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Planta

, Volume 233, Issue 2, pp 287–298 | Cite as

Advances in understanding pectin methylesterase inhibitor in kiwi fruit: an immunological approach

  • Evelien Vandevenne
  • Stefanie Christiaens
  • Sandy Van Buggenhout
  • Ruben P. Jolie
  • Margarita González-Vallinas
  • Thomas Duvetter
  • Paul J. Declerck
  • Marc E. Hendrickx
  • Ann Gils
  • Ann Van Loey
Original Article

Abstract

In order to gain insight into the in situ properties and localisation of kiwi pectin methylesterase inhibitor (PMEI), a toolbox of monoclonal antibodies (MA) towards PMEI was developed. Out of a panel of MA generated towards kiwi PMEI, three MA, i.e. MA-KI9A8, MA-KI15C12 and MA-KI15G7, were selected. Thorough characterisation proved that these MA bind specifically to kiwi PMEI and kiwi PMEI in complex with plant PME and recognise a linear epitope on PMEI. Extract screening of green kiwi (Actinidia deliciosa) and gold kiwi (Actinidia chinensis) confirmed the potential use of these MA as probes to screen for PMEI in other sources. Tissue printing revealed the overall presence of PMEI in pericarp and columella of ripe kiwi fruit. Further analysis on the cellular level showed PMEI label concentrated in the middle lamella and in the cell-wall region near the plasmalemma. Intercellular spaces, however, were either completely filled or lined with label. In conclusion, the developed toolbox of antibodies towards PMEI can be used as probes to localise PMEI on different levels, which can be of relevance for plant physiologists as well as food technologists.

Keywords

Immunolocalisation Kiwi fruit Monoclonal antibodies Pectin methylesterase inhibitor 

Abbreviations

fPME

Aspergillus aculeatus pectin methylesterase

MA

Monoclonal antibody

PME

Pectin methylesterase

PMEI

Pectin methylesterase inhibitor

t1PME

Tomato (Solanum Lycopersicon) pectin methylesterase

Notes

Acknowledgments

This research has been carried out with financial support from the Research Council K.U.Leuven (IDO/05/011). S. Christiaens and S. Van Buggenhout are researchers funded by the Research Foundation - Flanders (FWO). The authors would like to acknowledge ProMeta, the Interfacultary Centre for Proteomics and Metabolomics for the MALDI-TOF-MS analysis. Sincere thanks goes to Prof. J. Hofkens for giving us access to Olympus Fluoview 1000 confocal microscope.

