Advertisement

Journal of Plant Research

, Volume 126, Issue 6, pp 811–821 | Cite as

Chitosan and a fungal elicitor inhibit tracheary element differentiation and promote accumulation of stress lignin-like substance in Zinnia elegans xylogenic culture

  • Chisato Takeuchi
  • Kouji Nagatani
  • Yasushi Sato
Regular Paper

Abstract

We investigated the effect of elicitors on xylem differentiation and lignification using a Zinnia elegans xylogenic culture system. Water-soluble chitosan and a fungal elicitor derived from Botrytis cinerea were used as elicitors. Elicitor addition at the start of culturing inhibited tracheary element (TE) differentiation in a concentration-dependent manner, and 30 μg mL−1 of chitosan or 16.7 μg mL−1 of the fungal elicitor strikingly inhibited TE differentiation and lignification. Addition of chitosan (at 50 μg mL−1) or the fungal elicitor (at 16.7 μg mL−1) during the culturing period also inhibited TE differentiation without inhibiting cell division, except for immature TEs undergoing secondary wall thickening. Elicitor addition after immature TE appearance also caused the accumulation of an extracellular lignin-like substance. It appears that elicitor addition at the start of culturing inhibits the process by which dedifferentiated cells differentiate into xylem cell precursors. Elicitor addition during culturing also appears to inhibit the transition from xylem cell precursors to immature TEs, and induces xylem cell precursors or xylem parenchyma cells to produce an extracellular stress lignin-like substance.

Keywords

Botrytis cinerea Chitosan Fungal elicitor Stress lignin Tracheary element differentiation Zinnia elegans 

Abbreviations

MAMP

Microbe-associated molecular pattern

TE

Tracheary element

Notes

Acknowledgments

This work was supported in part by project grants to Y. S from Ehime University, Japan (Rudimentary Research Support) and from the Faculty of Science, Ehime University (Research Support).

Supplementary material

10265_2013_568_MOESM1_ESM.tif (4.2 mb)
Fig. S1 The method developed for measuring lignified areas. A 120-h culture with fungal elicitor addition at 72 h was subjected to the analysis with Image J. a Original RGB image. b G image of split RGB image. c The image with subtracted background. d The image with threshold adjusted to 0-223, TE and the extracellular lignin-like substance separated by a white line, and non-lignified particles removed. e Analysis of particle area. f Total of the area of lignified TEs or extracellular lignin-like substances (TIFF 4318 kb)
10265_2013_568_MOESM2_ESM.doc (28 kb)
Fig. S2 Macro program of Image J (version 1.45s) used for measuring lignified area.//, comment line; *, these parameters were adjusted for this research (DOC 28 kb)

