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Biochemistry (Moscow)

, 73:1053 | Cite as

Polygalacturonase-inhibiting protein is a structural component of plant cell wall

  • M. A. ProtsenkoEmail author
  • N. L. Buza
  • A. A. Krinitsyna
  • E. A. Bulantseva
  • N. P. Korableva
Review

Abstract

It is generally believed that plants “evolved a strategy of defending themselves from a phytopathogen attack” during evolution. This metaphor is used frequently, but it does not facilitate understanding of the mechanisms providing plant resistance to the invasion of foreign organisms and to other unfavorable external factors, as well as the role of these mechanisms in plant growth and development. Information on processes involving one of the plant resistance factors—polygalacturonase-inhibiting protein (PGIP)—is considered in this review. The data presented here indicate that PGIP, being an extracellular leucine-rich repeat-containing protein, performs important functions in the structure of plant cell wall. Amino acid residues participating in PGIP binding to homogalacturonan in the cell wall have been determined. The degree of methylation and the mode of distribution of homogalacturonan methyl groups are responsible for the formation of a complex structure, which perhaps determines the specificity of PGIP binding to pectin. PGIP is apparently one of the components of plant cell wall determining some of its mechanical properties; it is involved in biochemical processes related to growth, expansion, and maceration, and it influences plant morphology. Polygalacturonase (PG) is present within practically all plant tissues, but the manifestation of its activity varies significantly depending on physiological conditions in the tissue. Apparently, the regulation of PG functioning in apoplast significantly affects the development of processes associated with the modification of the structure of plant cell wall. PGIP can regulate PG activity through binding to homogalacturonan. The genetically determined structure of PGIP in plants determines the mode of its interaction with an invader and perhaps is one of the factors responsible for the set of pathogens causing diseases in a given plant species.

Key words

polygalacturonase-inhibiting protein PGIP polygalacturonase homogalacturonan plant cell wall resistance LRR proteins pectin 

