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Insights into the Cell Wall and Cytoskeletal Regulation by Mechanical Forces in Plants

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The Cytoskeleton

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 24))

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Abstract

Morphogenesis is a highly controlled biological process that causes a plant to develop particularly shaped organs. During this process, directional growth of cells is achieved by a combinatorial action of isotropic turgor driven expansion, which is spatially constrained or relaxed by either deposition or modification of cell wall polymers. Immense networks of genes and signaling cascades have been identified to govern the process of morphogenesis. However, for shape changes to occur concurrent modulations to structural properties of the cell wall that encapsulates plant cells are necessary. The microtubule cytoskeleton via its regulation of cellulose deposition and the activity of cell wall modifying enzymes controls directional growth and cell wall stiffness, respectively influencing morphogenesis. In this chapter, we outline the components that contribute to the mechanics of plant cells and organs that ultimately regulate plant growth and form.

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References

  • Ambrose JC, Shoji T, Kotzer AM, Pighin JA, Wasteneys GO (2007) The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division. Plant Cell 19:2763–2775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ambrose C, Allard JF, Cytrynbaum EN, Wasteneys GO (2011) A CLASP-modulated cell edge barrier mechanism drives cell-wide cortical microtubule organization in Arabidopsis. Nat Commun 2:430

    Article  PubMed  CAS  Google Scholar 

  • Anderson CT, Carroll A, Akhmetova L, Somerville C (2010) Real-time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots. Plant Physiol 152:787–796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anthony RG, Hussey PJ (1999) Dinitroaniline herbicide resistance and the microtubule cytoskeleton. Trends Plant Sci 4:112–116

    Article  CAS  PubMed  Google Scholar 

  • Arioli T, Peng L, Betzner AS, Burn J, Wittke W, Herth W, Camilleri C, Hofte H, Plazinski J, Birch R, Cork A, Glover J, Redmond J, Williamson RE (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279:717–720

    Article  CAS  PubMed  Google Scholar 

  • Baluska F, Jasik J, Edelmann HG, Salajova T, Volkmann D (2001) Latrunculin B-induced plant dwarfism: plant cell elongation is F-actin-dependent. Dev Biol 231:113–124

    Article  CAS  PubMed  Google Scholar 

  • Bidhendi AJ, Geitmann A (2016) Relating the mechanics of the primary plant cell wall to morphogenesis. J Exp Bot 67:449–461

    Article  CAS  PubMed  Google Scholar 

  • Branco R, Pearsall EJ, Rundle CA, White RG, Bradby JE, Hardham AR (2017) Quantifying the plant actin cytoskeleton response to applied pressure using nanoindentation. Protoplasma 254:1127–1137

    Article  CAS  PubMed  Google Scholar 

  • Braybrook SA, Peaucelle A (2013) Mechano-chemical aspects of organ formation in Arabidopsis thaliana: the relationship between auxin and pectin. PLoS One 8:e57813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bringmann M, LI E, Sampathkumar A, Kocabek T, Hauser MT, Persson S (2012) POM-POM2/cellulose synthase interacting1 is essential for the functional association of cellulose synthase and microtubules in Arabidopsis. Plant Cell 24:163–177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burk DH, Liu B, Zhong R, Morrison WH, Ye ZH (2001) A katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 13:807–827

    CAS  PubMed  PubMed Central  Google Scholar 

  • Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344:1879–1900

    Article  CAS  PubMed  Google Scholar 

  • Cavalier DM, Lerouxel O, Neumetzler L, Yamauchi K, Reinecke A, Freshour G, Zabotina OA, Hahn MG, Burgert I, Pauly M, Raikhel NV, Keegstra K (2008) Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wall component. Plant Cell 20:1519–1537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan J, Crowell E, Eder M, Calder G, Bunnewell S, Findlay K, Vernhettes S, Hofte H, Lloyd C (2010) The rotation of cellulose synthase trajectories is microtubule dependent and influences the texture of epidermal cell walls in Arabidopsis hypocotyls. J Cell Sci 123:3490–3495

    Article  CAS  PubMed  Google Scholar 

  • Chen T, Teng N, Wu X, Wang Y, Tang W, Samaj J, Baluska F, Lin J (2007) Disruption of actin filaments by latrunculin B affects cell wall construction in Picea meyeri pollen tube by disturbing vesicle trafficking. Plant Cell Physiol 48:19–30

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove DJ (2015) Plant expansins: diversity and interactions with plant cell walls. Curr Opin Plant Biol 25:162–172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cosgrove DJ (2016) Catalysts of plant cell wall loosening. F1000Res 5

