THE PLANT CELL, Vol 4, Issue 11 1425-1433, Copyright © 1992 by American Society of Plant Biologists

RESEARCH ARTICLES

Two Endogenous Proteins That Induce Cell Wall Extension in Plants

S. McQueen-Mason, D. M. Durachko and D. J. Cosgrove
Department of Biology, 208 Mueller Laboratory, Pennsylvania State University, University Park, Pennsylvania 16802

Plant cell enlargement is regulated by wall relaxation and yielding, which is thought to be catalyzed by elusive "wall-loosening" enzymes. By employing a reconstitution approach, we found that a crude protein extract from the cell walls of growing cucumber seedlings possessed the ability to induce the extension of isolated cell walls. This activity was restricted to the growing region of the stem and could induce the extension of isolated cell walls from various dicot stems and the leaves of amaryllidaceous monocots, but was less effective on grass coleoptile walls. Endogenous and reconstituted wall extension activities showed similar sensitivities to pH, metal ions, thiol reducing agents, proteases, and boiling in methanol or water. Sequential HPLC fractionation of the active wall extract revealed two proteins with molecular masses of 29 and 30 kD associated with the activity. Each protein, by itself, could induce wall extension without detectable hydrolytic breakdown of the wall. These proteins appear to mediate "acid growth" responses of isolated walls and may catalyze plant cell wall extension by a novel biochemical mechanism.

This article has been cited by other articles:

				F. Kerff, A. Amoroso, R. Herman, E. Sauvage, S. Petrella, P. Filee, P. Charlier, B. Joris, A. Tabuchi, N. Nikolaidis, et al. Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization PNAS, November 4, 2008; 105(44): 16876 - 16881. [Abstract] [Full Text] [PDF]

				Q. Zhao, S. Yuan, X. Wang, Y. Zhang, H. Zhu, and C. Lu Restoration of Mature Etiolated Cucumber Hypocotyl Cell Wall Susceptibility to Expansin by Pretreatment with Fungal Pectinases and EGTA in Vitro Plant Physiology, August 1, 2008; 147(4): 1874 - 1885. [Abstract] [Full Text] [PDF]

				X. Ding, Y. Cao, L. Huang, J. Zhao, C. Xu, X. Li, and S. Wang Activation of the Indole-3-Acetic Acid-Amido Synthetase GH3-8 Suppresses Expansin Expression and Promotes Salicylate- and Jasmonate-Independent Basal Immunity in Rice PLANT CELL, January 1, 2008; 20(1): 228 - 240. [Abstract] [Full Text] [PDF]

				V. S. T. Van Sandt, D. Suslov, J.-P. Verbelen, and K. Vissenberg Xyloglucan Endotransglucosylase Activity Loosens a Plant Cell Wall Ann. Bot., December 1, 2007; 100(7): 1467 - 1473. [Abstract] [Full Text] [PDF]

				J. Zhu, S. Alvarez, E. L. Marsh, M. E. LeNoble, I.-J. Cho, M. Sivaguru, S. Chen, H. T. Nguyen, Y. Wu, D. P. Schachtman, et al. Cell Wall Proteome in the Maize Primary Root Elongation Zone. II. Region-Specific Changes in Water Soluble and Lightly Ionically Bound Proteins under Water Deficit Plant Physiology, December 1, 2007; 145(4): 1533 - 1548. [Abstract] [Full Text] [PDF]

				J. Xu, J. Tian, F. C. Belanger, and B. Huang Identification and characterization of an expansin gene AsEXP1 associated with heat tolerance in C3 Agrostis grass species J. Exp. Bot., October 10, 2007; (2007) erm229v1. [Abstract] [Full Text] [PDF]

				C. Evered, B. Majevadia, and D. S. Thompson Cell wall water content has a direct effect on extensibility in growing hypocotyls of sunflower (Helianthus annuus L.) J. Exp. Bot., September 26, 2007; (2007) erm183v1. [Abstract] [Full Text] [PDF]

				R. E. Carey and D. J. Cosgrove Portrait of the Expansin Superfamily in Physcomitrella patens: Comparisons with Angiosperm Expansins Ann. Bot., June 1, 2007; 99(6): 1131 - 1141. [Abstract] [Full Text] [PDF]

