Hydroxyproline-Rich Glycoproteins: Form and Function

Annual Plant Reviews, Plant Polysaccharides: Biosynthesis and Bioengineering

Volumn 41, Issue , 2010, Pages 321-342

  Kieliszewski, Marcia J ^a   Lamport, Derek T A ^b   Tan, Li ^a   Cannon, Maura C ^c  

^a OHIO UNIVERSITY   (United States)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

arabinogalactan proteins; Diisodityrosine; Extensins; Hydroxyproline rich glycoproteins; Isodityrosine; O glycosylation

Indexed keywords

CELL MEMBRANES; GLYCOPROTEINS; GLYCOSYLATION; PLANTS (BOTANY); PLATES (STRUCTURAL COMPONENTS); PROTEINS; SCAFFOLDS (BIOLOGY);

ARABINOGALACTAN PROTEINS; DIISODITYROSINE; EXTENSINS; HYDROXYPROLINE RICH GLYCOPROTEINS; ISODITYROSINE; O-GLYCOSYLATION;

HYDROXYPROLINE;

EID: 79956011192     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781444391015.ch13     Document Type: Chapter

References (106)

1. 13C-NMR analysis of hydroxyproline arabi-nosides from Nicotiana tabacum. Agricultural and Biological Chemistry, 44, 2487-2489.
2. Allen, A.K., Desai, N.N., Neuberger, A., Creeth, J.M. (1978) Properties of potato lectin and the nature of its glycoprotein linkages. Biochemical Journal, 171, 665-674.
3. Ariga, K., Nakanishi, T., Michinobu, T. (2006) Immobilization of biomaterials to nano-assembled films (self-assembled monolayers, Langmuir-Blodgett films, and layer-by-l ayer assemblies) and their related functions 267. Journal of Nanoscience and Nanotechnology, 6(8), 2278-2301.
4. Ashford, D., Desai, N.N., Allen, A.K., Neuberger, A., O'Neill, M.A., Selvendran, R.R. (1982) Structural studies of the carbohydrate moieties of lectins from potato (Solanum tuberosum) tubers and thornapple (Datura stramonium) seeds. Biochemical Journal, 201, 199-208.
5. Aspinall, G.O., Malloy, J.A., Craig, J.W.T. (1969) Extracellular polysaccharides from suspension-cultured sycamore cells. Canadian Journal of Biochemistry, 47, 1063-1070.
6. Baldwin, T.C., McCann, M.C., Roberts, K. (1993) A novel hydroxyproline-deficient arabinogalactan protein secreted by suspension-cultured cells of Daucus carota. Plant Physiology, 103, 115-123.
7. Baldwin, T.C., Domingo, C., Schindler, T., Seetharaman, G., Stacey, N., Roberts, K. (2001) DcAGP1, a secreted arabinogalactan protein, is related to a family of basic proline-rich proteins. Plant Molecular Biology, 45(4), 421-435.
8. Baron-Epel, O., Gharyal, P.K., Schindler, M. (1988) Pectins as mediators of wall porosity in soybean cells. Planta, 175, 389-395.
9. Baumberger, N., Steiner, M., Ryser, U., Keller, B., Ringli, C. (2003) Synergistic interaction of the two paralogous Arabidopsis genes LRX1 and LRX2 in cell wall formation during root hair development. Plant Journal, 35(1), 71-81.
10. Bendtsen, J.D., Nielsen, H., von Heijne, G., Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. Journal of Molecular Biology, 340, 783-795.
11. Bernhardt, C., Tierney, M.L. (2000) Expression of AtPRP3, a proline-rich structural cell wall protein from Arabidopsis, is regulated by cell-type-specific developmental pathways involved in root hair formation. Plant Physiology, 122(3), 705-714.
12. Bollig, K., Lamshoeft, M., Schweimer, K., Marner, F.-J., Budzikiewiczc, H., Waffenschmidt, S. (2007) Structural analysis of linear hydroxyproline-bound O-glycans of Chlamydomonas reinhardtii-conservation of the inner core in Chlamydomonas and land plants. Carbohydrate Research, 342, 2557-2566.
13. Borner, G.H.H., Lilley, K.S., Stevens, T.J., Dupree, P. (2003) Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis. Plant Physiology, 132(2), 568-577.