    Google Scholar 

  • Cosgrove DJ (2018) Diffuse growth of plant cell walls. Plant Physiol 176:16–27

    Article  CAS  PubMed  Google Scholar 

  • Desprez T, Juraniec M, Crowell EF, Jouy H, Pochylova Z, Parcy F, Hofte H, Gonneau M, Vernhettes S (2007) Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proc Natl Acad Sci U S A 104:15572–15577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Driouich A, Follet-Gueye ML, Bernard S, Kousar S, Chevalier L, Vicre-Gibouin M, Lerouxel O (2012) Golgi-mediated synthesis and secretion of matrix polysaccharides of the primary cell wall of higher plants. Front Plant Sci 3:79

    Article  PubMed  PubMed Central  Google Scholar 

  • Eng RC, Sampathkumar A (2018) Getting into shape: the mechanics behind plant morphogenesis. Curr Opin Plant Biol 46:25–31

    Article  PubMed  Google Scholar 

  • Errera L (1888) Uber zellformen und seifenblasen. Bot Centralbl 34:395–398

    Google Scholar 

  • Fagard M, Desnos T, Desprez T, Goubet F, Refregier G, Mouille G, Mccann M, Rayon C, Vernhettes S, Hofte H (2000) PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12:2409–2424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandes AN, Thomas LH, Altaner CM, Callow P, Forsyth VT, Apperley DC, Kennedy CJ, Jarvis MC (2011) Nanostructure of cellulose microfibrils in spruce wood. Proc Natl Acad Sci U S A 108:E1195–E1203

    Article  PubMed  PubMed Central  Google Scholar 

  • Flanders DJ, Rawlins DJ, Shaw PJ, Lloyd CW (1990) Nucleus-associated microtubules help determine the division plane of plant epidermal cells: avoidance of four-way junctions and the role of cell geometry. J Cell Biol 110:1111–1122

    Article  CAS  PubMed  Google Scholar 

  • Fricke W (2017) Turgor pressure. In: eLS. Wiley, Chichester

    Google Scholar 

  • Fujita M, Himmelspach R, Ward J, Whittington A, Hasenbein N, Liu C, Truong TT, Galway ME, Mansfield SD, Hocart CH, Wasteneys GO (2013) The anisotropy1 D604N mutation in the Arabidopsis cellulose synthase1 catalytic domain reduces cell wall crystallinity and the velocity of cellulose synthase complexes. Plant Physiol 162:74–85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geldner N, Friml J, Stierhof YD, Jurgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428

    Article  CAS  PubMed  Google Scholar 

  • Goodbody KC, Venverloo CJ, Lloyd CW (1991) Laser microsurgery demonstrates that cytoplasmic strands anchoring the nucleus across the vacuole of premitotic plant cells are under tension. Implications for division plane alignment. Development 113:931–939

    Google Scholar 

  • Green PB (1962) Mechanism for plant cellular morphogenesis. Science 138:1404–1405

    Article  CAS  PubMed  Google Scholar 

  • Gu Y, Kaplinsky N, Bringmann M, Cobb A, Carroll A, Sampathkumar A, Baskin TI, Persson S, Somerville CR (2010) Identification of a cellulose synthase-associated protein required for cellulose biosynthesis. Proc Natl Acad Sci U S A 107:12866–12871

    Article  PubMed  PubMed Central  Google Scholar 

  • Gutierrez R, Lindeboom JJ, Paredez AR, Emons AM, Ehrhardt DW (2009) Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat Cell Biol 11:797–806

    Article  CAS  PubMed  Google Scholar 

  • Hamant O, Heisler MG, Jonsson H, Krupinski P, Uyttewaal M, Bokov P, Corson F, Sahlin P, Boudaoud A, Meyerowitz EM, Couder Y, Traas J (2008) Developmental patterning by mechanical signals in Arabidopsis. Science 322:1650–1655

    Article  CAS  PubMed  Google Scholar 

  • Hardham AR, Takemoto D, White RG (2008) Rapid and dynamic subcellular reorganization following mechanical stimulation of Arabidopsis epidermal cells mimics responses to fungal and oomycete attack. BMC Plant Biol 8:63

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 15:1899–1911

    Article  CAS  PubMed  Google Scholar 

  • 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:e1000516

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hocq L, Pelloux J, Lefebvre V (2017) Connecting homogalacturonan-type pectin remodeling to acid growth. Trends Plant Sci 22:20–29

    Article  CAS  PubMed  Google Scholar 

  • Hofmeister W (1863) Zusatze und Berichtigungen zu den 1851 veroffentlichen Untersuchungen der Entwicklung hoherer Kryptogamen. Jahrb Wiss Bot 3:259–193

    Google Scholar 

  • Hu Y, Zhong RQ, Morrison WH, Ye ZH (2003) The Arabidopsis RHD3 gene is required for cell wall biosynthesis and actin organization. Planta 217:912–921