				E. R. Valdivia, J. Sampedro, J. C. Lamb, S. Chopra, and D. J. Cosgrove Recent Proliferation and Translocation of Pollen Group 1 Allergen Genes in the Maize Genome Plant Physiology, March 1, 2007; 143(3): 1269 - 1281. [Abstract] [Full Text] [PDF]

				K. Takahashi, S. Hirata, N. Kido, and K. Katou Wall-Yielding Properties of Cell Walls from Elongating Cucumber Hypocotyls in Relation to the Action of Expansin Plant Cell Physiol., November 1, 2006; 47(11): 1520 - 1529. [Abstract] [Full Text] [PDF]

				N. H. Yennawar, L.-C. Li, D. M. Dudzinski, A. Tabuchi, and D. J. Cosgrove Inaugural Article: Crystal structure and activities of EXPB1 (Zea m 1), a beta-expansin and group-1 pollen allergen from maize PNAS, October 3, 2006; 103(40): 14664 - 14671. [Abstract] [Full Text] [PDF]

				T. H. Davis Profile of Daniel J. Cosgrove PNAS, October 3, 2006; 103(40): 14661 - 14663. [Full Text] [PDF]

				A. Maggio, J.-K. Zhu, P. M. Hasegawa, and R. A. Bressan Osmogenetics: Aristotle to Arabidopsis PLANT CELL, July 1, 2006; 18(7): 1542 - 1557. [Full Text] [PDF]

				D Suslov and J-P Verbelen Cellulose orientation determines mechanical anisotropy in onion epidermis cell walls J. Exp. Bot., July 1, 2006; 57(10): 2183 - 2192. [Abstract] [Full Text] [PDF]

				P. Veronico, D. Giannino, M. T. Melillo, A. Leone, A. Reyes, M. W. Kennedy, and T. Bleve-Zacheo A Novel Lipoxygenase in Pea Roots. Its Function in Wounding and Biotic Stress Plant Physiology, July 1, 2006; 141(3): 1045 - 1055. [Abstract] [Full Text] [PDF]

				M. Kwasniewski and I. Szarejko Molecular Cloning and Characterization of beta-Expansin Gene Related to Root Hair Formation in Barley Plant Physiology, July 1, 2006; 141(3): 1149 - 1158. [Abstract] [Full Text] [PDF]

				O. Shoseyov, Z. Shani, and I. Levy Carbohydrate Binding Modules: Biochemical Properties and Novel Applications Microbiol. Mol. Biol. Rev., June 1, 2006; 70(2): 283 - 295. [Abstract] [Full Text] [PDF]

				C. A. Esmon, A. G. Tinsley, K. Ljung, G. Sandberg, L. B. Hearne, and E. Liscum A gradient of auxin and auxin-dependent transcription precedes tropic growth responses PNAS, January 3, 2006; 103(1): 236 - 241. [Abstract] [Full Text] [PDF]

				A. J. Fleming The co-ordination of cell division, differentiation and morphogenesis in the shoot apical meristem: a perspective J. Exp. Bot., January 1, 2006; 57(1): 25 - 32. [Abstract] [Full Text] [PDF]

				N. O'LOONEY and S. C. FRY Oxaziclomefone, a New Herbicide, Inhibits Wall Expansion in Maize Cell-cultures without Affecting Polysaccharide Biosynthesis, Xyloglucan Transglycosylation, Peroxidase Action or Apoplastic Ascorbate Oxidation Ann. Bot., November 1, 2005; 96(6): 1097 - 1107. [Abstract] [Full Text] [PDF]

				N. Ezaki, N. Kido, K. Takahashi, and K. Katou The Role of Wall Ca2+ in the Regulation of Wall Extensibility During the Acid-induced Extension of Soybean Hypocotyl Cell Walls Plant Cell Physiol., November 1, 2005; 46(11): 1831 - 1838. [Abstract] [Full Text] [PDF]

				D. S. Thompson How do cell walls regulate plant growth? J. Exp. Bot., September 1, 2005; 56(419): 2275 - 2285. [Abstract] [Full Text] [PDF]

