Abstract
Expansins are plant cell wall-loosening proteins that promote cell growth and are essential for many critical developmental processes and stress responses. The molecular basis for expansin action is uncertain. Recently, it has been proposed that expansins loosen the wall by means of the generation of mobile conformational defects at the surface of cellulose microfibrils. The present work addresses this hypothesis by elaborating three assumptions: (1) microfibril–matrix interfaces cause steep stress gradients on the microfibril surface, (2) stress gradients drive the motion of conformational defects along the microfibril surface toward the microfibril–matrix interfaces, and (3) the approach of the defects to the microfibril–matrix interfaces facilitates the dissociation of matrix polysaccharides from cellulose microfibrils.
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References
Bergenstrahle M, Thormann E, Nordgren N, Berglund LA (2009) Force pulling of single cellulose chains at the crystalline cellulose–liquid interface: a molecular dynamics study. Langmuir 25:4635–4642. doi:10.1021/la803915c
Boyd RH (1985) Relaxation processes in crystalline polymers: molecular interpretation—a review. Polymer 26:1123–1133. doi:10.1016/0032-3861(85)90240-X
Carey RE, Hepler NK, Cosgrove DJ (2013) Selaginella moellendorffii has a reduced and highly conserved expansin superfamily with genes more closely related to angiosperms than to bryophytes. BMC Plant Biol 13:4. doi:10.1186/1471-2229-13-4
Cheniclet C, Rong WY, Causse M, Frangne N, Bolling L, Carde JP, Renaudin JP (2005) Cell expansion and endoreduplication show a large genetic variability in pericarp and contribute strongly to tomato fruit growth. Plant Physiol 139:1984–1994. doi:10.1104/pp.105.068767
Choi D, Cho H-T, Lee Y (2006) Expansins: expanding importance in plant growth and development. Physiol Plant 126:511–518. doi:10.1111/j.1399-3054.2006.00612.x
Cosgrove DJ (1989) Characterization of long-term extension of isolated cell walls from growing cucumber hypocotyls. Planta 177:121–130
Cosgrove DJ (1993) Water-uptake by growing cells—an assessment of the controlling roles of wall relaxation, solute uptake, and hydraulic conductance. Int J Plant Sci 154:10–21
Cosgrove DJ (1998) Cell wall loosening by expansins. Plant Physiol 118:333–339. doi:10.1104/pp.118.2.333
Cosgrove DJ (2000a) Expansive growth of plant cell walls. Plant Physiol Biochem 28:109–124. doi:10.1016/S0981-9428(00)00164-9
Cosgrove DJ (2000b) Loosening of plant cell walls by expansins. Nature 407:321–326. doi:10.1038/35030000
Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861. doi:10.1038/nrm1746
Cosgrove DJ, Bedinger P, Durachko DM (1997) Group I allergens of grass pollen as cell wall-loosening agents. Proc Natl Acad Sci USA 94:6559–6564
Cosgrove DJ, Durachko DM, Li L-C (1998) Expansins may have cryptic endoglucanase activity and can synergize the breakdown of cellulose by fungal cellulases. Annu Meet Am Soc Plant Physiol Abstr 171
Cosgrove DJ, Li LC, Cho HT, Hoffmann-Benning S, Moore RC, Blecker D (2002) The growing world of expansins. Plant Cell Physiol 43:1436–1444. doi:10.1093/pcp/pcf180
Davies LM, Harris PJ, Newman RH (2002) Molecular ordering of cellulose after extraction of polysaccharides from primary cell walls of Arabidopsis thaliana: a solid-state CP/MAS 13C NMR study. Carbohydr Res 337:587–593. doi:10.1016/S0008-6215(02)00038-1
Dick-Pérez M, Zhang Y, Hayes J, Salazar A, Zabotina OA, Hong M (2011) Structure and interactions of plant cell-wall polysaccharides by two-and three-dimensional magic-angle-spinning solid-state NMR. Biochemistry 50:989–1000. doi:10.1021/bi101795q