14. Boudart, G., Jamet, E., Rossignol, M., et al. (2005) Cell wall proteins in apoplastic fluids of Arabidopsis thaliana rosettes: Identification by mass spectrometry and bioinformatics. Proteomics, 5(1), 212-221.
15. Brady, J.D., Sadler, I.H., Fry, S.C. (1996) Di-isodityrosine, a novel tetrameric derivative of tyrosine in plant cell wall proteins: a new potential cross-link. Biochemical Journal, 315, 323-327.
16. Brady, J.D., Sadler, I.H., Fry, S.C. (1998) Pulcherosine, an oxidatively coupled trimer of tyrosine in plant cell walls: its role in cross-link formation. Phytochemistry, 47, 349-353.
17. Brown, R.M., Jr., Romanovicz, D.K. (1976) Biogenesis and structure of Golgi-derived cellulosic scales in Pleurochrysis. I. Role of the endomembrane system in scale assembly and exocytosis. Appied Polymer Symposium, 28, 537-585.
18. Buglass, S., Lamport, D.T.A., Xu, J., Tan, Li., Kieliszewksi, M.J. (2008) Origin of the land plants: is Coleochaete their closest living relative? The writing is on the wall. 11th Cell Wall Meeting, Copenhagen, Abstract 17.
19. Cannon, M.C., Terneus, K.A., Hall, Q., et al. (2008) Self-assembly of the plant cell wall requires an extensin scaffold. Proceedings of the National Academy of Sciences of the U S A, 105(6), 2226-2231.
20. Carpita, N., Sabularse, D., Montezinos, D., Delmer, D.P. (1979) Determination of the pore size of cell walls of living plant cells. Science, 205, 1144-1147.
21. Cho, Y.-P., Chrispeels, M.J. (1976) Serine-O-galactosyl linkages in glycopeptides from carrot cell walls. Phytochemistry, 15, 165-169.
22. Cleland, R.E. (2001) Unlocking the mysteries of leaf primordia formation. Proceedings of the National Academy of Sciences of the U S A, 98(20), 10981-10982.
23. Cleland, R.E., Karlsnes, A. (1967) A possible role for hydroxyproline-containing proteins in the cessation of cell elongation. Plant Physiology, 42, 669-671.
24. Cooper, J.B., Heuser, J.E., Varner, J.E. (1994) 3,4-Dehydroproline inhibits cell wall assembly and cell division in tobacco protoplasts. Plant Physiology, 104, 747-752.
25. Epstein, L., Lamport, D.T.A. (1984) An intramolecular linkage involving isodityrosine in extensin. Phytochemistry, 23, 1241-1246.
26. Esquerre-Tugaye, M.T., Lamport, D.T.A. (1979) Cell surfaces in plant-microorganism interactions. I. A structural investigation of cell wall hydroxyproline-rich glycoproteins which accumulate in fungus-infected plants. Plant Physiology, 64, 314-319.
27. Estevez, J.M., Kieliszewski, M.J., Khitrov, N., Somerville, C. (2006) Characterization of synthetic hydroxyproline-rich proteoglycans with arabinogalactan protein and extensin motifs in Arabidopsis. Plant Physiology, 142(2), 458-470.
28. Fincher, G.B., Sawyer, W.H., Stone, B.A. (1974) Chemical and physical properties of an arabinogalactan-peptide from wheat endosperm. Biochemical Journal, 139, 535-545.
29. Fowler, T.J., Bernhardt, C., Tierney, M.L. (1999) Characterization and expression of four proline-rich cell wall protein genes in Arabidopsis encoding two distinct subsets of multiple domain proteins. Plant Physiology, 121(4), 1081-1091.
30. Fry, S.C. (1982) Isodityrosine, a new cross-linking amino acid from plant cell-wall glyoprotein. Biochemical Journal, 204, 449-455.
31. Goodenough, U.W., Heuser, J.E. (1989) Molecular organization of cell-wall crystals from Chlamydomonas reinhardtii and Volvox carteri. Journal of Cell Science, 90, 717-733.