				J. Nieuwland, R. Feron, B. A.H. Huisman, A. Fasolino, C. W. Hilbers, J. Derksen, and C. Mariani Lipid Transfer Proteins Enhance Cell Wall Extension in Tobacco PLANT CELL, July 1, 2005; 17(7): 2009 - 2019. [Abstract] [Full Text] [PDF]

				E. J. Belfield, B. Ruperti, J. A. Roberts, and S. McQueen-Mason Changes in expansin activity and gene expression during ethylene-promoted leaflet abscission in Sambucus nigra J. Exp. Bot., March 1, 2005; 56(413): 817 - 823. [Abstract] [Full Text] [PDF]

				M. Gray-Mitsumune, E. J. Mellerowicz, H. Abe, J. Schrader, A. Winzell, F. Sterky, K. Blomqvist, S. McQueen-Mason, T. T. Teeri, and B. Sundberg Expansins Abundant in Secondary Xylem Belong to Subgroup A of the {alpha}-Expansin Gene Family Plant Physiology, July 1, 2004; 135(3): 1552 - 1564. [Abstract] [Full Text] [PDF]

				C. X. WANG, L. WANG, and C. R. THOMAS Modelling the Mechanical Properties of Single Suspension-Cultured Tomato Cells Ann. Bot., April 1, 2004; 93(4): 443 - 453. [Abstract] [Full Text] [PDF]

				M. J. Pena, P. Ryden, M. Madson, A. C. Smith, and N. C. Carpita The Galactose Residues of Xyloglucan Are Essential to Maintain Mechanical Strength of the Primary Cell Walls in Arabidopsis during Growth Plant Physiology, January 1, 2004; 134(1): 443 - 451. [Abstract] [Full Text] [PDF]

				L.-C. Li, P. A. Bedinger, C. Volk, A. D. Jones, and D. J. Cosgrove Purification and Characterization of Four {beta}-Expansins (Zea m 1 Isoforms) from Maize Pollen Plant Physiology, August 1, 2003; 132(4): 2073 - 2085. [Abstract] [Full Text] [PDF]

				D. Choi, Y. Lee, H.-T. Cho, and H. Kende Regulation of Expansin Gene Expression Affects Growth and Development in Transgenic Rice Plants PLANT CELL, June 1, 2003; 15(6): 1386 - 1398. [Abstract] [Full Text]

				W. H. VRIEZEN, Z. ZHOU, and D. VAN DER STRAETEN Regulation of Submergence-induced Enhanced Shoot Elongation in Oryza sativa L. Ann. Bot., January 2, 2003; 91(2): 263 - 270. [Abstract] [Full Text] [PDF]

				K. Nishitani New Directions to Post-genomic Cell Wall Research Plant Cell Physiol., December 15, 2002; 43(12): 1397 - 1397. [Full Text] [PDF]

				D. J. Cosgrove, L. C. Li, H.-T. Cho, S. Hoffmann-Benning, R. C. Moore, and D. Blecker The Growing World of Expansins Plant Cell Physiol., December 15, 2002; 43(12): 1436 - 1444. [Abstract] [Full Text] [PDF]

				H.-T. Cho and D. J. Cosgrove Regulation of Root Hair Initiation and Expansin Gene Expression in Arabidopsis PLANT CELL, December 1, 2002; 14(12): 3237 - 3253. [Abstract] [Full Text] [PDF]

				Y. Lee and H. Kende Expression of alpha -Expansin and Expansin-Like Genes in Deepwater Rice Plant Physiology, November 1, 2002; 130(3): 1396 - 1405. [Abstract] [Full Text] [PDF]

				S. Pagant, A. Bichet, K. Sugimoto, O. Lerouxel, T. Desprez, M. McCann, P. Lerouge, S. Vernhettes, and H. Hofte KOBITO1 Encodes a Novel Plasma Membrane Protein Necessary for Normal Synthesis of Cellulose during Cell Expansion in Arabidopsis PLANT CELL, September 1, 2002; 14(9): 2001 - 2013. [Abstract] [Full Text] [PDF]

				A. J.M. Peeters, M. C.H. Cox, J. J. Benschop, R. A.M. Vreeburg, J. Bou, and L. A.C.J. Voesenek Submergence research using Rumex palustris as a model; looking back and going forward J. Exp. Bot., March 1, 2002; 53(368): 391 - 398. [Abstract] [Full Text] [PDF]

