Aust J Plant Physiol 601–613
Wymer CL, Wymer SA, Cosgrove DJ, Cyr RJ (1996) Plant cell growth responds to external forces and the response requires intact microtubules. Plant Physiol 110:425–430
Yeoman PM, Brown R (1971) Effects of mechanical stress on the plane of cell division in developing callus cultures. Ann Bot 1102–1112
Zerzour R, Kroeger J, Geitmann A (2009) Polar growth in pollen tubes is associated with spatially confined dynamic changes in cell mechanical properties. Dev Biol 334:437–446
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer International Publishing AG, part of Springer Nature
About this chapter
Cite this chapter
Hervieux, N., Hamant, O. (2018). Mechanical Conflicts in Growth Heterogeneity. In: Geitmann, A., Gril, J. (eds) Plant Biomechanics. Springer, Cham. https://doi.org/10.1007/978-3-319-79099-2_9
Download citation
DOI: https://doi.org/10.1007/978-3-319-79099-2_9
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-79098-5
Online ISBN: 978-3-319-79099-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)