32. Goodenough, U.W., Adair, W.S., Collin-Osdoby, P., Heuser, J.E. (1985) Structure of the Chlamydomonas agglutinin and related flagellar surface proteins in vitro and in situ. Journal of Cell Biology, 101, 924-941.
33. Goodenough, U.W., Gebhart, B., Mecham, R.P., Heuser, J.E. (1986) Crystals of the Chlamydomonas reinhardtii cell wall: polymerization, depolymerization and purification of glycoprotein monomers. Journal of Cell Biology, 103, 405-417.
34. Goodrum, L.J., Patel, A., Leykam, J.F., Kieliszewski, M.J. (2000) Gum arabic glycoprotein contains glycomodules of both extensin and arabinogalactan-glycoproteins. Phytochemistry, 54(1), 99-106.
35. Grobe, K., Poppelmann, M., Becker, W.-M., Petersen, A. (2002) Properties of group I allergens from grass pollen and their relation to cathepsin B, a member of the C1 family of cysteine proteinases. European Journal of Biochemistry, 269, 2083-2092.
36. Hall, Q., Cannon, M.C. (2002) The cell wall hydroxyproline-rich glycoprotein RSH is essential for normal embryo development in Arabidopsis. Plant Cell, 14, 1161-1172.
37. Held, M.A., Tan, L., Kamyab, A., Hare, M., Shpak, E., Kieliszewksi, M.J. (2004) Diisodityrosine is the intermolecular cross-link of isodityrosine-rich extensin analogs cross-linked in vitro. Journal ofBiological Chemistry, 279, 55474-55482.
38. Helm, M., Schmid, M., Hierl, G., et al. (2008) KDEL-tailed cysteine endopeptidases involved in programmed cell death,intercalation of new cells and dismantling of extensin scaffolds. American Journal of Botany, 95, 1049-1062.
39. Hieta, R., Myllyharju, J. (2002) Cloning and characterization of a low molecular weight prolyl 4-hydroxylase from Arabidopsis thaliana. Effective hydroxylation of proline-rich, collagen-like, and hypoxia-inducible transcription factor a-like peptides. Journal of Biological Chemistry, 277(26), 23965-23971.
40. Hills, G.J., Phillips, J.M., Gay, M.R., Roberts, K. (1975) Self-assembly of a plant cell wall in vitro. Journal of Molecular Biology, 96, 431-444.
41. Ito, M., Kodama, H., Komamine, A., Watanabe, A. (1998) Expression of extensin genes is dependent on the stage of the cell cycle and cell proliferation in suspension-cultured Catharanthus roseus cells. Plant Molecular Biology, 36(3), 343-351.
42. Jermyn, M.A., Yeow, Y.M. (1975) A class of lectins present in the tissues of seed plants. Australian Journal of Plant Physiology, 2, 501-531.
43. Johnson, K.L., Jones, B.J., Bacic, A., Schultz, C.J. (2003a) The fasciclin-like arabinoga-lactan proteins of Arabidopsis. A multigene family of putative cell adhesion molecules. Plant Physiology, 133(4), 1911-1925.
44. Johnson, K.L., Jones, B.J., Schultz, C.J., Bacic, A. (2003b) Non-enzymic cell wall (glyco)proteins. In: The Plant Cell Wall, Annual Plant Reviews Vol. 8 (ed. J.K. Rose), pp. 111-154. Blackwell Publishing Ltd., Oxford.
45. Kauss, H., Seehaus, K., Franke, R., Gilbert, S., Dietrich, R.A., Kroger, N. (2003) Silica deposition by a strongly cationic proline-rich protein from systemically resistant cucumber plants. Plant Journal, 33(1), 87-95.
46. Keller, B. (1993) Structural cell wall proteins. Plant Physiology, 101, 1127-1130.
47. Kieliszewski, M.J., Lamport, D.T.A. (1994) Extensin: repetitive motifs, functional sites, posttranslational codes and phylogeny. Plant Journal, 5, 157-172.
48. Kieliszewski, M.J., Kamyab, A., Leykam, J.F., Lamport, D.T.A. (1992) A histidine-rich extensin from Zea mays is an arabinogalactan protein. Plant Physiology, 99, 538-547.