				F. Chen, H. Nonogaki, and K. J. Bradford A gibberellin-regulated xyloglucan endotransglycosylase gene is expressed in the endosperm cap during tomato seed germination J. Exp. Bot., February 1, 2002; 53(367): 215 - 223. [Abstract] [Full Text] [PDF]

				T. Kaku, A. Tabuchi, K. Wakabayashi, S. Kamisaka, and T. Hoson Action of Xyloglucan Hydrolase within the Native Cell Wall Architecture and Its Effect on Cell Wall Extensibility in Azuki Bean Epicotyls Plant Cell Physiol., January 1, 2002; 43(1): 21 - 26. [Abstract] [Full Text] [PDF]

				F. Chen, P. Dahal, and K. J. Bradford Two Tomato Expansin Genes Show Divergent Expression and Localization in Embryos during Seed Development and Germination Plant Physiology, November 1, 2001; 127(3): 928 - 936. [Abstract] [Full Text] [PDF]

				Y. Lee and H. Kende Expression of beta -Expansins Is Correlated with Internodal Elongation in Deepwater Rice Plant Physiology, October 1, 2001; 127(2): 645 - 654. [Abstract] [Full Text] [PDF]

				A. Okamoto-Nakazato, K. Takahashi, R. Katoh-Semba, and K. Katou Distribution of Yieldin, a Regulatory Protein of the Cell Wall Yield Threshold, in Etiolated Cowpea Seedlings Plant Cell Physiol., September 1, 2001; 42(9): 952 - 958. [Abstract] [Full Text] [PDF]

				S. Yuan, Y. Wu, and D. J. Cosgrove A Fungal Endoglucanase with Plant Cell Wall Extension Activity Plant Physiology, September 1, 2001; 127(1): 324 - 333. [Abstract] [Full Text] [PDF]

				E. P. Harrison, S. J. McQueen-Mason, and K. Manning Expression of six expansin genes in relation to extension activity in developing strawberry fruit J. Exp. Bot., July 1, 2001; 52(360): 1437 - 1446. [Abstract] [Full Text] [PDF]

				D.S. Thompson Extensiometric determination of the rheological properties of the epidermis of growing tomato fruit J. Exp. Bot., June 1, 2001; 52(359): 1291 - 1301. [Abstract] [Full Text] [PDF]

				Y. Wu, R. B. Meeley, and D. J. Cosgrove Analysis and Expression of the {alpha}-Expansin and {beta}-Expansin Gene Families in Maize Plant Physiology, May 1, 2001; 126(1): 222 - 232. [Abstract] [Full Text]

				B. P. Downes, C. R. Steinbaker, and D. N. Crowell Expression and Processing of a Hormonally Regulated {beta}-Expansin from Soybean Plant Physiology, May 1, 2001; 126(1): 244 - 252. [Abstract] [Full Text]

				T. A. Wagner and B. D. Kohorn Wall-Associated Kinases Are Expressed throughout Plant Development and Are Required for Cell Expansion PLANT CELL, February 1, 2001; 13(2): 303 - 318. [Abstract] [Full Text]

				D. J. Cosgrove Wall Structure and Wall Loosening. A Look Backwards and Forwards Plant Physiology, January 1, 2001; 125(1): 131 - 134. [Full Text]

				A. R. Taylor and S. M. Assmann Apparent Absence of a Redox Requirement for Blue Light Activation of Pump Current in Broad Bean Guard Cells Plant Physiology, January 1, 2001; 125(1): 329 - 338. [Abstract] [Full Text]

				N. Zhang and K. H. Hasenstein Distribution of Expansins in Graviresponding Maize Roots Plant Cell Physiol., December 1, 2000; 41(12): 1305 - 1312. [Abstract] [Full Text] [PDF]

				F. Chen and K. J. Bradford Expression of an Expansin Is Associated with Endosperm Weakening during Tomato Seed Germination Plant Physiology, November 1, 2000; 124(3): 1265 - 1274. [Abstract] [Full Text]