Georgelis N, Tabuchi A, Nikolaidis N, Cosgrove DJ (2011) Structure-function analysis of the bacterial expansin EXLX1. J Biol Chem 286:16814–16823. doi:10.1074/jbc.M111.225037
Georgelis N, Yennawar N, Cosgrove DJ (2012) Structural basis for entropy-driven cellulose binding by a type-A cellulose-binding module (CBM) and bacterial expansin. Proc Natl Acad Sci USA 109:14830–14835. doi:10.1073/pnas.1213200109
Hackney JM, Atalla RH, VanderHart DL (1994) Modification of crystallinity and crystalline structure of Acetobacter xylinum cellulose in the presence of water-soluble beta-1,4-linked polysaccharides: 13C-NMR Evidence. Int J Biol Macromol 16:215–218
Hardy BJ, Sarko A (1996) Molecular dynamic simulations and diffraction-based analysis of the native cellulose fibre: structural modeling of the I-α and I-β phases and their interconversion. Polymer 37:1833–1839. doi:10.1016/0032-3861(96)87299-5
Horikawa Y, Sugiyama J (2009) Localization of crystalline allomorphs in cellulose microfibril. Biomacromolecules 10:2235–2239. doi:10.1021/bm900413k
Jarvis MC (2000) Interconversion of the Iα and Iβ crystalline forms of cellulose by bending. Carbohydr Res 325:150–154. doi:10.1016/S0008-6215(99)00316-X
Kerff F, Amoroso A, Herman R, Sauvage E, Petrella S, Filée P, Charlier P, Joris B, Tabuchi A, Nikolaidis N, Cosgrove DJ (2008) Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization. Proc Natl Acad Sci USA 105:16876–16881. doi:10.1073/pnas.0809382105
Kutschera U (1996) Cessation of cell elongation in rye coleoptiles is accompanied by a loss of cell-wall plasticity. J Exp Bot 47:1387–1394. doi:10.1093/jxb/47.9.1387
Li Z-C, Durachko DM, Cosgrove DJ (1993) An oat coleoptile wall protein that induces wall extension in vitro and that is antigenically related to a similar protein from cucumber hypocotyls. Planta 191:349–356. doi:10.1007/BF00195692
Lipchinsky A (2010) A model for expansin action by activation of soliton excitations in cellulose microfibrils. St. Petersburg University, Bulletin Ser. 3 No 1:108–119
Manevich LI, Simmons VV (2008) Solitons in Macromolecular Systems. Nova Science Publishers, New York, p 134
McQueen-Mason SJ, Cosgrove DJ (1994) Disruption of hydrogen-bonding between plant cell wall polymers by proteins that induce wall extension. Proc Natl Acad Sci USA 91:6574–6578. doi:10.1073/pnas.91.14.6574
McQueen-Mason S, Cosgrove DJ (1995) Expansin mode of action on cell walls. Analysis of wall hydrolysis, stress relaxation, and binding. Plant Physiol 107:87–100
McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell-wall extension in plants. Plant Cell 4:1425–1433. doi:10.1105/tpc.4.11.1425
McQueen-Mason SJ, Fry SC, Durachko DM, Cosgrove DJ (1993) The relationship between xyloglucan endotransglycosylase and in vitro cell wall extension in cucumber hypocotyls. Planta 190:327–331. doi:10.1007/BF00196961
Nishiyama Y, Langan P, Chanzy H (2002) Crystal structure and hydrogen-bonding system in cellulose Iβ from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 124:9074–9082. doi:10.1021/ja0257319
Nishiyama Y, Sugiyama J, Chanzy H, Langan P (2003) Crystal structure and hydrogen bonding system in cellulose Iα from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 125:14300–14306. doi:10.1021/ja037055w
Rondeau-Mouro C, Bouchet B, Pontoire B, Robert P, Mazoyer J, Buléon A (2003) Structural features and potential texturising properties of lemon and maize cellulose microfibrils. Carbohydr Polym 53:241–252. doi:10.1016/S0144-8617(03)00069-9