Abbreviations

eLRR

completely extracellular leucine-rich repeat-containing proteins

LRR

leucine-rich repeats

LRX

leucine-rich extensin

PEX1

pollen-specific extensin

PG

polygalacturonase

PGIP

polygalacturonase-inhibiting protein

PME

pectin methyl esterase

References

  1. 1.
    Albersheim, P., and Anderson, A. J. (1971) Proc. Natl. Acad. Sci. USA, 68, 1815–1819.PubMedCrossRefGoogle Scholar
  2. 2.
    Darvill, A., Bergmann, C., Cervone, R., de Lorenzo, G., Ham, K.-S., Spiro, M. D., York, W. S., and Albersheim, P. (1994) Biochem. Soc. Symp., 60, 89–94.PubMedGoogle Scholar
  3. 3.
    De Lorenzo, G., D’Ovidio, R., and Cervone, F. (2001) Annu. Rev. Phytopathol., 39, 313–335.PubMedCrossRefGoogle Scholar
  4. 4.
    Abu-Goukh, A. A., and Labavitch, J. M. (1983) Physiol. Plant Pathol., 23, 123–135.CrossRefGoogle Scholar
  5. 5.
    Favaron, F., Castiglioni, C., D’Ovidio, R., and Alghisi, P. (1997) Physiol. Mol. Plant Pathol., 50, 403–417.CrossRefGoogle Scholar
  6. 6.
    Di, C., Zhang, M., Xu, S., Cheng, T., and An, L. (2006) Crit. Rev. Microbiol., 32, 91–100.PubMedCrossRefGoogle Scholar
  7. 7.
    Federici, L., di Matteo, A., Fernandez-Recio, J., Tsernoglou, D., and Cervone, F. (2006) Trends Plant Sci., 11, 65–70.PubMedCrossRefGoogle Scholar
  8. 8.
    Glinka, E. M., Protsenko, M. A., Bulantseva, E. A., and Sal’kova, E. G. (2001) Prikl. Biokhim. Mikrobiol., 37, 607–611.PubMedGoogle Scholar
  9. 9.
    Kajava, A. V. (1998) J. Mol. Biol., 277, 519–527.PubMedCrossRefGoogle Scholar
  10. 10.
    Martin, G. B., Bogdanove, A. G., and Sessa, G. (2003) Annu. Rev. Plant Biol., 54, 23–61.PubMedCrossRefGoogle Scholar
  11. 11.
    Mattei, B., Bemalda, M. S., Federici, L., Roepstorff, P., Cervone, F., and Boffi, A. (2001) Biochemistry, 40, 569–576.PubMedCrossRefGoogle Scholar
  12. 12.
    Di Matteo, A., Federici, L., Mattei, B., Salvi, G., de Lorenzo, G., Tsernoglou, D., and Cervone, F. (2003) Proc. Natl. Acad. Sci. USA, 100, 10124–10128.PubMedCrossRefGoogle Scholar
  13. 13.
    Leckie, F., Mattei, B., Capodicasa, C., Hemmings, A., Nuss, L., Aracri, B., de Lorenzo, G., and Cervone, F. (1999) EMBO J., 18, 2352–2363.PubMedCrossRefGoogle Scholar
  14. 14.
    D’Ovidio, R., Mattei, B., Roberti, S., and Bellincampi, D. (2004) Biochim. Biophys. Acta, 1696, 237–244.PubMedGoogle Scholar
  15. 15.
    Lafitte, C., Barthe, J. P., Montillet, J. L., and Touze, A. (1984) Physiol. Plant Pathol., 25, 39–53.CrossRefGoogle Scholar
  16. 16.
    Powell, A. L. T., van Kan, J., ten Have, A., Visser, J., Greve, L. C., Bennett, A. B., and Labavitch, J. M. (2000) Mol. Plant-Microbe Interact., 13, 942–950.PubMedCrossRefGoogle Scholar
  17. 17.
    Krinitsyna, A. A., Speranskaya, A. S., Poltronieri, P., Santino, A., Bogacheva, A. M., Buza, N. L., Protsenko, M. A., and Shevelev, A. B. (2006) Genetika, 42, 477–486.Google Scholar
  18. 18.
    Salvi, G., Giarrizzo, F., de Lorenzo, G., and Cervone, F. (1990) Plant Physiol., 136, 513–518.Google Scholar
  19. 19.
    Gazendam, I., Oelofse, D., and Berger, D. K. (2004) Physiol. Mol. Plant Pathol., 65, 145–155.CrossRefGoogle Scholar
  20. 20.