    Article  CAS  PubMed  Google Scholar 

  • Ivakov A, Persson S (2012) Plant cell walls. In: eLS. Wiley, Chichester

    Google Scholar 

  • Kandasamy MK, Mckinney EC, Meagher RB (2009) A single vegetative actin isovariant overexpressed under the control of multiple regulatory sequences is sufficient for normal Arabidopsis development. Plant Cell 21:701–718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kierzkowski D, Nakayama N, Routier-Kierzkowska AL, 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

    Article  CAS  PubMed  Google Scholar 

  • Kubicki JD, Yang H, Sawada D, O’Neill H, Oehme D, Cosgrove D (2018) The shape of native plant cellulose microfibrils. Sci Rep 8:13983

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leyser O (2018) Auxin signaling. Plant Physiol 176:465–479

    Article  CAS  PubMed  Google Scholar 

  • Li S, Lei L, Somerville CR, Gu Y (2012) Cellulose synthase interactive protein 1 (CSI1) links microtubules and cellulose synthase complexes. Proc Natl Acad Sci U S A 109:185–190

    Article  CAS  PubMed  Google Scholar 

  • Livanos P, Muller S (2019) Division plane establishment and cytokinesis. Annu Rev Plant Biol 70:239–267

    Article  PubMed  Google Scholar 

  • Louveaux M, Hamant O (2013) The mechanics behind cell division. Curr Opin Plant Biol 16:774–779

    Article  PubMed  Google Scholar 

  • Louveaux M, Julien JD, Mirabet V, Boudaoud A, Hamant O (2016a) Cell division plane orientation based on tensile stress in Arabidopsis thaliana. Proc Natl Acad Sci U S A 113:E4294–E4303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Louveaux M, Rochette S, Beauzamy L, Boudaoud A, Hamant O (2016b) The impact of mechanical compression on cortical microtubules in Arabidopsis: a quantitative pipeline. Plant J 88:328–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mcfarlane HE, Doring A, Persson S (2014) The cell biology of cellulose synthesis. Annu Rev Plant Biol 65:69–94

    Article  CAS  PubMed  Google Scholar 

  • Mei Y, Gao HB, Yuan M, Xue HW (2012) The Arabidopsis ARCP protein, CSI1, which is required for microtubule stability, is necessary for root and anther development. Plant Cell 24:1066–1080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milani P, Braybrook SA, Boudaoud A (2013) Shrinking the hammer: micromechanical approaches to morphogenesis. J Exp Bot 64:4651–4662

    Article  CAS  PubMed  Google Scholar 

  • Palevitz BA (1987) Actin in the preprophase band of Allium cepa. J Cell Biol 104:1515–1519

    Article  CAS  PubMed  Google Scholar 

  • Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:1491–1495

    Article  CAS  PubMed  Google Scholar 

  • Park YB, Cosgrove DJ (2012) Changes in cell wall biomechanical properties in the xyloglucan-deficient xxt1/xxt2 mutant of Arabidopsis. Plant Physiol 158:465–475

    Article  CAS  PubMed  Google Scholar 

  • Park YB, Cosgrove DJ (2015) Xyloglucan and its interactions with other components of the growing cell wall. Plant Cell Physiol 56:180–194

    Article  CAS  PubMed  Google Scholar 

  • Parre E, Geitmann A (2005) Pectin and the role of the physical properties of the cell wall in pollen tube growth of Solanum chacoense. Planta 220:582–592

    Article  CAS  PubMed  Google Scholar 

  • Peaucelle A, Braybrook SA, Le Guillou L, Bron E, Kuhlemeier C, Hofte H (2011) Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Curr Biol 21:1720–1726

    Article  CAS  PubMed  Google Scholar 

  • Peaucelle A, Braybrook S, Hofte H (2012) Cell wall mechanics and growth control in plants: the role of pectins revisited. Front Plant Sci 3:121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Persson S, Paredez A, Carroll A, Palsdottir H, Doblin M, Poindexter P, Khitrov N, Auer M, Somerville CR (2007) Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc Natl Acad Sci U S A 104:15566–15571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rayle DL, Cleland RE (1992) The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiol 99:1271–1274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Refrégier G, Pelletier S, Jaillard D, Höfte H (2004) Interaction between wall deposition and cell elongation in dark-grown hypocotyl cells in Arabidopsis. Plant Physiol 135:959–968

    Article  PubMed  PubMed Central  Google Scholar 

  • Routier-Kierzkowska AL, Smith RS (2013) Measuring the mechanics of morphogenesis. Curr Opin Plant Biol 16:25–32

    Article  PubMed  Google Scholar 

  • Rubery PH, Sheldrake AR (1974) Carrier-mediated auxin transport. Planta 118:101–121

    Article  CAS  PubMed  Google Scholar 

  • Sachs J (1878) Ueber die Anordnung der Zellen in jüngsten Pflanzentheilen. Arbeiten d Bot Inst 46–104