				F. Tardieu, M. Reymond, P. Hamard, C. Granier, and B. Muller Spatial distributions of expansion rate, cell division rate and cell size in maize leaves: a synthesis of the effects of soil water status, evaporative demand and temperature J. Exp. Bot., September 1, 2000; 51(350): 1505 - 1514. [Abstract] [Full Text] [PDF]

				Y. Wu and D. J. Cosgrove Adaptation of roots to low water potentials by changes in cell wall extensibility and cell wall proteins J. Exp. Bot., September 1, 2000; 51(350): 1543 - 1553. [Abstract] [Full Text] [PDF]

				R. C. O'Malley and D. G. Lynn Expansin Message Regulation in Parasitic Angiosperms: Marking Time in Development PLANT CELL, August 1, 2000; 12(8): 1455 - 1466. [Abstract] [Full Text]

				H. Nonogaki, O. H. Gee, and K. J. Bradford A Germination-Specific Endo-beta -Mannanase Gene Is Expressed in the Micropylar Endosperm Cap of Tomato Seeds Plant Physiology, August 1, 2000; 123(4): 1235 - 1246. [Abstract] [Full Text]

				D. Caderas, M. Muster, H. Vogler, T. Mandel, J. K.C. Rose, S. McQueen-Mason, and C. Kuhlemeier Limited Correlation between Expansin Gene Expression and Elongation Growth Rate Plant Physiology, August 1, 2000; 123(4): 1399 - 1414. [Abstract] [Full Text]

				J. K.C. Rose, D. J. Cosgrove, P. Albersheim, A. G. Darvill, and A. B. Bennett Detection of Expansin Proteins and Activity during Tomato Fruit Ontogeny Plant Physiology, August 1, 2000; 123(4): 1583 - 1592. [Abstract] [Full Text]

				K. Vissenberg, I. M. Martinez-Vilchez, J.-P. Verbelen, J. G. Miller, and S. C. Fry In Vivo Colocalization of Xyloglucan Endotransglycosylase Activity and Its Donor Substrate in the Elongation Zone of Arabidopsis Roots PLANT CELL, July 1, 2000; 12(7): 1229 - 1238. [Abstract] [Full Text]

				J. Burstin Differential expression of two barley XET-related genes during coleoptile growth J. Exp. Bot., May 1, 2000; 51(346): 847 - 852. [Abstract] [Full Text] [PDF]

				C. Catalá, J. K.C. Rose, and A. B. Bennett Auxin-Regulated Genes Encoding Cell Wall-Modifying Proteins Are Expressed during Early Tomato Fruit Growth Plant Physiology, February 1, 2000; 122(2): 527 - 534. [Abstract] [Full Text]

				P. M. Civello, A. L.T. Powell, A. Sabehat, and A. B. Bennett An Expansin Gene Expressed in Ripening Strawberry Fruit Plant Physiology, December 1, 1999; 121(4): 1273 - 1279. [Abstract] [Full Text]

				D. A. Brummell, M. H. Harpster, P. M. Civello, J. M. Palys, A. B. Bennett, and P. Dunsmuir Modification of Expansin Protein Abundance in Tomato Fruit Alters Softening and Cell Wall Polymer Metabolism during Ripening PLANT CELL, November 1, 1999; 11(11): 2203 - 2216. [Abstract] [Full Text]

				G.-T. Kim, H. Tsukaya, Y. Saito, and H. Uchimiya Changes in the shapes of leaves and flowers upon overexpression of cytochrome P450 in Arabidopsis PNAS, August 3, 1999; 96(16): 9433 - 9437. [Abstract] [Full Text] [PDF]

				K. W. Hutchison, P. B. Singer, S. McInnis, C. Diaz-Sala, and M. S. Greenwood Expansins Are Conserved in Conifers and Expressed in Hypocotyls in Response to Exogenous Auxin Plant Physiology, July 1, 1999; 120(3): 827 - 832. [Abstract] [Full Text]

				B. M. Link and D. J. Cosgrove Acid-Growth Response and alpha -Expansins in Suspension Cultures of Bright Yellow 2 Tobacco Plant Physiology, November 1, 1998; 118(3): 907 - 916. [Abstract] [Full Text]

