1887

Abstract

Previously, we observed an acid-induced short-term wall extension in apical stipes during a 15 min period after a change from a neutral to an acidic pH. This acid-induced stipe wall extension was eliminated by heating and reconstituted by a snail expansin-like protein, although we failed to isolate any endogenous expansin-like protein from because of its limited 1 mm fast elongation region. In this study, we report that stipes possess a 9 mm fast elongation apical region, which is suitable as a model material for wall extension studies. The elongating apical stipe showed two phases of acid-induced wall extension, an initial quick short-term wall extension during the first 15 min and a slower, gradually decaying long-term wall extension over the subsequent 2 h. After heating or protein inactivation pretreatment, apical stipes lost the long-term wall extension, retaining a slower short-term wall extension, which was reconstituted by an expansin-like snail protein. In contrast, the non-elongating basal stipes showed only a weaker short-term wall extension. We propose that the long-term wall extension is a protein-mediated process involved in stipe elongation, whereas the short-term wall extension is a non-protein mediated process not involved in stipe elongation.

Funding
This study was supported by the:
  • National Natural Science Foundation of China (Award 31170028)
  • Priority Academic Development Program of Jiangsu Higher Education Institutions and the Scientific Innovation Research Program of Graduates at Nanjing Normal University (Award CXLX13-384)
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2014-09-01
2021-10-21
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References