References

  1. An SH, Sohn KH, Choi HW, Hwang IS, Lee SC, Hwang BK (2008) Pepper pectin methylesterase inhibitor protein CaPMEI1 is required for antifungal activity, basal disease resistance and abiotic stress tolerance. Planta 228:61–78CrossRefPubMedGoogle Scholar
  2. Balestrieri C, Castaldo D, Giovane A, Quagliuolo L, Servillo L (1990) A glycoprotein inhibitor of pectin methylesterase in kiwi fruit (Actinidia chinensis). Eur J Biochem 193:183–187CrossRefPubMedGoogle Scholar
  3. Blumer JM, Clay RP, Bergmann CW, Albersheim P, Darvill A (2000) Characterization of changes in pectin methylesterase expression and pectin esterification during tomato fruit ripening. Can J Bot/Rev Can Bot 78:607–618CrossRefGoogle Scholar
  4. Bordenave M (1996) Analysis of pectin methyl esterases. In: Linskens HF, Jacksons JF (eds) Modern methods of plant analysis: plant cell wall analysis. Springer, Berlin, pp 165–180Google Scholar
  5. Bosch M, Hepler PK (2005) Pectin methylesterase and pectin dynamics in pollen tubes. Plant Cell 17:3219–3226CrossRefPubMedGoogle Scholar
  6. Camardella L, Carratore V, Ciardiello MA, Servillo L, Balestrieri C, Giovane A (2000) Kiwi protein inhibitor of pectin methylesterase: amino-acid sequence and structural importance of two disulfide bridges. Eur J Biochem 267:4561–4565CrossRefPubMedGoogle Scholar
  7. Camardella L, Giovane A, Servillo L (2003) Structure-function of a proteinaceous inhibitor of plant pectin methylesterase. In: Voragen F, Schols H, Servillo L (eds) Advances in pectins and pectinase research. Kluwer Academic Publishing, London, pp 363–372Google Scholar
  8. Castaldo D, Lovoi A, Quagliuolo L, Servillo L, Balestrieri C, Giovane A (1991) Orange juices and concentrates stabilization by a proteic inhibitor of pectin methylesterase. J Food Sci 56:1632–1634CrossRefGoogle Scholar
  9. Chat J, Jauregui B, Petit RJ, Nadot S (2004) Reticulate evolution in kiwifruit (Actinidia, Actinidiaceae) identified by comparing their maternal and paternal phylogenies. Am J Bot 91:736–747CrossRefGoogle Scholar
  10. Christensen TMIE, Nielsen JE, Kreiberg JD, Rasmussen P, Mikkelsen JD (1998) Pectin methyl esterase from orange fruit: characterization and localization by in situ hybridization and immunohistochemistry. Planta 206:493–503CrossRefPubMedGoogle Scholar
  11. Ciardiello MA, D’Avino R, Amoresano A, Tuppo L, Carpentieri A, Carratore V, Tamburrini M, Giovane A, Pucci P, Camardella L (2008) The peculiar structural features of kiwi fruit pectin methylesterase: amino acid sequence, oligosaccharides structure, and modeling of the interaction with its natural proteinaceous inhibitor. Proteins 71:195–206CrossRefPubMedGoogle Scholar
  12. D’Avino R, Camardella L, Christensen T, Giovane A, Servillo L (2003) Tomato pectin methylesterase: modeling, fluorescence, and inhibitor interaction studies-comparison with the bacterial (Erwinia chrysanthemi) enzyme. Proteins 53:830–839CrossRefPubMedGoogle Scholar
  13. Di Matteo A, Giovane A, Raiola A, Camardella L, Bonivento D, De Lorenzo G, Cervone F, Bellincampi D, Tsernoglou D (2005) Structural basis for the interaction between pectin methylesterase and a specific inhibitor protein. Plant Cell 17:849–858CrossRefPubMedGoogle Scholar
  14. Duvetter T, Van Loey A, Smout C, Verlent I, Nguyen BL, Hendrickx M (2005) Aspergillus aculeatus pectin methylesterase: study of the inactivation by temperature and pressure and the inhibition by pectin methylesterase inhibitor. Enzyme Microb Technol 36:385–390CrossRefGoogle Scholar
  15. Duvetter T, Sila DN, Van Buggenhout S, Jolie R, Van Loey A, Hendrickx M (2009) Pectins in processed fruit and vegetables. Part I. Stability and catalytic activity of pectinases. Compr Rev Food Sci Food Saf 8:75–85CrossRefGoogle Scholar
  16. Ferguson AR (1999) Kiwifruit cultivars: breeding and selection. Acta Hortic 498:43–51Google Scholar
  17. Galfrè G, Milstein C (1981) Preparation of monoclonal antibodies: strategies and procedures. Methods Enzymol 73:3–46CrossRefPubMedGoogle Scholar
