Planta

, Volume 218, Issue 4, pp 673–681 | Cite as

A xylogalacturonan epitope is specifically associated with plant cell detachment

  • William G. T. Willats
  • Lesley McCartney
  • Clare G. Steele-King
  • Susan E. Marcus
  • Andrew Mort
  • Miranda Huisman
  • Gert-Jan van Alebeek
  • Henk A. Schols
  • Alphons G. J. Voragen
  • Angélique Le Goff
  • Estelle Bonnin
  • Jean-François Thibault
  • J. Paul Knox
Original Article

Abstract

A monoclonal antibody (LM8) was generated with specificity for xyloglacturonan (XGA) isolated from pea (Pisum sativum L.) testae. Characterization of the LM8 epitope indicates that it is a region of XGA that is highly substituted with xylose. Immunocytochemical analysis indicates that this epitope is restricted to loosely attached inner parenchyma cells at the inner face of the pea testa and does not occur in other cells of the testa. Elsewhere in the pea seedling, the LM8 epitope was found only in association with root cap cell development at the root apex. Furthermore, the LM8 epitope is specifically associated with root cap cells in a range of angiosperm species. In embryogenic carrot suspension cell cultures the epitope is abundant at the surface of cell walls of loosely attached cells in both induced and non-induced cultures. The LM8 epitope is the first cell wall epitope to be identified that is specifically associated with a plant cell separation process that results in complete cell detachment.

Keywords

Cell wall Pectin (monoclonal antibody) Plant cell adhesion Plant cell detachment Xylogalacturonan 

