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Planta

, Volume 241, Issue 2, pp 359–370 | Cite as

Fungal hemicellulose-degrading enzymes cause physical property changes concomitant with solubilization of cell wall polysaccharides

  • Machiko Takahashi
  • Ryoichi Yamamoto
  • Naoki Sakurai
  • Yuki Nakano
  • Takumi Takeda
Original Article

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.

Keywords

Xylanase 1,3-1,4-β-Glucanase Viscoelastic properties Hemicellulosic tethers Polysaccharide solubilization 

Notes

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.

Acknowledgments

This work was supported by Iwate Prefecture.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

425_2014_2176_MOESM1_ESM.pdf (389 kb)
Supplementary material 1 (PDF 388 kb)

References

  1. Carpita NC (1983) Hemicellulosic polymers of cell walls of Zea coleoptiles. Plant Physiol 72:515–521PubMedCentralPubMedCrossRefGoogle Scholar
  2. Carpita NC (1996) Structure and biogenesis of the cell walls of grasses. Annu Rev Plant Physiol Plant Mol Biol 47:445–476PubMedCrossRefGoogle Scholar
  3. 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 3:1–30PubMedCrossRefGoogle Scholar
  4. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861PubMedCrossRefGoogle Scholar
  5. 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 91–162Google Scholar
  6. 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 12:140–147PubMedCrossRefGoogle Scholar
  7. Fry SC (1989) Cellulases, hemicelluloses and auxin-stimulated growth: a possible relationship. Plant Physiol 75:532–536CrossRefGoogle Scholar
  8. Gibeaut DM, Pauly M, Bacic A, Fincher GB (2005) Changes in cell wall polysaccharides in developing barley (Hordeum vulgare) coleoptiles. Planta 221:729–738PubMedCrossRefGoogle Scholar
  9. Guillén D, Sánchez S, Rodriguez-Sanoja R (2010) Carbohydrate-binding domains: multiplicity of biological roles. Appl Microbiol Biotechbol 85:1241–1249CrossRefGoogle Scholar
  10. Hayashi T (1989) Xyloglucans in the primary cell wall. Annu Rev Plant Physiol Plant Mol Biol 40:139–168CrossRefGoogle Scholar
  11. Hayashi T, Wong YS, Maclachlan G (1984) Pea xyloglucan and cellulose. II. Hydrolysis by pea endo-1,4-β-glucanases. Plant Physiol 75:605–610PubMedCentralPubMedCrossRefGoogle Scholar
  12. 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 90:1353–1358PubMedCentralPubMedCrossRefGoogle Scholar
  13. Inouhe M, Nevins DJ (1991) Inhibition of auxin-induced cell elongation of maize coleoptiles by antibodies specific for cell wall glucanases. Plant Physiol 96:426–431PubMedCentralPubMedCrossRefGoogle Scholar
  14. 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 20:688–691PubMedCrossRefGoogle Scholar
  15. Kamata Y, Rector D, Kinsella JE (1988) Influence of temperature of measurement on creep phenomena in glycinin gels. J Food Sci 53:589–591CrossRefGoogle Scholar
  16. Kato Y, Nevins DJ (1985) A (1→3)-β-d-glucan isolated from Zea shoot cell wall preparations. Plant Physiol 78:20–24PubMedCentralPubMedCrossRefGoogle Scholar
  17. Labavitch JM, Lay PM (1974) Turnover of cell wall polysaccharides in elongating pea stem segments. Plant Physiol 53:669–673PubMedCentralPubMedCrossRefGoogle Scholar
  18. Miller M (1972) A new reaction for colorimetric determination of carbohydrates. Anal Biochem 47:273–279CrossRefGoogle Scholar
  19. 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 81:1008–1019PubMedCrossRefGoogle Scholar
  20. 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 33:1099–1106PubMedCrossRefGoogle Scholar
  21. 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 215:51–59PubMedCrossRefGoogle Scholar
  22. 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 20:1349–1357Google Scholar
  23. Scalbert A, Monties B, Lallemand JY, Guittet E, Rolando C (1985) Ether linkage between phenolic acids and lignin fractions from wheat straw. Phytochemistry 24:1359–1362CrossRefGoogle Scholar
  24. Sherwood RT, Vance CP (1990) Resistance to fungal penetration in Gramineae. Phytopathology 70:273–279CrossRefGoogle Scholar
  25. Shoseyov O, Shani Z, Levy I (2006) Carbohydrate binding modules: biochemical properties and novel applications. Microbiol Mol Biol Rev 70:283–295PubMedCentralPubMedCrossRefGoogle Scholar
  26. Tabuchi A, Li LC, Cosgrove DJ (2011) Matrix solubilization and cell wall weakening by β-expansin (group-1 allergen) from maize pollen. Plant J 68:546–559PubMedCrossRefGoogle Scholar
  27. Taiz L (1984) Plant cell expansion: regulation of cell wall mechanical properties. Annu Rev Plant Physiol 35:585–657CrossRefGoogle Scholar
  28. 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 76:6583–6590PubMedCentralPubMedCrossRefGoogle Scholar
  29. 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 288:13821–13830PubMedCentralPubMedCrossRefGoogle Scholar
  30. 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 99:9055–9060PubMedCentralPubMedCrossRefGoogle Scholar
  31. 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 139:413–420PubMedGoogle Scholar
  32. 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 88:1113–1123PubMedCrossRefGoogle Scholar
  33. 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 226:21–28CrossRefGoogle Scholar
  34. 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 3:207–225CrossRefGoogle Scholar
  35. 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 103:14664–14671PubMedCentralPubMedCrossRefGoogle Scholar
  36. Yuan S, Wu Y, Cosgrove DJ (2001) A fungal endoglucanase with plant cell wall extension activity. Plant Physiol 127:324–333PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Machiko Takahashi
    • 1
  • Ryoichi Yamamoto
    • 2
  • Naoki Sakurai
    • 3
  • Yuki Nakano
    • 1
  • Takumi Takeda
    • 1
  1. 1.Iwate Biotechnology Research CenterKitakamiJapan
  2. 2.Institute of Human and Environmental SciencesTezukayama UniversityNaraJapan
  3. 3.Graduate School of Biosphere ScienceHiroshima UniversityHigashihiroshimaJapan

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