    Milner, J., and Avigard, G. (1967) Carbohydr. Res., 4, 359–3621.CrossRefGoogle Scholar
  21. 21.
    Dingle, J., Reid, W. W., and Solomonos, G. L. (1953) J. Sci. Food Agric., 4, 149–153.CrossRefGoogle Scholar
  22. 22.
    Devoto, A., Clark, A. J., Nuss, L., Cervone, F., and de Lorenzo, G. (1997) Planta, 202, 284–292.CrossRefGoogle Scholar
  23. 23.
    Pressey, R. (1996) Phytochemistry, 42, 1267–1270.PubMedCrossRefGoogle Scholar
  24. 24.
    Toubart, P., Desiderio, A., Salvi, G., Cervone, F., Daroda, L., de Lorenzo, G., Bergmann, C., Darvill, A. G., and Albersheim, P. (1992) Plant J., 2, 367–373.PubMedGoogle Scholar
  25. 25.
    Buza, N. L., Krinitsyna, A. A., and Protsenko, M. A. (2005) Materials of Int. Sci.-Pract. Conf. “Urgent Problems of Protection of Potato, Fruit and Vegetable Cultures from Diseases, Vermins, and Weeds”, Minsk, pp. 392–396.Google Scholar
  26. 26.
    Degra, L., Salvi, G., Mariotti, D., de Lorenzo, G., and Cervone, F. (1988) J. Plant Physiol., 133, 364–366.Google Scholar
  27. 27.
    Guyon, V., Tang, W., Monti, M. M., Raiola, A., de Lorenzo, G., McCormick, S., and Taylor, L. P. (2004) Plant J., 39, 643–654.PubMedCrossRefGoogle Scholar
  28. 28.
    Thornburg, R. W., Carter, C., Powell, A., Mittler, R., Rizhsky, L., and Horner, H. T. (2003) Plant Syst. Evol., 238, 211–218.Google Scholar
  29. 29.
    Fish, W. W. (2005) Eur. J. Plant Pathol., 111, 67–76.CrossRefGoogle Scholar
  30. 30.
    Abu-Goukh, A. A., Strand, L. L., and Labavitch, J. M. (1983) Physiol. Plant Pathol., 23, 101–109.CrossRefGoogle Scholar
  31. 31.
    Stotz, H. U., Contos, J. J. A., Powell, A. L. T., Bennett, A. B., and Labavitch, J. M. (1994) Plant Mol. Biol., 25, 607–617.PubMedCrossRefGoogle Scholar
  32. 32.
    Buza, N. L., Krinitsyna, A. A., Protsenko, M. A., and Vartapetyan, V. V. (2004) Prikl. Biokhim. Mikrobiol., 40, 104–108.PubMedGoogle Scholar
  33. 33.
    Johnston, D. J., Ramanathan, V., and Williamson, B. (1993) J. Exp. Bot., 44, 971–976.CrossRefGoogle Scholar
  34. 34.
    Mehli, L., Schaart, J. G., Kjellsen, T. D., Tran, D. H., Salentijn, E. M. J., Schouten, H. J., and Iversen, T. H. (2004) New Phytologist, 163, 99–110.CrossRefGoogle Scholar
  35. 35.
    D’Hallewin, G., Schirra, M., Powell, A. L. T., Greve, L. C., and Labavitch, J. M. (2004) Physiol. Plant., 120, 395–404.PubMedCrossRefGoogle Scholar
  36. 36.
    Redgwell, R. J., MacRae, E. A., Hallett, I., Fischer, M., Perry, J., and Harker, R. (1997) Planta, 203, 162–173.CrossRefGoogle Scholar
  37. 37.
    Nuss, L., Mahe, A., Clark, A. J., Grisvard, J., Dron, M., Cervone, F., and de Lorenzo, G. (1996) Physiol. Mol. Plant Pathol., 48, 83–89.CrossRefGoogle Scholar
  38. 38.
    Li, R., Rimmer, R., Min, Yu, Sharpe, A. G., Serguin-Swartz, G., Lydiate, D., and Hegedus, D. D. (2003) Planta, 217, 299–308.PubMedGoogle Scholar
  39. 39.
    Ahsan, N., Yoon, H.-S., and Jo, J. (2005) Plant Sci., 169, 1081–1089.CrossRefGoogle Scholar
  40. 40.
    Devoto, A., Leckie, F., Lupotto, E., Cervone, F., and de Lorenzo, G. (1998) Planta, 205, 165–174.PubMedCrossRefGoogle Scholar
  41. 41.
