Skip to main content
SpringerLink
Log in

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

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

MAMP:

Microbe-associated molecular pattern

TE:

Tracheary element

References

  • Bruce RJ, West CA (1989) Elicitation of lignin biosynthesis and isoperoxidase activity by pectic fragments in suspension cultures of castor bean. Plant Physiol 91:889–897

    Article  PubMed  CAS  Google Scholar 

  • Campbell MM, Ellis BE (1992) Fungal elicitor-mediated responses in pine cell cultures : III. Purification and characterization of phenylalanine ammonia-lyase. Plant Physiol 98:62–70

    Article  PubMed  CAS  Google Scholar 

  • 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 113:1396–1403

    Article  PubMed  CAS  Google Scholar 

  • Chen GC, Johnson BR (1983) Improved colorimetric determination of cell wall chitin in wood decay fungi. Appl Environ Microbiol 46:13–16

    PubMed  CAS  Google Scholar 

  • de Wit PJGM (2007) How plants recognize pathogens and defend themselves. Cell Mol Life Sci 64:2726–2732

    Article  PubMed  Google Scholar 

  • Develey-Rivere M-P, Galiana E (2007) Resistance to pathogens and host developmental stage: a multifaceted relationship within the plant kingdom. New Phytol 175:405–416

    Article  Google Scholar 

  • Fukuda H (2004) Signals that control plant vascular cell differentiation. Nat Rev Mol Cell Biol 5:379–391

    Article  PubMed  CAS  Google Scholar 

  • 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 65:57–60

    Article  PubMed  CAS  Google Scholar 

  • 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 155:423–430

    Article  CAS  Google Scholar 

  • 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 223:975–989

    Article  PubMed  CAS  Google Scholar 

  • 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 42:959–968

    Article  PubMed  CAS  Google Scholar 

  • Ito Y, Tokunaga N, Sato Y, Fukuda H (2004) Transfer of phenylpropanoids via the medium between xylem cells in Zinnia xylogenic culture. Plant Biotechnol 21:205–213

    Article  CAS  Google Scholar 

  • 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 313:842–845

    Article  PubMed  CAS  Google Scholar 

  • 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 103:11086–11091

    Article  PubMed  CAS  Google Scholar 

  • 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 66:59–68

    Article  CAS  Google Scholar 

  • Lange BM, Lapierre C, Sandermann H Jr (1995) Elicitor-induced spruce stress lignin (structural similarity to early developmental lignins). Plant Physol 108:1277–1287

    CAS  Google Scholar 

  • 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 104:19613–19618

    Article  PubMed  CAS  Google Scholar 

  • Motose H, Sugiyama M, Fukuda H (2001) Cell-cell interactions during vascular development. J Plant Res 114:473–481

    Article  Google Scholar 

  • 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 52:360–376

    Article  PubMed  CAS  Google Scholar 

  • Naoumkina MA, Zhao Q, Gallego-Giraldo L, Dai X, Zhao PX, Dixon RA (2010) Genome-wide analysis of phenylpropanoid defence pathways. Mol Plant Pathol 11:829–846

    Google Scholar 

  • Oelofse D, Dubery IA (1996) Induction of defense responses in cultured tobacco cells by elicitors from Phytophthora nicotianae. Int J Biochem Cell Biol 28:295–301

    Article  PubMed  CAS  Google Scholar 

  • 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 176:75–82

    Article  CAS  Google Scholar 

  • Rabea EI, Badawy ME-T, Stevens CV, Smagghe G, Steurbaut W (2003) Chitosan as antimicrobial agent: applications and mode of action. Biomacromolecules 4:1457–1465

    Article  PubMed  CAS  Google Scholar 

  • Rasband WS (1997–2013) ImageJ, U. S. National Institutes of Health, Bethesda, Maryland. http://rsb.info.nih.gov/ij/

  • 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 16:1604–1615

    Article  PubMed  CAS  Google Scholar 

  • 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 113:425–430

    Article  PubMed  CAS  Google Scholar 

  • 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 47:493–503

    Article  PubMed  CAS  Google Scholar 

  • 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 66:88–95

    Article  CAS  Google Scholar 

  • Sharp JK, Valent B, Albersheim P (1984) Purification and partial characterization of β-glucan fragment that elicits phytoalexin accumulation in soybean. J Biol Chem 259:11312–11320

    PubMed  CAS  Google Scholar 

  • Siegel SM (1953) On the biosynthesis of lignin. Physiol Plant 6:134–139

    Article  CAS  Google Scholar 

  • 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 170:942–952

    Article  CAS  Google Scholar 

  • Street PFS, Robb J, Ellis BE (1986) Secretion of vascular coating components by xylem parenchyma cells of tomatoes infected with Verticillium albo-atrum. Protoplasma 132:1–11

    Article  Google Scholar 

  • 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 36:281–289

    CAS  Google Scholar 

  • 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 29:183–191

    Article  PubMed  CAS  Google Scholar 

  • 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 46:224–232

    Article  PubMed  CAS  Google Scholar 

  • Tokunaga N, Utimura N, Sato Y (2006) Involvement of gibberellin in tracheary element differentiation and lignification in Zinnia elegans xylogenic culture. Protoplasma 228:179–187

    Article  PubMed  CAS  Google Scholar 

  • 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 136:237–249

    Article  PubMed  CAS  Google Scholar 

  • 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 12:817–826

    PubMed  CAS  Google Scholar 

  • Yang Y, Shah J, Klessig DF (1997) Signal perception and transduction in plant defense responses. Genes Dev 11:1621–1639

    Article  PubMed  CAS  Google Scholar 

  • Zhao S, Qi X (2008) Signaling in plant disease resistance and symbiosis. J Int Plant Biol 50:799–807

    Article  CAS  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Science, Ehime University, Matsuyama, 790-8577, Japan

    Chisato Takeuchi & Kouji Nagatani

  2. Biology and Environmental Science, Graduate School of Science, Ehime University, Matsuyama, 790-8577, Japan

    Yasushi Sato

Authors
  1. Chisato Takeuchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kouji Nagatani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yasushi Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yasushi Sato.

Additional information

C. Takeuchi and K. Nagatani contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10265_2013_568_MOESM1_ESM.tif

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

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)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Takeuchi, C., Nagatani, K. & Sato, Y. Chitosan and a fungal elicitor inhibit tracheary element differentiation and promote accumulation of stress lignin-like substance in Zinnia elegans xylogenic culture. J Plant Res 126, 811–821 (2013). https://doi.org/10.1007/s10265-013-0568-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-013-0568-0

Keywords

Search

Navigation