  1. Bartnicki-García S. ( 1999). Glucans, walls, and morphogenesis: on the contributions of J. G. H. Wessels to the golden decades of fungal physiology and beyond. Fungal Genet Biol 27:119–127 [View Article][PubMed]
    [Google Scholar]
  2. Bowman S. M., Free S. J. ( 2006). The structure and synthesis of the fungal cell wall. Bioessays 28:799–808 [View Article][PubMed]
    [Google Scholar]
  3. Cabib E., Arroyo J. ( 2013). How carbohydrates sculpt cells: chemical control of morphogenesis in the yeast cell wall. Nat Rev Microbiol 11:648–655 [View Article][PubMed]
    [Google Scholar]
  4. Christensen M. J., Bennett R. J., Ansari H. A., Koga H., Johnson R. D., Bryan G. T., Simpson W. R., Koolaard J. P., Nickless E. M., Voisey C. R. ( 2008). Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genet Biol 45:84–93 [View Article][PubMed]
    [Google Scholar]
  5. Cosgrove D. J. , ( 1989). Characterization of long-term extension of isolated cell walls from growing cucumber hypocotyls. Planta 177:121–130 [View Article]
    [Google Scholar]
  6. Cosgrove D. J. ( 1993). Wall extensibility: its nature, measurement and relationship to plant cell growth. New Phytol 124:1–23 [View Article][PubMed]
    [Google Scholar]
  7. Cosgrove D. J. ( 2000). Loosening of plant cell walls by expansins. Nature 407:321–326 [View Article][PubMed]
    [Google Scholar]
  8. Cosgrove D. J. ( 2005). Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861 [View Article][PubMed]
    [Google Scholar]
  9. Cosgrove D. J., Bedinger P., Durachko D. M. ( 1997). Group I allergens of grass pollen as cell wall-loosening agents. Proc Natl Acad Sci U S A 94:6559–6564 [View Article][PubMed]
    [Google Scholar]
  10. Cox R. J., Niederpruem D. J. ( 1975). Differentiation in Coprinus lagopus. III. Expansion of excised fruit-bodies. Arch Microbiol 105:257–260 [View Article][PubMed]
    [Google Scholar]
  11. Craig G. D., Gull K., Wood D. A. ( 1977). Stipe elongation in Agaricus bisporus.. J Gen Microbiol 102:337–347 [View Article]
    [Google Scholar]
  12. Eilers F. I. ( 1974). Growth regulation in Coprinus radiatus.. Arch Microbiol 96:353–364 [View Article]
    [Google Scholar]
  13. Fang H. J., Zhang W. M., Niu X., Liu Z. H., Lu C. M., Wei H., Yuan S. ( 2014). Stipe wall extension of Flammulina velutipes could be induced by an expansin-like protein from Helix aspersa.. Fungal Biol 118:1–11 [View Article][PubMed]
    [Google Scholar]
  14. Gooday G. W. ( 1985). Elongation of the stipe of Coprinus cinereus. Developmental Biology of Higher Fungi311–332 Moore D., Casselton L. A., Wood D. A., Frankland J. C. Cambridge: Cambridge University Press;
    [Google Scholar]
  15. Gruen H. E. ( 1963). Endogenous growth regulation in carpophores of Agaricus bisporus.. Plant Physiol 38:652–666 [View Article][PubMed]
    [Google Scholar]
  16. Haindl E., Monzer J. ( 1994). Elongation growth and gravitropic curvature in the Flammulina velutipes (Agaricales) fruiting body. Exp Mycol 18:150–158 [View Article][PubMed]
    [Google Scholar]
  17. Hejazi R., Amiji M. ( 2003). Chitosan-based gastrointestinal delivery systems. J Control Release 89:151–165 [View Article][PubMed]
    [Google Scholar]
  18. Kamada T., Takemaru T. ( 1977). Stipe elongation during basidiocarp maturation in Coprinus macrorhizus: Mechanical properties of stipe cell wall. Plant Cell Physiol 18:831–840
    [Google Scholar]
  19. Kamada T., Hamada Y., Takemaru T. ( 1982). Autolysis in vitro of the stipe cell wall in Coprinus macrorhizus.. J Gen Microbiol 128:1041–1046
    [Google Scholar]
  20. Kamada T., Fujii T., Nakagawa T., Takemaru T. ( 1985). Changes in (1→3)-β-glucanase activities during stipe elongation in Coprinus cinereus.. Curr Microbiol 12:257–259 [View Article]
    [Google Scholar]
  21. Kamada T., Takemaru T., Prosser J. I., Gooday G. W. ( 1991). Right and left handed helicity of chitin microfibrils in stipe cells in Coprinus cinereus.. Protoplasma 165:64–70 [View Article]
    [Google Scholar]
  22. Li L. C., Bedinger P. A., Volk C., Jones A. D., Cosgrove D. J. ( 2003). Purification and characterization of four β-expansins (Zea m 1 isoforms) from maize pollen. Plant Physiol 132:2073–2085 [View Article][PubMed]
    [Google Scholar]
  23. Li Z. C., Durachko D. M., Cosgrove D. J. ( 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 [View Article]
    [Google Scholar]
  24. McQueen-Mason S. J., Durachko D. M., Cosgrove D. J. ( 1992). Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4:1425–1433 [View Article][PubMed]
    [Google Scholar]
  25. Mol P. C., Wessels J. G. H. ( 1990). Differences in wall structure between substrate hyphae and hyphae of fruit-body stipes in Agaricus bisporus.. Mycol Res 94:472–479 [View Article]
    [Google Scholar]
  26. Mol P. C., Vermeulen C. A., Wessels J. G. H. ( 1990). Diffuse extension of hyphae in stipes of Agaricus bisporus may be based on a unique wall structure. Mycol Res 94:480–488 [View Article]
    [Google Scholar]
  27. Money N. P., Ravishankar J. P. ( 2005). Biomechanics of stipe elongation in the basidiomycete Coprinopsis cinerea.. Mycol Res 109:627–634 [View Article][PubMed]
    [Google Scholar]
  28. Ramakrishnan C., Prasad N. ( 1972). Rigid-body refinement and conformation of -chitin. Biochim Biophys Acta 261:123–135 [View Article][PubMed]
    [Google Scholar]
  29. Ruiz-Herrera J., Ortiz-Castellanos L. ( 2010). Analysis of the phylogenetic relationships and evolution of the cell walls from yeasts and fungi. FEMS Yeast Res 10:225–243 [View Article][PubMed]
    [Google Scholar]
  30. Sampedro J., Cosgrove D. J. ( 2005). The expansin superfamily. Genome Biol 6:242 [View Article][PubMed]
    [Google Scholar]
  31. Shieh M. W., Cosgrove D. J. ( 1998). Expansins. J Plant Res 111:149–157 [View Article][PubMed]
    [Google Scholar]
  32. Shioya T., Nakamura H., Ishii N., Takahashi N., Sakamoto Y., Ozaki N., Kobayashi M., Okano K., Kamada T., Muraguchi H. ( 2013). The Coprinopsis cinerea septin Cc.Cdc3 is involved in stipe cell elongation. Fungal Genet Biol 58-59:80–90 [View Article][PubMed]
    [Google Scholar]
  33. Voisey C. R. ( 2010). Intercalary growth in hyphae of filamentous fungi. Fungal Biol Rev 24:123–131 [View Article]
    [Google Scholar]
  34. Wang T., Park Y. B., Caporini M. A., Rosay M., Zhong L., Cosgrove D. J., 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 [View Article][PubMed]
    [Google Scholar]
  35. Zhao Q. X., Yuan S., Wang X., Zhang Y. L., Zhu H., Lu C. M. ( 2008). Restoration of mature etiolated cucumber hypocotyl cell wall susceptibility to expansin by pretreatment with fungal pectinases and EGTA in vitro. Plant Physiol 147:1874–1885 [View Article][PubMed]
    [Google Scholar]
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