    Worrall, D., Elias, L., Ashford, D., Smallwood, M., Sidebottom, C., Littford, P., Talford, J., Holt, C., and Bowles, D. (1998) Science, 282, 115–117.PubMedCrossRefGoogle Scholar
  42. 42.
    Meyer, K., Keil, M., and Naldrett, M. J. (1999) FEBS Lett., 447, 171–178.PubMedCrossRefGoogle Scholar
  43. 43.
    Zhang, D.-Q., Wang, H.-B., Liu, B., Feng, D.-R., He, Y.-M., and Wang, J.-F. (2006) Acta Genet. Sin., 33, 1027–1036.PubMedCrossRefGoogle Scholar
  44. 44.
    Baumberger, N., Steiner, M., Ryser, U., Keller, B., and Ringli, C. (2003) Plant J., 35, 71–81.PubMedCrossRefGoogle Scholar
  45. 45.
    Stratford, S., Barnes, W., Hohorst, D. L., Sagert, J. G., Cotter, R., Golubiewski, A., Showalter, A. M., McCormick, S., and Bedinger, P. (2001) Plant Mol. Biol., 46, 43–56.PubMedCrossRefGoogle Scholar
  46. 46.
    Jang, S., Lee, B., Kim, C., Kim, S.-J., Yim, J., Han, J.-J., Lee, S., Kim, S.-R., and An, G. (2003) Plant Mol. Biol., 53, 357–369.PubMedCrossRefGoogle Scholar
  47. 47.
    Albersheim, P., Darvill, A. G., O’Neill, M. A., Schols, H. A., and Voragen, A. G. J. (1996) in Pectins and Pectinases (Visser, J., and Voragen, A. G. J., eds.) Elsevier Science BV, Amsterdam, pp. 47–55.CrossRefGoogle Scholar
  48. 48.
    Perez, S., Mazeau, K., and Herve du Penhoat, C. (2000) Plant Physiol. Biochem., 38, 37–55.CrossRefGoogle Scholar
  49. 49.
    Micheli, F. (2001) Trends Plant Sci., 6, 414–419.PubMedCrossRefGoogle Scholar
  50. 50.
    Willats, W. G. T., McCartney, L., Mackie, W., and Knox, J. P. (2001) Plant Mol. Biol., 47, 9–27.PubMedCrossRefGoogle Scholar
  51. 51.
    Wydra, K., and Beri, H. (2006) Physiol. Mol. Plant Pathol., 68, 41–50.CrossRefGoogle Scholar
  52. 52.
    Di Matteo, A., Bonivento, D., Tsernoglou, D., Federici, L., and Cervone, F. (2006) Phytochemistry, 67, 528–533.PubMedCrossRefGoogle Scholar
  53. 53.
    Sakamoto, T., Bonnin, E., and Thibault, J.-F. (2003) Biochim. Biophys. Acta, 1621, 280–284.PubMedGoogle Scholar
  54. 54.
    Spadoni, S., Zabotina, O., di Matteo, A., Mikkelsen, J. D., Cervone, F., de Lorenzo, G., Mattei, B., and Bellincampi, D. (2006) Plant Physiol., 141, 557–564.PubMedCrossRefGoogle Scholar
  55. 55.
    Willats, W. G. T., Marcus, S. E., and Knox, J. P. (1998) Carbohydr. Res., 308, 149–152.PubMedCrossRefGoogle Scholar
  56. 56.
    Jarvis, M. C., Briggs, S. P. H., and Knox, J. P. (2003) Plant Cell Environ., 26, 977–989.CrossRefGoogle Scholar
  57. 57.
    Willats, W. G. T., Limberg, G., Buchholt, H. C., van Alebeek, G.-J., Benen, J., Christensen, T. M. I. E., Visser, J., Voragen, A., Mikkelsen, J. D., and Knox, J. P. (2000) Carbohydr. Res., 327, 309–320.PubMedCrossRefGoogle Scholar
  58. 58.
    Clausen, M. H., Willats, W. G. T., and Knox, J. P. (2003) Carbohydr. Res., 338, 1797–1800.PubMedCrossRefGoogle Scholar
  59. 59.
    Roberts, J. A., Elliott, K. A., and Gonzalez-Carranza, Z. H. (2002) Annu. Rev. Plant Biol., 53, 131–158.PubMedCrossRefGoogle Scholar
  60. 60.
    Bush, M. S., Marry, M., and Huxham, I. M. (2001) Planta, 213, 869–880.PubMedCrossRefGoogle Scholar
  61. 61.
    Salerno, M.-I., Gianinazzi, S., Arnould, C., and Gianinazzi-Pearson, V. (2004) J. Gen. Plant Pathol., 70, 153–158.CrossRefGoogle Scholar