References

  1. Bruce RJ, West CA (1989) Elicitation of lignin biosynthesis and isoperoxidase activity by pectic fragments in suspension cultures of castor bean. Plant Physiol 91:889–897PubMedCrossRefGoogle Scholar
  2. Campbell MM, Ellis BE (1992) Fungal elicitor-mediated responses in pine cell cultures : III. Purification and characterization of phenylalanine ammonia-lyase. Plant Physiol 98:62–70PubMedCrossRefGoogle Scholar
  3. Cantu DL, Greve LC, Labavitch JM, Ann LT, Powell ALT (2009) Characterization of the cell wall of the ubiquitous plant pathogen Botrytis cinerea. Mycol Res 113:1396–1403PubMedCrossRefGoogle Scholar
  4. Chen GC, Johnson BR (1983) Improved colorimetric determination of cell wall chitin in wood decay fungi. Appl Environ Microbiol 46:13–16PubMedGoogle Scholar
  5. de Wit PJGM (2007) How plants recognize pathogens and defend themselves. Cell Mol Life Sci 64:2726–2732PubMedCrossRefGoogle Scholar
  6. Develey-Rivere M-P, Galiana E (2007) Resistance to pathogens and host developmental stage: a multifaceted relationship within the plant kingdom. New Phytol 175:405–416CrossRefGoogle Scholar
  7. Fukuda H (2004) Signals that control plant vascular cell differentiation. Nat Rev Mol Cell Biol 5:379–391PubMedCrossRefGoogle Scholar
  8. Fukuda H, Komamine A (1980) Establishment of an experimental system for the study of tracheary element differentiation from single cells isolated from the mesophyll of Zinnia elegans. Plant Physiol 65:57–60PubMedCrossRefGoogle Scholar
  9. Fukuda H, Komamine A (1982) Lignin synthesis and its related enzymes as markers of tracheary-element differentiation in single cells isolated from the mesophyll of Zinnia elegans. Planta 155:423–430CrossRefGoogle Scholar
  10. Hano C, Addi M, Bensaddek L, Cronier D, Baltora-Rosset S, Doussot J, Maury S, Mesnard F, Chabbert B, Hawkins S, Laine E, Lamblin F (2006) Differential accumulation of monolignol-derived compounds in elicited flax (Linum usitatissimum) cell suspension cultures. Planta 223:975–989PubMedCrossRefGoogle Scholar
  11. Hosokawa M, Suzuki S, Umezawa T, Sato Y (2001) Progress of lignification mediated by intercellular transportation of monolignols during tracheary element differentiation of isolated Zinnia mesophyll cells. Plant Cell Physiol 42:959–968PubMedCrossRefGoogle Scholar
  12. Ito Y, Tokunaga N, Sato Y, Fukuda H (2004) Transfer of phenylpropanoids via the medium between xylem cells in Zinnia xylogenic culture. Plant Biotechnol 21:205–213CrossRefGoogle Scholar
  13. Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S, Dohmae N, Fukuda H (2006) Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313:842–845PubMedCrossRefGoogle Scholar
  14. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, Minami E, Shibuya N (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci USA 103:11086–11091PubMedCrossRefGoogle Scholar
  15. Kawaguchi Y, Nishiuchi T, Kodama H, Nakano T, Nishimura K, Shimamura K, Yamaguchi K, Kuchitsu K, Shinshi H, Suzuki K (2012) Fungal elicitor-induced retardation and its restoration of root growth in tobacco seedlings. Plant Growth Regul 66:59–68CrossRefGoogle Scholar
  16. Lange BM, Lapierre C, Sandermann H Jr (1995) Elicitor-induced spruce stress lignin (structural similarity to early developmental lignins). Plant Physol 108:1277–1287Google Scholar
  17. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysMd receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104:19613–19618PubMedCrossRefGoogle Scholar
  18. Motose H, Sugiyama M, Fukuda H (2001) Cell-cell interactions during vascular development. J Plant Res 114:473–481CrossRefGoogle Scholar
  19. Moura JCMS, Bonine CAV, Viana JOF, Dornelas MC, Mazzafera P (2010) Abiotic and biotic stresses and changes in the lignin content and composition in plants. J Integr Plant Biol 52:360–376PubMedCrossRefGoogle Scholar
  20. Naoumkina MA, Zhao Q, Gallego-Giraldo L, Dai X, Zhao PX, Dixon RA (2010) Genome-wide analysis of phenylpropanoid defence pathways. Mol Plant Pathol 11:829–846Google Scholar
  21. Oelofse D, Dubery IA (1996) Induction of defense responses in cultured tobacco cells by elicitors from Phytophthora nicotianae. Int J Biochem Cell Biol 28:295–301PubMedCrossRefGoogle Scholar