  18. Gils A, Ceresa E, Macovei AM, Marx PF, Peeters M, Compernolle G, Declerck PJ (2005) Modulation of TAFI function through different pathways—implications for the development of TAFI inhibitors. J Thromb Haemost 3:2745–2753CrossRefPubMedGoogle Scholar
  19. Giovane A, Balestrieri C, Quagliuolo L, Castaldo D, Servillo L (1995) A glycoprotein inhibitor of pectin methylesterase in kiwi fruit—purification by affinity-chromatography and evidence of a ripening-related precursor. Eur J Biochem 233:926–929CrossRefPubMedGoogle Scholar
  20. Giovane A, Servillo L, Balestrieri C, Raiola A, D'Avino R, Tamburrini M, Ciardiello MA, Camardella L (2004) Pectin methylesterase inhibitor. BBA Proteins Proteom 1696:245–252CrossRefGoogle Scholar
  21. Giovane A, Quagliuolo L, Castaldo D, Servillo L, Balestrieri C (1990) Pectin methylesterase from Actinidia chinensis fruits. Phytochemistry 29:2821–2823CrossRefGoogle Scholar
  22. Hallett IC, Macrae EA, Wegrzyn TF (1992) Changes in kiwifruit cell-wall ultrastructure and cell packing during postharvest ripening. Int J Plant Sci 153:49–60CrossRefGoogle Scholar
  23. Heukeshoven J, Dernick R (1985) Simplified method for silver staining of proteins in polyacrylamide gels and the mechanism of silver staining. Electrophoresis 6:103–112CrossRefGoogle Scholar
  24. Hothorn M, Wolf S, Aloy P, Greiner S, Scheffzek K (2004) Structural insights into the target specificity of plant invertase and pectin methylesterase inhibitory proteins. Plant Cell 16:3437–3447CrossRefPubMedGoogle Scholar
  25. Jauneau A, Roy S, Reis D, Vian B (1998) Probes and microscopical methods for the localization of pectins in plant cells. Int J Plant Sci 159:1–13CrossRefGoogle Scholar
  26. Jolie RP, Duvetter T, Houben K, Clynen E, Sila DN, Van Loey AM, Hendrickx ME (2009) Carrot pectin methylesterase and its inhibitor from kiwi fruit: study of activity, stability and inhibition. Innov Food Sci Emerg 10:601–609CrossRefGoogle Scholar
  27. Jolie RP, Duvetter T, Vandevenne E, Van Buggenhout S, Van Loey AM, Hendrickx ME (2010) A pectin-methylesterase-inhibitor-based molecular probe for in situ detection of plant pectin methylesterase activity. J Agric Food Chem 58:5449–5456CrossRefPubMedGoogle Scholar
  28. Knox JP, Linstead PJ, King J, Cooper C, Roberts K (1990) Pectin esterification is spatially regulated both within cell-walls and between developing tissues of root apices. Planta 181:512–521CrossRefGoogle Scholar
  29. Ly-Nguyen B, Van Loey AM, Smout C, Verlent I, Duvetter T, Hendrickx ME (2004) Effect of intrinsic and extrinsic factors on the interaction of plant pectin methylesterase and its proteinaceous inhibitor from kiwi fruit. J Agric Food Chem 52:8144–8150CrossRefPubMedGoogle Scholar
  30. Marttila S, Santén K (2007) Practical aspects of immunomicroscopy on plant material. In: Mendez-Vilas A, Diaz J (eds) Modern research and educational topics in microscopy. Formatex, Badajoz, pp 1015–1021Google Scholar
  31. Micheli F (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci 6:414–419CrossRefPubMedGoogle Scholar
  32. Montefiori M, McGhie TK, Hallett IC, Costa G (2009) Changes in pigments and plastid ultrastructure during ripening of green-fleshed and yellow-fleshed kiwifruit. Sci Hortic (Amsterdam) 119:377–387CrossRefGoogle Scholar
  33. Morvan O, Quentin M, Jauneau A, Mareck A, Morvan C (1998) Immunogold localization of pectin methylesterases in the cortical tissues of flax hypocotyl. Protoplasma 202:175–184CrossRefGoogle Scholar
  34. O’Neill MA, York WS (2003) The composition and structure of plant primary cell walls. In: Rose JKC (ed) Annual plant reviews, vol 8: the plant cell wall. Blackwell, Oxford, pp 1–54Google Scholar
  35. Pelloux J, Rusterucci C, Mellerowicz EJ (2007) New insights into pectin methylesterase structure and function. Trends Plant Sci 12:267–277CrossRefPubMedGoogle Scholar
