Abstract
Main conclusion
Physical properties of wheat coleoptile segments decreased after treatment with hemicellulose-degrading enzymes, indicating that hemicellulosic polysaccharides function to control the strength of primary cell walls.
Abstract
Changes in the physical properties of plant cell walls, a viscoelastic structure, are thought to be one of the growth-limiting factors for plants and one of the infection-affecting factors for fungi. To study the significance of hemicellulosic polysaccharides that form cross-bridges between cellulose microfibrils in controlling cell wall strength in monocot plants, the effects of hemicellulose degradation by recombinant Magnaporthe oryzae xylanase and 1,3-1,4-β-glucanase, and recombinant Aspergillus oryzae xyloglucanase on the physical properties and polysaccharide solubilization were investigated using wheat (Triticum aestivum L.) coleoptiles. Treatments with xylanase or 1,3-1,4-β-glucanase significantly decreased the viscosity and elasticity of wheat coleoptile segments. In addition, xyloglucanase treatment slightly decreased the viscoelasticity. Furthermore, 1,3-1,4-β-glucan polymer was solubilized during hydrolysis with xylanase and xyloglucanase, even though neither enzyme had hydrolytic activity towards 1,3-1,4-β-glucan. These results suggest that xylan and xyloglucan interact with 1,3-1,4-β-glucan and that the composites and hemicellulosic polysaccharides form inter-molecular bridges. Degradation of these bridges causes decreases in the physical properties, resulting in increased extensibility of the cell walls. These findings provide a testable model in which wheat coleoptile cell walls are loosened by the degradation of hemicellulosic polysaccharides and hemicellulose-degrading enzymes play a significant role in loosening the walls during fungal infection.
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References
Carpita NC (1983) Hemicellulosic polymers of cell walls of Zea coleoptiles. Plant Physiol 72:515–521
Carpita NC (1996) Structure and biogenesis of the cell walls of grasses. Annu Rev Plant Physiol Plant Mol Biol 47:445–476
Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30
Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861
Darvill AG, McNeil M, Albersheim P, Delmer DP (1980) The primary cell walls of higher plants. In: Tolbert NE (ed) The biochemistry of plants, vol 1. Academic Press, New York, pp 91–162
Fincher GB (2009) Exploring the evolution of (1,3;1,4)-β-d-glucans in plant cell walls: comparative genomics can help! Curr Opin Plant Biol 12:140–147
Fry SC (1989) Cellulases, hemicelluloses and auxin-stimulated growth: a possible relationship. Plant Physiol 75:532–536
Gibeaut DM, Pauly M, Bacic A, Fincher GB (2005) Changes in cell wall polysaccharides in developing barley (Hordeum vulgare) coleoptiles. Planta 221:729–738
Guillén D, Sánchez S, Rodriguez-Sanoja R (2010) Carbohydrate-binding domains: multiplicity of biological roles. Appl Microbiol Biotechbol 85:1241–1249
Hayashi T (1989) Xyloglucans in the primary cell wall. Annu Rev Plant Physiol Plant Mol Biol 40:139–168
Hayashi T, Wong YS, Maclachlan G (1984) Pea xyloglucan and cellulose. II. Hydrolysis by pea endo-1,4-β-glucanases. Plant Physiol 75:605–610
Hoson T, Nevins DJ (1989) β-d-Glucan antibodies inhibit anxin-induced cell elongation and changes in the cell wall of Zea coleoptile segments. Plant Physiol 90:1353–1358
Inouhe M, Nevins DJ (1991) Inhibition of auxin-induced cell elongation of maize coleoptiles by antibodies specific for cell wall glucanases. Plant Physiol 96:426–431
Ito J, Fujita Y, Ueda M, Fukuda H, Kondo A (2004) Improvement of cellulose-degrading ability of a yeast strain displaying Trichoderma reesei endoglucanase II by recombination of cellulose-binding domains. Biotechnol Prog 20:688–691
Kamata Y, Rector D, Kinsella JE (1988) Influence of temperature of measurement on creep phenomena in glycinin gels. J Food Sci 53:589–591
Kato Y, Nevins DJ (1985) A (1→3)-β-d-glucan isolated from Zea shoot cell wall preparations. Plant Physiol 78:20–24