				D. J. Cosgrove Cell Wall Loosening by Expansins Plant Physiology, October 1, 1998; 118(2): 333 - 339. [Full Text]

				D. Reinhardt, F. Wittwer, T. Mandel, and C. Kuhlemeier Localized Upregulation of a New Expansin Gene Predicts the Site of Leaf Formation in the Tomato Meristem PLANT CELL, September 1, 1998; 10(9): 1427 - 1438. [Abstract] [Full Text]

				G.-T. Kim, H. Tsukaya, and H. Uchimiya The ROTUNDIFOLIA3 gene of Arabidopsis thaliana encodes a new member of the cytochrome P-450 family that is required for the regulated polar elongation of leaf cells Genes & Dev., August 1, 1998; 12(15): 2381 - 2391. [Abstract] [Full Text]

				E. Shpigel, L. Roiz, R. Goren, and O. Shoseyov Bacterial Cellulose-Binding Domain Modulates in Vitro Elongation of Different Plant Cells Plant Physiology, August 1, 1998; 117(4): 1185 - 1194. [Abstract] [Full Text]

				D. J. Cosgrove, P. Bedinger, and D. M. Durachko Group I allergens of grass pollen as cell wall-loosening agents PNAS, June 10, 1997; 94(12): 6559 - 6564. [Abstract] [Full Text] [PDF]

				D. J. Cosgrove Creeping walls, softening fruit, and penetrating pollen tubes: The growing roles of expansins PNAS, May 27, 1997; 94(11): 5504 - 5505. [Full Text] [PDF]

				J. K. C. Rose, H. H. Lee, and A. B. Bennett Expression of a divergent expansin gene is fruit-specific and ripening-regulated PNAS, May 27, 1997; 94(11): 5955 - 5960. [Abstract] [Full Text] [PDF]

				H Wang, S K Lockwood, M F Hoeltzel, and J W Schiefelbein The ROOT HAIR DEFECTIVE3 gene encodes an evolutionarily conserved protein with GTP-binding motifs and is required for regulated cell enlargement in Arabidopsis. Genes & Dev., March 15, 1997; 11(6): 799 - 811. [Abstract] [PDF]

				J. Topping, V. May, P. Muskett, and K Lindsey Mutations in the HYDRA1 gene of Arabidopsis perturb cell shape and disrupt embryonic and seedling morphogenesis Development, January 11, 1997; 124(21): 4415 - 4424. [Abstract] [PDF]

				T Desnos, V Orbovic, C Bellini, J Kronenberger, M Caboche, J Traas, and H Hofte Procuste1 mutants identify two distinct genetic pathways controlling hypocotyl cell elongation, respectively in dark- and light-grown Arabidopsis seedlings Development, January 2, 1996; 122(2): 683 - 693. [Abstract] [PDF]

				W G Rerie, K A Feldmann, and M D Marks The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes & Dev., June 15, 1994; 8(12): 1388 - 1399. [Abstract] [PDF]

				R. Goldberg, M. Pierron, M. Bordenave, C. Breton, C. Morvan, and C. H. du Penhoat Control of Mung Bean Pectinmethylesterase Isoform Activities. INFLUENCE OF pH AND CARBOXYL GROUP DISTRIBUTION ALONG THE PECTIC CHAINS J. Biol. Chem., March 16, 2001; 276(12): 8841 - 8847. [Abstract] [Full Text] [PDF]

				H.-T. Cho and D. J. Cosgrove From the Cover: Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana PNAS, August 15, 2000; 97(17): 9783 - 9788. [Abstract] [Full Text] [PDF]

				S. Pien, J. Wyrzykowska, S. McQueen-Mason, C. Smart, and A. Fleming From the Cover: Local expression of expansin induces the entire process of leaf development and modifies leaf shape PNAS, September 25, 2001; 98(20): 11812 - 11817. [Abstract] [Full Text] [PDF]

				Y. Li, C. P. Darley, V. Ongaro, A. Fleming, O. Schipper, S. L. Baldauf, and S. J. McQueen-Mason Plant Expansins Are a Complex Multigene Family with an Ancient Evolutionary Origin Plant Physiology, March 1, 2002; 128(3): 854 - 864. [Abstract] [Full Text] [PDF]