  22. Parker JE, Hahlbrock K, Scheel D (1988) Different cell-wall components from Phytophthora megasperma f. sp. glycinea elicit phytoalexin production in soybean and parsley. Planta 176:75–82CrossRefGoogle Scholar
  23. Rabea EI, Badawy ME-T, Stevens CV, Smagghe G, Steurbaut W (2003) Chitosan as antimicrobial agent: applications and mode of action. Biomacromolecules 4:1457–1465PubMedCrossRefGoogle Scholar
  24. Rasband WS (1997–2013) ImageJ, U. S. National Institutes of Health, Bethesda, Maryland. http://rsb.info.nih.gov/ij/
  25. Ron M, Avni A (2004) The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16:1604–1615PubMedCrossRefGoogle Scholar
  26. Sato Y, Watanabe T, Komamine A, Hibino T, Shibata D, Sugiyama M, Fukuda H (1997) Changes in the activity and mRNA of cinnamyl alcohol dehydrogenase during tracheary element differentiation in zinnia. Plant Physiol 113:425–430PubMedCrossRefGoogle Scholar
  27. Sato Y, Demura T, Yamawaki K, Inoue Y, Sato S, Sugiyama M, Fukuda H (2006) Isolation and characterization of a novel peroxidase gene ZPO-C whose expression and function are closely associated with lignification during tracheary element differentiation. Plant Cell Physiol 47:493–503PubMedCrossRefGoogle Scholar
  28. Sato Y, Yajima Y, Tokunaga N, Whetten R (2011) Comparison between tracheary element lignin formation and extracellular lignin-like substance formation during the culture of isolated Zinnia elegans mesophyll cells. Biologia 66:88–95CrossRefGoogle Scholar
  29. Sharp JK, Valent B, Albersheim P (1984) Purification and partial characterization of β-glucan fragment that elicits phytoalexin accumulation in soybean. J Biol Chem 259:11312–11320PubMedGoogle Scholar
  30. Siegel SM (1953) On the biosynthesis of lignin. Physiol Plant 6:134–139CrossRefGoogle Scholar
  31. Soylu S (2006) Accumulation of cell-wall bound phenolic compounds and hytoalexin in Arabidopsis thaliana leaves following inoculation with pathovars of Pseudomonas syringae. Plant Sci 170:942–952CrossRefGoogle Scholar
  32. Street PFS, Robb J, Ellis BE (1986) Secretion of vascular coating components by xylem parenchyma cells of tomatoes infected with Verticillium albo-atrum. Protoplasma 132:1–11CrossRefGoogle Scholar
  33. Suzuki K, Fukuda Y, Shinsh H (1995) Studies on elicitor signal transduction leading to differential expression of defense genes in cultured tobacco cells. Plant Cell Physiol 36:281–289Google Scholar
  34. Suzuki K, Nishiuchi T, Nakayama Y, Ito M, Shinshi H (2006) Elicitor-induced down-regulation of cell cycle-related genes in tobacco cells. Plant Cell Environ 29:183–191PubMedCrossRefGoogle Scholar
  35. Tokunaga N, Sakakibara N, Umezawa T, Ito Y, Fukuda H, Sato Y (2005) Involvement of extracellular dilignols in lignification during tracheary element differentiation of isolated Zinnia mesophyll cells. Plant Cell Physiol 46:224–232PubMedCrossRefGoogle Scholar
  36. Tokunaga N, Utimura N, Sato Y (2006) Involvement of gibberellin in tracheary element differentiation and lignification in Zinnia elegans xylogenic culture. Protoplasma 228:179–187PubMedCrossRefGoogle Scholar
  37. Tokunaga N, Kaneta T, Sato S, Sato Y (2009) Analysis of expression profiles of three peroxidase genes associated with lignification in Arabidopsis thaliana. Physiol Plant 136:237–249PubMedCrossRefGoogle Scholar
  38. Yamaguchi T, Yamada A, Hong N, Ogawa T, Ishii T, Shibuya N (2000) Differences in the recognition of glucan elicitor signals between rice and soybean: β-glucan fragments from the rice blast disease fungus Pyricularia oryzae that elicit phytoalexin biosynthesis in suspension-cultured rice cells. Plant Cell 12:817–826PubMedGoogle Scholar
  39. Yang Y, Shah J, Klessig DF (1997) Signal perception and transduction in plant defense responses. Genes Dev 11:1621–1639PubMedCrossRefGoogle Scholar
  40. Zhao S, Qi X (2008) Signaling in plant disease resistance and symbiosis. J Int Plant Biol 50:799–807CrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2013

Authors and Affiliations

  • Chisato Takeuchi
    • 1
  • Kouji Nagatani
    • 1
  • Yasushi Sato
    • 2
  1. 1.Department of Biology, Faculty of ScienceEhime UniversityMatsuyamaJapan
  2. 2.Biology and Environmental Science, Graduate School of ScienceEhime UniversityMatsuyamaJapan

Personalised recommendations