Labavitch JM, Lay PM (1974) Turnover of cell wall polysaccharides in elongating pea stem segments. Plant Physiol 53:669–673
Miller M (1972) A new reaction for colorimetric determination of carbohydrates. Anal Biochem 47:273–279
Nguyen QB, Itoh K, Vu BV, Tosa Y, Nakayashiki H (2011) Simultaneous silencing of endo-β-1,4 xylanase genes reveals their roles in the virulence of Magnaporthe oryzae. Mol Microbiol 81:1008–1019
Park YW, Tominaga R, Sugiyama J, Furuta Y, Tanimoto E, Samejima M, Sakai F, Hayashi T (2003) Enhancement of growth by expression of poplar cellulose in Arabidopsis thaliana. Plant J 33:1099–1106
Roulin S, Buchala AJ, Fincher GB (2002) Induction of (1→3, 1→4)-β-d-glucan hydrolases in leaves of dark-incubated barley seedlings. Planta 215:51–59
Sakurai N, Nishitani K, Masuda Y (1979) Auxin-induced changes in the molecular weight of hemicellulosic polysaccharides of the Avena coleoptile cell wall. Plant Cell Physiol 20:1349–1357
Scalbert A, Monties B, Lallemand JY, Guittet E, Rolando C (1985) Ether linkage between phenolic acids and lignin fractions from wheat straw. Phytochemistry 24:1359–1362
Sherwood RT, Vance CP (1990) Resistance to fungal penetration in Gramineae. Phytopathology 70:273–279
Shoseyov O, Shani Z, Levy I (2006) Carbohydrate binding modules: biochemical properties and novel applications. Microbiol Mol Biol Rev 70:283–295
Tabuchi A, Li LC, Cosgrove DJ (2011) Matrix solubilization and cell wall weakening by β-expansin (group-1 allergen) from maize pollen. Plant J 68:546–559
Taiz L (1984) Plant cell expansion: regulation of cell wall mechanical properties. Annu Rev Plant Physiol 35:585–657
Takahashi M, Takahashi H, Nakano Y, Konishi T, Terauchi R, Takeda T (2010) Characterization of a cellobiohydrolase (MoCel6A) produced by Magnaporthe oryzae. Appl Environ Microbiol 76:6583–6590
Takahashi M, Yoshioka K, Imai T, Miyoshi Y, Nakano Y, Yoshida K, Furuta Y, Watanabe T, Sugiyama J, Takeda T (2013) Degradation and synthesis of β-glucans by a Magnaporthe oryzae endotransglucosylase, glucoside hydrolase 7 family. J Biol Chem 288:13821–13830
Takeda T, Furuta Y, Awano T, Mizuno K, Mitsuishi Y, Hayashi T (2002) Suppression and acceleration of cell elongation by integration of xyloglucans in pea stem segments. Proc Natl Acad Sci USA 99:9055–9060
Takeda H, Sugahara T, Kotake T, Nakagawa N, Sakurai N (2010) Sugar treatment inhibits IAA-induced expression of endo-1,3:1,4-β-glucanase EI transcripts in barley coleoptile segments. Physiol Plant 139:413–420
Takeda T, Takahashi M, Nakanishi-Masuno T, Nakano Y, Saitoh H, Hirabuchi A, Fujisawa S, Terauchi R (2010) Characterization of endo-1,3-1,4-β-glucanases in GH family 12 from Magnaporthe oryzae. Appl Microbiol Biotechnol 88:1113–1123
Tanimoto E, Fujii S, Yamamoto R, Inanaga S (2000) Measurement of viscoelastic properties of root cell walls affected by low pH in lateral roots of Pisum sativum L. Plant Soil 226:21–28
Woodward JR, Fincher GB, Stone BA (1983) Water-soluble (1→3), (1→4)-β-d-glucans from barley (Hordeum vulgare) endosperm II. Fine structure. Carbohydr Polym 3:207–225
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
Yuan S, Wu Y, Cosgrove DJ (2001) A fungal endoglucanase with plant cell wall extension activity. Plant Physiol 127:324–333
Author contribution
M.T., Y. N. and T.T. performed research; R. Y. and N. S. analyzed data; T.T. designed research; T.T. wrote the manuscript. All authors read and approved the manuscript.
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This work was supported by Iwate Prefecture.
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The authors declare that they have no conflict of interest.
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Takahashi, M., Yamamoto, R., Sakurai, N. et al. Fungal hemicellulose-degrading enzymes cause physical property changes concomitant with solubilization of cell wall polysaccharides. Planta 241, 359–370 (2015). https://doi.org/10.1007/s00425-014-2176-1
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DOI: https://doi.org/10.1007/s00425-014-2176-1