Rose JKC, Braam J, Fry SC, Nishitani K (2002) The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol 43:1421–1435. doi:10.1093/pcp/pcf171
Ruel K, Nishiyama Y, Joseleau JP (2012) Crystalline and amorphous cellulose in the secondary walls of Arabidopsis. Plant Sci 193–194:48–61. doi:10.1016/j.plantsci.2012.05.008
Schopfer P (2006) Biomechanics of plant growth. Am J Bot 93:1415–1425. doi:10.3732/ajb.93.10.1415
Sharova EI (2007) Expansins: proteins involved in cell wall softening during plant growth and morphogenesis. Russ J Plant Physiol 54:713–727. doi:10.1134/S1021443707060015
Shcherban TY, Shi J, Durachko DM, Guiltinan MJ, McQueen-Mason SJ, Shieh M, Cosgrove DJ (1995) Molecular cloning and sequence analysis of expansins—a highly conserved, multigene family of proteins that mediate cell-wall extension in plants. Proc Natl Acad Sci USA 92:9245–9249. doi:10.1073/pnas.92.20.9245
Smith BG, Harris PJ, Melton LD, Newman RH (1998) Crystalline cellulose in hydrated primary cell walls of three monocotyledons and one dicotyledon. Plant Cell Physiol 39:711–720
Šturcová A, His I, Apperley DC, Sugiyama J, Jarvis MC (2004) Structural details of crystalline cellulose from higher plants. Biomacromolecules 5:1333–1339. doi:10.1021/bm034517p
Tabuchi A, Li L-C, Cosgrove DJ (2011) Matrix solubilization and cell wall weakening by expansin (group-1 allergen) from maize pollen. Plant J 68:546–559. doi:10.1111/j.1365-313X.2011.04705.x
Tokoh C, Takabe K, Sugiyama J, Fujita M (2002) Cellulose synthesized by Acetobacter xylinum in the presence of plant cell wall polysaccharides. Cellulose 9:65–74. doi:10.1023/A:1015827121927
Tomos D, Pritchard J (1994) Biophysical and biochemical control of cell expansion in roots and leaves. J Exp Bot 45:1721–1731
Van Sandt V, Suslov D, Verbelen J-P, Vissenberg K (2007) Xyloglucan endotransglucosylase activity loosens a plant cell wall. Ann Bot 100:1467–1473. doi:10.1093/aob/mcm248
Vandenbussche F, Verbelen J-P, Van Der Straeten D (2005) Of light and length: regulation of hypocotyl growth in Arabidopsis. BioEssays 27:275–284. doi:10.1002/bies.20199
Veytsman BA, Cosgrove DJ (1998) A model of cell wall expansion based on thermodynamics of polymer networks. Biophys J 75:2240–2250. doi:10.1016/S0006-3495(98)77668-4
Viëtor RJ, Newman RH, Ha M-A, Apperley DC, Jarvis MC (2002) Conformational features of crystal-surface cellulose from higher plants. Plant J 30:721–731. doi:10.1046/j.1365-313X.2002.01327.x
Wojtaszek P (2000) Genes and plant cell walls: a difficult relationship. Biol Rev 75:437–475. doi:10.1111/j.1469-185X.2000.tb00051.x
Wojtaszek P, Volkmann D, Baluška F (2004) Polarity and cell walls. In: Lindsey K (ed) Polarity in Plants, Blackwell Publishing,Oxford pp 72–121.
Yennawar NH, Li LC, Dudzinski DM, Tabuchi A, Cosgrove DJ (2006) Crystal structure and activities of EXPB1 (Zea m 1), a β-expansin and group-1 pollen allergen from maize. Proc Natl Acad Sci USA 103:14664–14671. doi:10.1073/pnas.0605979103
Yuan S, Wu Y, Cosgrove DJ (2001) A fungal endoglucanase with plant cell wall extension activity. Plant Physiol 127:324–333. doi:10.1104/pp.127.1.324
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Communicated by A. K. Kononowicz.
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Lipchinsky, A. How do expansins control plant growth? A model for cell wall loosening via defect migration in cellulose microfibrils. Acta Physiol Plant 35, 3277–3284 (2013). https://doi.org/10.1007/s11738-013-1341-7
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DOI: https://doi.org/10.1007/s11738-013-1341-7