49. Kieliszewski, M.J., Leykam, J.F., Lamport, D.T.A. (1990) Structure of the threonine-rich extensin from Zea mays. Plant Physiology, 92, 316-326.
50. Kieliszewski, M.J., Showalter, A.M., Leykam, J.F. (1994) Potato lectin: a modular protein sharing sequence similarities with the extensin family, the hevein lectin family, and snake venom disintegrins (platelet aggregation inhibitors). Plant Journal, 5, 849-861.
51. Lamport, D.T.A. (1963) Oxygen fixation into hydroxyproline of plant cell wall protein. Journal ofBiological Chemistry, 238, 1438-1440.
52. Lamport, D.T.A. (1965) The protein component of primary cell walls. Advances in Botanical Research, 2, 151-218.
53. Lamport, D.T.A. (1967) Hydroxyproline-O-glycosidic linkage of the plant cell wall glycoprotein extensin. Nature, 216, 1322-1324.
54. Lamport, D.T.A. (1970) Cell wall metabolism. Annual Review ofPlant Physiology, 21, 235-270.
55. Lamport, D.T.A. (1973) The glycopeptide linkages of extensin, O-D-galactosyl serine and O-L-arabinosyl hydroxyproline. In: Biogenesis ofPlant Cell Wall Polysaccharides, pp. 149-164. Academic Press, New York.
56. Lamport, D.T.A. (1977) Structure, biosynthesis and significance of cell wall glycoproteins. In: Recent Advances in Phytochemistry, 11 (eds F.A. Loewus and V.C. Runeckles), pp. 79-115. Plenum Press, New York.
57. Lamport, D.T.A. (2001) Life behind cell walls: Paradigm lost, paradigm regained. Cellular and Molecular Life Sciences, 58, 1363-1385.
58. Lamport, D.T.A., Northcote, D.H. (1960) Hydroxyproline in primary cell walls of higher plants. Nature, 188, 665-666.
59. Lamport, D.T.A., Katona, L., Roerig, S. (1973) Galactosyl serine in extensin. Biochemical Journal, 133, 125-131.
60. Lamport, D.T.A., Kieliszewksi, M.J., Showalter, A.M. (2006) Salt-stress upregulates periplasmic arabinogalactan-proteins: using salt-stress to analyse AGP function. New Phytologist, 169(3), 479-492.
61. Leucci, M.R., Di Sansebastiano, G.P., Gigante, M., Dalessandro, G., Piro, G. (2007) Secretion marker proteins and cell-wall polysaccharides move through different secretory pathways. Planta, 225(4), 1001-1017.
62. Li, L.C., Cosgrove, D.J. (2001) Grass group I pollen allergens (?-expansins) lack proteinase activity and do not cause wall loosening via proteolysis. European Journal of Biochemistry, 268(15), 4217-4226.
63. Miller, D.H., Lamport, D.T.A., Miller, M. (1972) Hydroxyproline heterooligosaccharides in Chlamydomonas. Science, 176, 918-920.
64. Oxley, D., Bacic, A. (1999) Structure of the glycosylphosphatidylinositol anchor of an arabinogalactan protein from Pyrus communis suspension-cultured cells. Proceedings of the National Academy of Sciences of the U S A, 96(25), 1424614251.
65. Petersen, A., Grobe, K., Schramm, G., et al. (1999) Structure and function can determine important features in allergenicity: investigations on the group I allergens of the grasses. International Symposium on Food Allergens, 1(3), 95-101.
66. Pope, D.G. (1977) Relationships between hydroxyproline-containing proteins secreted into the cell wall and medium by suspension-cultured Acer pseudoplatanus cells. Plant Physiology, 59, 894-900.
67. Qi, W., Fong, C., Lamport, D.T.A. (1991) Gum arabic glycoprotein is a twisted hairy rope: a new model based on O-galactosylhydroxyproline as the polysaccharide attachment site. Plant Physiology, 96, 848-855.
68. Rapaport, H. (2006) Ordered peptide assemblies at interfaces218. Supramolecular Chemistry, 18(5), 445-454.