  62. 62.
    Lenartowska, M., Rodriguez-Garcia, M. I., and Bednarska, E. (2001) Hort. Planta, 213, 182–191.Google Scholar
  63. 63.
    Leboeuf, E., Guillon, F., Thoiron, S., and Lahaye, M. (2005) J. Exp. Bot., 56, 3171–3182.PubMedCrossRefGoogle Scholar
  64. 64.
    Hadfield, K. A., and Bennett, A. B. (1998) Plant Physiol., 117, 337–343.PubMedCrossRefGoogle Scholar
  65. 65.
    Brummell, D. A., and Harpster, M. H. (2001) Plant Mol. Biol., 47, 311–340.PubMedCrossRefGoogle Scholar
  66. 66.
    Smith, C. J. S., Watson, C. F., Ray, J., Bird, C. R., Morris, P. C., Schuch, W., and Grierson, D. (1988) Nature, 334, 724–726.CrossRefGoogle Scholar
  67. 67.
    Kalaitzis, P., Solomos, T., and Tucker, M. L. (1997) Plant Physiol., 113, 1303–1308.PubMedCrossRefGoogle Scholar
  68. 68.
    Roberts, J. A., Whitelaw, C. A., Gonzalez-Carranza, Z. H., and McManus, M. T. (2000) Ann. Bot., 86, 223–235.CrossRefGoogle Scholar
  69. 69.
    Pressey, R., and Reger, B. J. (1989) Plant Sci., 59, 57–62.CrossRefGoogle Scholar
  70. 70.
    Rhee, S. Y., and Somerville, C. R. (1998) Plant J., 15, 79–88.PubMedCrossRefGoogle Scholar
  71. 71.
    Sander, L., Child, R., Ulvskov, P., Albrechtsen, M., and Borkhardt, B. (2001) Plant Mol. Biol., 46, 469–479.PubMedCrossRefGoogle Scholar
  72. 72.
    Dearnaley, J. D. W., and Daggard, G. A. (2001) Sex Plant Reprod., 13, 265–271.CrossRefGoogle Scholar
  73. 73.
    Capodicasa, C., Vairo, D., Zabotina, O., McCartney, L., Caprari, C., Mattei, B., Manfredini, C., Aracri, B., Benen, J., Knox, J. P., de Lorenzo, G., and Cervone, F. (2004) Plant Physiol., 135, 1294–1304.PubMedCrossRefGoogle Scholar
  74. 74.
    Atkinson, R. G., Schroder, R., Hallett, I. C., Cohen, D., and MacRae, E. A. (2002) Plant Physiol., 129, 122–133.PubMedCrossRefGoogle Scholar
  75. 75.
    Pressey, R., and Avants, J. K. (1977) Plant Physiol., 60, 548–553.PubMedGoogle Scholar
  76. 76.
    Zang, Z., Pierce, M. L., and Mort, A. (2007) Phytochemistry, 68, 1094–1103.CrossRefGoogle Scholar
  77. 77.
    Sitrit, Y., Downie, B., Bennet, A. B., and Bradford, K. J. (1996) Plant Physiol., 111, 161 (Abstr. No. 752) Suppl.Google Scholar
  78. 78.
    Peretto, R., Favaron, F., Bettini, V., de Lorenzo, G., Marini, S., Alghisi, P., Cervone, F., and Bonfante, P. (1992) Planta, 188, 164–172.CrossRefGoogle Scholar
  79. 79.
    Jones, T. M., Anderson, A. J., and Albersheim, P. (1972) Physiol. Plant Pathol., 2, 153–166.CrossRefGoogle Scholar
  80. 80.
    Vasil’eva, K. V., Gladkikh, T. A., and Davydova, M. A. (1984) in Biochemistry of Immunity, Rest, and Aging of Plants (Berezin, I. V., ed.) [in Russian], Nauka, Moscow, pp. 105–124.Google Scholar
  81. 81.
    Herron, S. R., Benen, J. A., Scavetta, R. D., Visser, J., and Jumak, F. (2000) Proc. Natl. Acad. Sci. USA, 97, 8762–8769.PubMedCrossRefGoogle Scholar
  82. 82.
    Federici, L., Caprari, C., Mattei, B., Savino, C., di Matteo, A., de Lorenzo, G., Cervone, F., and Tsernoglou, D. (2001) Proc. Natl. Acad. Sci. USA, 98, 13425–13430.PubMedCrossRefGoogle Scholar
  83. 83.
    King, D., Bergmann, C., Orlando, R., Benen, J. A., Kester, H. C., and Visser, J. (2002) Biochemistry, 41, 10225–10233.PubMedCrossRefGoogle Scholar