    Google Scholar 

  • Saladie M, Rose JK, Cosgrove DJ, Catala C (2006) Characterization of a new xyloglucan endotransglucosylase/hydrolase (XTH) from ripening tomato fruit and implications for the diverse modes of enzymic action. Plant J 47:282–295

    Article  CAS  PubMed  Google Scholar 

  • Sampathkumar A, Gutierrez R, Mcfarlane HE, Bringmann M, Lindeboom J, Emons AM, Samuels L, Ketelaar T, Ehrhardt DW, Persson S (2013) Patterning and lifetime of plasma membrane-localized cellulose synthase is dependent on actin organization in Arabidopsis interphase cells. Plant Physiol 162:675–688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sampathkumar A, Krupinski P, Wightman R, Milani P, Berquand A, Boudaoud A, Hamant O, Jonsson H, Meyerowitz EM (2014a) Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. elife 3:e01967

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sampathkumar A, Yan A, Krupinski P, Meyerowitz EM (2014b) Physical forces regulate plant development and morphogenesis. Curr Biol 24:R475–R483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sampathkumar A, Peaucelle A, Fujita M, Schuster C, Persson S, Wasteneys GO, Meyerowitz EM (2019) Primary wall cellulose synthase regulates shoot apical meristem mechanics and growth. Development 146(10). https://doi.org/10.1242/dev.179036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sassi M, Ali O, Boudon F, Cloarec G, Abad U, Cellier C, Chen X, Gilles B, Milani P, Friml J (2014) An auxin-mediated shift toward growth isotropy promotes organ formation at the shoot meristem in Arabidopsis. Curr Biol 24:2335–2342

    Article  CAS  PubMed  Google Scholar 

  • Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289

    Article  CAS  PubMed  Google Scholar 

  • Smith LG (2001) Plant cell division: building walls in the right places. Nat Rev Mol Cell Biol 2:33–39

    Article  CAS  PubMed  Google Scholar 

  • Sugimoto K, Williamson RE, Wasteneys GO (2001) Wall architecture in the cellulose-deficientrsw1 mutant of Arabidopsis thaliana: microfibrils but not microtubules lose their transverse alignment before microfibrils become unrecognizable in the mitotic and elongation zones of roots. Protoplasma 215:172–183

    Article  CAS  PubMed  Google Scholar 

  • Taylor-Teeples M, Lanctot A, Nemhauser JL (2016) As above, so below: auxin’s role in lateral organ development. Dev Biol 419:156–164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas LH, Forsyth VT, Sturcova A, Kennedy CJ, May RP, Altaner CM, Apperley DC, Wess TJ, Jarvis MC (2013) Structure of cellulose microfibrils in primary cell walls from collenchyma. Plant Physiol 161:465–476

    Article  CAS  PubMed  Google Scholar 

  • Uyttewaal M, Burian A, Alim K, Landrein B, Borowska-Wykret D, Dedieu A, Peaucelle A, Ludynia M, Traas J, Boudaoud A, Kwiatkowska D, Hamant O (2012) Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis. Cell 149:439–451

    Article  CAS  PubMed  Google Scholar 

  • Vanstraelen M, Van Damme D, De Rycke R, Mylle E, Inze D, Geelen D (2006) Cell cycle-dependent targeting of a kinesin at the plasma membrane demarcates the division site in plant cells. Curr Biol 16:308–314

    Article  CAS  PubMed  Google Scholar 

  • Wang T, Park YB, Caporini MA, Rosay M, Zhong L, Cosgrove DJ, Hong M (2013) Sensitivity-enhanced solid-state NMR detection of expansin’s target in plant cell walls. Proc Natl Acad Sci U S A 110:16444–16449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu S-Z, Bezanilla M (2018) Actin and microtubule cross talk mediates persistent polarized growth. J Cell Biol 217:3531–3544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao C, Zhang T, Zheng Y, Cosgrove DJ, Anderson CT (2016) Xyloglucan deficiency disrupts microtubule stability and cellulose biosynthesis in Arabidopsis, altering cell growth and morphogenesis. Plant Physiol 170:234–249

    Article  CAS  PubMed  Google Scholar 

  • Yanagisawa M, Desyatova AS, Belteton SA, Mallery EL, Turner JA, Szymanski DB (2015) Patterning mechanisms of cytoskeletal and cell wall systems during leaf trichome morphogenesis. Nat Plants 1:15014

    Article  CAS  PubMed  Google Scholar 

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Wang, Y., Kulshreshtha, R., Sampathkumar, A. (2019). Insights into the Cell Wall and Cytoskeletal Regulation by Mechanical Forces in Plants. In: Sahi, V., Baluška, F. (eds) The Cytoskeleton. Plant Cell Monographs, vol 24. Springer, Cham. https://doi.org/10.1007/978-3-030-33528-1_2

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