69. Roberts, K. (1974) Crystalline glycoprotein cell walls of algae: Their structure, composition and assembly. Philosophical Transactions of the Royal Society of London Series B, 268, 129-146.
70. Roberts, K. (1990) Structures at the plant cell surface. Current Opinion in Cell Biology, 2, 920-928.
71. Roy, S., Jauh, G.Y., Hepler, P.K., Lord, E.M. (1998) Effects of Yariv phenylglycoside on cell wall assembly in the lily pollen tube. Planta, 204(4), 450-458.
72. Sadava, D., Chrispeels, M.J. (1971) Hydroxyproline biosynthesis in plant cells: pep-tidyl proline hydroxylase from carrot disks. Biochimica et Biophysica Acta, 227, 278-287.
73. Sadava, D., Chrispeels, M.J. (1973) Hydroxyproline-rich cell wall protein (extensin): role in the cessation of elongation in excised pea epicotyls. Developmental Biology, 30, 49-55.
74. Salditt, T., Schubert, U.S. (2002) Layer-by-layer self-assembly of supramolecular and biomolecular films. Reviews in Molecular Biotechnology, 90(1), 55-70.
75. Schnabelrauch, L.S., Kieliszewski, M.J., Upham, B.L., Alizedeh, H., Lamport, D.T.A. (1996) Isolation of pl 4.6 extensin peroxidase from tomato cell suspension cultures and identification of Val-Tyr-Lys as putative intermolecular cross-link site. Plant Journal, 9, 477-489.
76. Schultz, C.J., Rumsewicz, M.P., Johnson, K.L., Jones, B.J., Gaspar, Y.M., Bacic, A. (2002) Using genomic resources to guide research directions. The Arabinogalactan protein gene family as a test case. Plant Physiology, 129(4), 1448-1463.
77. Schultz, C.J., Ferguson, K.L., Lahnstein, J., Bacic, A. (2004) Post-translational modifications of arabinogalactan-peptides of Arabidopsis thaliana: ER and GPI-anchor signal cleavage sites and hydroxylation of proline. Journal of Biological Chemistry, 279, 1-48.
78. Sherrier, D.J., Prime, T.A., Dupree, P. (1999) Glycosylphosphatidylinositol-anchored cell-surface proteins from Arabidopsis. Electrophoresis, 20(10), 2027-2035.
79. Shimizu, M., Igasaki, T., Yamada, M., et al. (2005) Experimental determination of proline hydroxylation and hydroxyproline arabinogalactosylation motifs in secretory proteins. Plant Journal, 42, 877-889.
80. Shirsat, A.H., Bell, A., Spence, J., Harris, J.N. (1996) The Brassica napus extA extensin gene is expressed in regions of the plant subject to tensile stresses. Planta, 199, 618-624.
81. Shirsat, A.H., Thomson, H.E.C., Elliott, K.A. (2003) The Brassica napus extA extensin gene negative regulatory region controls expression in response to mechanical stresses. Plant, 26(10), 1647-1655.
82. Showalter, A.M., Zhou, J., Rumeau, D., Worst, S.G., Varner, J.E. (1991) Tomato extensin and extensin-like cDNAs: structure and expression in response to wounding. Plant Molecular Biology, 16, 547-565.
83. Shpak, E., Leykam, J.F., Kieliszewski, M.J. (1999) Synthetic genes for glycoprotein design and the elucidation of hydroxyproline-O-glycosylation codes. Proceedings of the National Academy of Sciences of the U S A, 96(26), 14736-14741.
84. Shpak, E., Barbar, E., Leykam, J.F., Kieliszewski, M.J. (2001) Contiguous hydroxy-proline residues direct hydroxyproline arabinosylation in Nicotiana tabacum. Journal of Biological Chemistry, 276(14), 11272-11278.
85. Smith, J.J., Muldoon, E.P., Lamport, D.T.A. (1984) Isolation of extensin precursors by direct elution of intact tomato cell suspension cultures. Phytochemistry, 23, 1233-1239.
86. Smith, J.J., Muldoon, E.P., Willard, J.J., Lamport, D.T.A. (1986) Tomato extensin precursors P1 and P2 are highly periodic structures. Phytochemistry, 25, 1021-1030.