  84. 84.
    Carpita, N. C., and Gibeaut, D. M. (1993) Plant J., 3, 1–30.PubMedCrossRefGoogle Scholar
  85. 85.
    Sakamoto, T., Bonnin, E., and Thibault, J.-F. (2003) Biochim. Biophys. Acta, 1621, 280–284.PubMedGoogle Scholar
  86. 86.
    Caprari, C., Mattei, B., Basile, M. L., Salvi, G., Crescenzi, V., de Lorenzo, G., and Cervone, F. (1996) Mol. Plant-Microbe Interact., 9, 617–624.PubMedGoogle Scholar
  87. 87.
    Stotz, H. U., Bishop, J. G., Bergmann, C. W., Koch, M., Albersheim, P., Darvill, A., and Labavitch, J. M. (2000) Physiol. Mol. Plant Pathol., 56, 117–130.CrossRefGoogle Scholar
  88. 88.
    Barmore, C. R., and Nguyen, T. K. (1985) Phytopathology, 75, 446–449.CrossRefGoogle Scholar
  89. 89.
    Desiderio, A., Aracri, B., Leckie, F., Mattei, B., Salvi, G., Tigelaar, H., van Roekel, J. S. C., Baulcombe, D. C., Melchers, L. S., de Lorenzo, G., and Cervone, F. (1997) Mol. Plant-Microbe Interact., 10, 852–860.PubMedCrossRefGoogle Scholar
  90. 90.
    Kemp, G., Stanton, L., Bergmann, C. W., Clay, R. P., Albersheim, P., and Darvill, A. (2004) Mol. Plant-Microbe Interact., 17, 888–894.PubMedCrossRefGoogle Scholar
  91. 91.
    Nalumpang, S., Gotoh, Y., Tsuboi, H., Gomi, K., Yamamoto, H., and Akimitsu, K. (2002) J. Gen. Plant Pathol., 68, 118–127.CrossRefGoogle Scholar
  92. 92.
    Van der Hoorn, R. A. L., Wulff, B. B. H., Rivas, S., Durrant, M. C., van der Ploeg, A., de Wit, P. J. G. M., and Jonesb, J. D. G. (2005) Plant Cell, 17, 1000–1015.PubMedCrossRefGoogle Scholar
  93. 93.
    Cervone, F., de Lorenzo, G., Pressey, R., Darvill, A. G., and Albersheim, P. (1990) Phytochemistry, 29, 447–449.CrossRefGoogle Scholar
  94. 94.
    Ferrari, S., Vairo, D., Ausubel, F. M., Cervone, F., and de Lorenzo, G. (2003) Plant Cell, 15, 93–106.PubMedCrossRefGoogle Scholar
  95. 95.
    Wu, Q., Szakacs-Dobozi, M., Hemmat, M., and Hrazdina, G. (1995) Plant Physiol., 102, 219–225.Google Scholar
  96. 96.
    Yao, C. L., Conway, W. S., and Sams, C. E. (1993) Phytopathology, 85, 1373–1377.CrossRefGoogle Scholar
  97. 97.
    Brown, A. E. (1984) Phytopathol. Z., 111, 122–132.CrossRefGoogle Scholar
  98. 98.
    Gazendam, I., Oelofse, D., and Berger, D. K. (2004) Physiol. Mol. Plant Pathol., 65, 145–155.CrossRefGoogle Scholar
  99. 99.
    Federici, L., di Matteo, A., Fernandez-Recio, J., Tsernoglou, D., and Cervone, F. (2006) Trends Plant Sci., 11, 65–70.PubMedCrossRefGoogle Scholar
  100. 100.
    Lee, S.-J., Saravanan, R. S., Damasceno, C. M. B., Yamane, H., Kim, B.-D., and Rose, J. K. C. (2004) Plant Physiol. Biochem., 42, 979–988.PubMedCrossRefGoogle Scholar
  101. 101.
    Gorshkova, T. A. (2007) Plant Cell Wall as a Dynamic System [in Russian], Nauka, Moscow.Google Scholar

Copyright information

© MAIK Nauka 2008

Authors and Affiliations

  • M. A. Protsenko
    • 1
    Email author
  • N. L. Buza
    • 1
  • A. A. Krinitsyna
    • 1
  • E. A. Bulantseva
    • 1
  • N. P. Korableva
    • 1
  1. 1.Bach Institute of BiochemistryRussian Academy of SciencesMoscowRussia

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