  36. Quentin M, Jauneau A, Morvan O, Mareck A, Gaffé J, Morvan C (1997) Immunolocalization of pectin methylesterases in the hypocotyl tissues of flax. Plant Physiol Biochem 35:475–482Google Scholar
  37. Redgwell RJ, Melton LD, Brasch DJ (1992a) Cell-wall dissolution in ripening kiwifruit (Actinidia deliciosa): solubilization of the pectic polymers. Plant Physiol 98:71–81CrossRefPubMedGoogle Scholar
  38. Redgwell RJ, Melton LD, Brasch DJ, Coddington JM (1992b) Structures of the pectic polysaccharides from the cell-walls of kiwifruit. Carbohydr Res 226:287–302CrossRefGoogle Scholar
  39. Redgwell RJ, MacRae E, Hallett I, Fischer M, Perry J, Harker R (1997) In vivo and in vitro swelling of cell walls during fruit ripening. Planta 203:162–173CrossRefGoogle Scholar
  40. Sila DN, Van Buggenhout S, Duvetter T, Fraeye I, De Roeck A, Van Loey A, Hendrickx M (2009) Pectins in processed fruit and vegetables. Part II. Structure–function relationships. Compr Rev Food Sci F 8:86–104CrossRefGoogle Scholar
  41. Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T, Vorwerk S, Youngs H (2004) Toward a systems approach to understanding plant cell walls. Science 306:2206–2211CrossRefPubMedGoogle Scholar
  42. Steele NM, McCann MC, Roberts K (1997) Pectin modification in cell walls of ripening tomatoes occurs in distinct domains. Plant Physiol 114:373–381PubMedGoogle Scholar
  43. Sutherland P, Hallett L, Redgwell R, Benhamou N, MacRae E (1999) Localization of cell wall polysaccharides during kiwifruit (Actinidia deliciosa) ripening. Int J Plant Sci 160:1099–1109CrossRefPubMedGoogle Scholar
  44. Van Buggenhout S, Sila DN, Duvetter T, Van Loey A, Hendrickx M (2009) Pectins in processed fruits and vegetables. Part III. Texture engineering. Compr Rev Food Sci Food Saf 8:105–117CrossRefGoogle Scholar
  45. Van den Broeck I, Ludikhuyze LR, Weemaes CA, Van Loey AM, Hendrickx ME (1999) Thermal inactivation kinetics of pectinesterase extracted from oranges. J Food Process Preserv 23:391–406CrossRefGoogle Scholar
  46. Vandevenne E, Van Buggenhout S, Duvetter T, Brouwers E, Declerck PJ, Hendrickx ME, Van Loey A, Gils A (2009) Development and evaluation of monoclonal antibodies as probes to assess the differences between two tomato pectin methylesterase isoenzymes. J Immunol Methods 349:18–27CrossRefPubMedGoogle Scholar
  47. Vierstraete E, Cerstiaens A, Baggerman G, Van den Bergh G, De Loof A, Schoofs L (2003) Proteomics in Drosophila melanogaster: first 2D database of larval hemolymph proteins. Biochem Biophys Res Commun 304:831–838CrossRefPubMedGoogle Scholar
  48. Waldron KW, Parker ML, Smith AC (2003) Plant cell walls and food quality. Compr Rev Food Sci Food Saf 2:128–146CrossRefGoogle Scholar
  49. Willats WGT, Knox P, Mikkelsen JD (2006) Pectin: new insights into an old polymer are starting to gel. Trends Food Sci Technol 17:97–104CrossRefGoogle Scholar
  50. Wolf S, Grsic-Rausch S, Rausch T, Greiner S (2003) Identification of pollen-expressed pectin methylesterase inhibitors in Arabidopsis. FEBS Lett 555:551–555CrossRefPubMedGoogle Scholar
  51. Wolf S, Rausch T, Greiner S (2009) The N-terminal pro region mediates retention of unprocessed type-I PME in the Golgi apparatus. Plant J 58:361–375CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Evelien Vandevenne
    • 1
  • Stefanie Christiaens
    • 1
  • Sandy Van Buggenhout
    • 1
  • Ruben P. Jolie
    • 1
  • Margarita González-Vallinas
    • 1
  • Thomas Duvetter
    • 1
  • Paul J. Declerck
    • 2
  • Marc E. Hendrickx
    • 1
  • Ann Gils
    • 2
  • Ann Van Loey
    • 1
  1. 1.Laboratory of Food Technology and Leuven Food Science and Nutrition Research Centre (LFoRCe), Department of Microbial and Molecular Systems (M2S)Katholieke Universiteit LeuvenLeuvenBelgium
  2. 2.Laboratory for Pharmaceutical Biology, Department of Pharmaceutical SciencesKatholieke Universiteit LeuvenLeuvenBelgium

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