Abbreviations

DAA

Days after anthesis

2,4-D

2,4-Dichlorophenoxyacetic acid

ELISA

Enzyme-linked immunosorbent assay

GalA

Galacturonic acid

HGA

Homogalacturonan

HPAEC

High-performance anion-exchange chromatography

HPSEC

High-performance size-exclusion chromatography

RG-I

Rhamnogalacturonan-I

RG-II

Rhamnogalacturonan-II

XGA

Xylogalacturonan

References

  1. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815PubMedGoogle Scholar
  2. Bazin H (1982) Production of rat monoclonal antibodies with the LOU rat non-secreting IR983F myeloma cell line. Protein Biol Fluids 29:615–618Google Scholar
  3. Beldman G, van den Broek LAM, Schols HA, Searle-van Leeuwen MJF, van Laere KMJ, Voragen AGJ (1996) An exogalacturonase from Aspergillus aculeatus able to degrade xylogalacturonan. Biotechnol Lett 18:707–712Google Scholar
  4. Bouveng HO (1965) Polysaccharides in pollen. Acta Chim Scand 19:953–963Google Scholar
  5. Huisman MM, Fransen CT, Kamerling JP, Vliegenthart JF, Schols HA, Voragen AG (2001) The CDTA-soluble pectic substances from soybean meal are composed of rhamnogalacturonan and xylogalacturonan but not homogalacturonan. Biopolymers 58:279–94CrossRefPubMedGoogle Scholar
  6. Iwai H, Ishii T, Satoh S (2001) Absence of arabinan in the side chains of the pectic polysaccharides strongly associated with cell walls of Nicotiana plumbaginifolia non-organogenic callus with loosely attached constituent cells. Planta 213:907–915PubMedGoogle Scholar
  7. Iwai H, Masaoka N, Ishii T, Satoh S (2002) A pectin glucuronyltransferase gene is essential for intercellular attachment in the plant meristem. Proc Natl Acad Sci USA 99:16319–16324CrossRefPubMedGoogle Scholar
  8. Jarvis MC, Briggs SPH, Knox JP (2003) Intercellular adhesion and cell separation in plants. Plant Cell Environ 26:977–989CrossRefGoogle Scholar
  9. Jones L, Seymour GB, Knox JP (1997) Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1→4)-β-d-galactan. Plant Physiol 113:1405–1412Google Scholar
  10. Kikuchi A, Edashige Y, Ishii T, Satoh S (1996) A xylogalacturonan whose level is dependent on the size of cell clusters is present in the pectin from cultured carrot cells. Planta 200:369–372Google Scholar
  11. Knox JP (1997) The use of antibodies to study the architecture and developmental regulation of plant cell walls. Int Rev Cytol 171:79–120PubMedGoogle Scholar
  12. Le Goff A, Renard CMGC, Bonnin E, Thibault J-F (2001) Extraction, purification and chemical characterisation of xylogalacturonan from pea hulls. Carbohydr Polym 45:325–334CrossRefGoogle Scholar
  13. Matsuura Y (1984) Chemical structure of pectic polysaccharide of kidney beans. Nippon Nogei Kagaku Kaishi 58:253–259Google Scholar
  14. Matsuura Y, Hatanaka C (1988) Isolation and characterisation of a xylose-rich pectic polysaccharide from Japanese radish. Agric Biol Chem 52:3215–3216Google Scholar
  15. McCartney L, Knox JP (2002) Regulation of pectic polysaccharide domains in relation to cell development and cell properties in the pea testa. J Exp Bot 53:707–713CrossRefPubMedGoogle Scholar
  16. McCartney L, Ormerod AP, Gidley MJ, Knox JP (2000) Temporal and spatial regulation of pectic (1→4)-β-d-galactan in cell walls of developing pea cotyledons: implications for mechanical properties. Plant J 22:105–113PubMedGoogle Scholar
  17. Nakamura A, Furuta H, Maeda H, Takao T, Nagamatsu Y (2002) Analysis of the molecular construction of xylogalacturonan isolated from soluble soybean polysaccharides. Biosci Biotechnol Biochem 66:1155–1158CrossRefPubMedGoogle Scholar
  18. Orfila C, Knox JP (2000) Spatial regulation of pectic polysaccharides in relation to pit fields in cell walls of tomato fruit pericarp. Plant Physiol 122:775–781PubMedGoogle Scholar
  19. Orfila C, Seymour GB, Willats WGT, Huxham IM, Jarvis MC, Dover CJ, Thompson AJ, Knox JP (2001) Altered middle lamella homogalacturonan and disrupted deposition of (1→5)-α-l-arabinan in the pericarp of Cnr, a ripening mutant of tomato. Plant Physiol 126:210–221PubMedGoogle Scholar
  20. Redgwell RJ, Hansen CE (2000) Isolation and characterisation of cell wall polysaccharides from cocoa (Theobroma cacao L.) beans. Planta 210:823–830CrossRefPubMedGoogle Scholar
  21. Renard CMGC, Weightman RM, Thibault JF (1997) The xylose-rich pectins from pea hulls. Int J Biol Macromol 21:155–162CrossRefPubMedGoogle Scholar
  22. Ridley BL, O’Neill MA, Mohnen D (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57:929–967PubMedGoogle Scholar
  23. Roberts JA, Elliot KA, Gonzalez-Carranza ZH (2002) Abscission, dehiscence and other cell separation processes. Annu Rev Plant Biol 53:131–58Google Scholar
  24. Ros JM, Schols HA, Voragen AGJ (1998) Lemon albedo cell walls contain distinct populations of pectic hairy regions. Carbohydr Polym 37:159–166CrossRefGoogle Scholar
  25. Schols HA, Bakx EJ, Schipper D, Voragen AGJ (1995) A xylogalacturonan subunit present in the modified hairy regions of apple pectin. Carbohydr Res 279:265–279CrossRefGoogle Scholar
  26. Thompson HJM, Knox JP (1998) Stage-specific responses of embryogenic carrot cell suspension cultures to arabinogalactan protein-binding β-glucosyl Yariv reagent. Planta 205:32–38CrossRefGoogle Scholar
  27. van der Vlugt-Bergmans CJB, Meeuwsen PJA, Voragen AGJ, van Ooyen AJJ (2000) Endo-xylogalacturonan hydrolase, a novel pectinolytic enzyme. Appl Environ Microbiol 66:36–41PubMedGoogle Scholar
  28. Wen F, Zhu Y, Hawes MC (1999) Effect of pectin methylesterase gene expression on pea root development. Plant Cell 11:1129–1140Google Scholar
  29. Willats WGT, Marcus SE, Knox JP (1998) Generation of a monoclonal antibody specific to (1→5)-α-l-arabinan. Carbohydr Res 308:149–152PubMedGoogle Scholar
  30. Willats WGT, Steele-King CG, Marcus SE, Knox JP (1999) Side chains of pectic polysaccharides are regulated in relation to cell proliferation and cell differentiation. Plant J 20:610–628CrossRefGoogle Scholar
  31. Willats WGT, McCartney L, Knox JP (2001a) In-situ analysis of pectic polysaccharides in seed mucilage and at the root surface of Arabidopsis thaliana. Planta 213:37–44CrossRefPubMedGoogle Scholar
  32. Willats WGT, McCartney L, Mackie W, Knox JP (2001b) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9–27CrossRefPubMedGoogle Scholar
  33. Willats WGT, Orfila C, Limberg G, Buchholt HC, van Alebeek G-JWM, Voragen AGJ, Marcus SE, Christensen TMIE, Mikkelsen JD, Murray BS, Knox JP (2001c) Modulation of the degree and pattern of methyl-esterification of pectic homogalacturonan in plant cell walls: implications for pectin methyl esterase action, matrix properties and cell adhesion. J Biol Chem 276:19404–19413CrossRefPubMedGoogle Scholar
  34. Yu L, Mort AJ (1996) Partial characterization of xylogalacturonans from cell walls of ripe watermelon fruit: inhibition of endopolygalacturonase activity by xylosylation. In: Visser J, Voragen AGJ (eds) Pectins and pectinases. Elsevier, Amsterdam, pp 79–88Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • William G. T. Willats
    • 1
    • 5
  • Lesley McCartney
    • 1
  • Clare G. Steele-King
    • 1
  • Susan E. Marcus
    • 1
  • Andrew Mort
    • 2
  • Miranda Huisman
    • 3
  • Gert-Jan van Alebeek
    • 3
  • Henk A. Schols
    • 3
  • Alphons G. J. Voragen
    • 3
  • Angélique Le Goff
    • 4
  • Estelle Bonnin
    • 4
  • Jean-François Thibault
    • 4
  • J. Paul Knox
    • 1
  1. 1.Centre for Plant SciencesUniversity of LeedsLeedsUK
  2. 2.Department of Biochemistry and Molecular BiologyOklahoma State UniversityStillwaterUSA
  3. 3.Department of Agrotechnology and Food SciencesWageningen UniversityEV WageningenThe Netherlands
  4. 4.Unité de Recherche sur les Polysaccharides, leurs Organisations et InteractionsINRANantes Cedex 03France
  5. 5.Department of Plant Physiology, Institute of Molecular BiologyUniversity of CopenhagenCopenhagen KDenmark

Personalised recommendations