87. Stafstrom, J.P., Staehelin, L.A. (1986) Cross-linking patterns in salt-extractable extensin from carrot cell walls. Plant Physiology, 81, 234-241.
88. Svetek, J., Yadav, M.P., Nothnagel, E.A. (1999) Presence of a glycosylphosphatidyli-nositol lipid anchor on rose arabinogalactan proteins. Journal of Biological Chemistry, 274(21), 14724-14733.
89. Tan, L., Leykam, J.F., Kieliszewski, M.J. (2003) Glycosylation motifs that direct arabi-nogalactan addition to arabinogalactan-proteins. Plant Physiology, 132(3), 1362-1369.
90. Tan, L., Qiu, F., Lamport, D.T.A., Kieliszewski, M.J. (2004) Structure of a hydroxy-proline (Hyp)-arabinogalactan polysaccharide from repetitive Ala-Hyp expressed in transgenic Nicotiana tabacum. Journal of Biological Chemistry, 279(13), 13156-13165.
91. Tan, L., Xu, J., Lamport, D.T.A., Feng, Q., Cottrell, C., Jin, Q., Kieliszewksi, M.J. (2007) The AGP Hyp-arabinogalactan backbone is a folded polysaccharide of reverse-turn hairpins generated by ß-(1-6) linked repeats of ß-(1-3) trigalactosyl units. 11th Cell Wall Meeting, Copenhagen, Abstract 68.
92. Tiainen, P., Myllyharju, J., Koivunen, P. (2005) Characterization of a second arabidop-sis thaliana prolyl 4-hydroxylase with distinct substrate specificity. Journal of Biological Chemistry, 280, 1142-1148.
93. Titel, C., Woelecke, H., Afifi, I., Ehwald, R. (1997) Dynamics of limiting cell wall porosity in plant suspension cultures. Planta, 203(3), 320-326.
94. Uchida, K., Muramatsu, T., Jamet, E., Furuya, Y. (1998) Control of expression of a gene encoding an extensin by phytochrome and a blue light receptor in spores of Adiantum capillus-veneris. Plant Journal, 15, 813-819.
95. Van Damme, Barre, A., Rouge, P., Peumans, W.J. (2004) Potato lectin: an updated model of a unique chimeric plant protein. Plant Journal, 37(1), 34-45.
96. Waffenschmidt, S., Woessner, J.P., Beer, K., Goodenough, U.W. (1993) Isodityrosine cross-linking mediates insolubilization of cell walls in Chlamydomonas. Plant Cell, 5, 809-820.
97. Wei, G., Shirsat, A.H. (2006) Extensin over-expression in Arabidopsis limits pathogen invasiveness. Molec.Plant Pathol, 7, 579-592.
98. Wilson, R.C., Long, F., Maruoka, E.M., Cooper, J.B. (1994) A new proline-rich early nodulin from Medicago truncatula is highly expressed in nodule meristematic cells. Plant Cell, 6, 1265-1275.
99. Xu, J., Tan, L., Goodrum, K.J., Kieliszewksi, M.J. (2007) High yields and extended serum half-life of human interferon a2b expressed in tobacco cells as Arabinogalactan-protein fusion. Biotechnology and Bioengineering, 97(5), 997-1008.
100. Xu, J., Tan, L., Lamport, D.T.A., Showalter, A.M., Kieliszewksi, M.J. (2008) The O-Hyp glycosylation code in tobacco and Arabidopsis and a proposed role of Hyp-glycans in secretion. Phytochemistry, 69(8), 1631-1640.
101. Yariv, J., Rapport, M.M., Graf, L. (1962) The interaction of glycosides and saccharides with antibody to the corresponding phenylazo glycosides. Biochemical Journal, 85, 383-388.
102. Yariv, J., Lis, H., Katchalski, E. (1967) Precipitation of arabic acid and some seed polysaccharides by glycosylphenylazo dyes. Biochemical Journal, 105,1C-2C.
103. Yasuhara, H. (2005) Caffeine inhibits callose deposition in the cell plate and the depolymerization of microtubules in the central region of the phragmoplast. Plant Cell Physiology, 46, 1083-1092.
104. Ye, Z.-H., Varner, J.E. (1991) Tissue-specific expression of cell wall proteins in developing soybean tissues. Plant Cell, 3, 23-37.
105. Zhao, Z.D., Tan, L., Showalter, A.M., Lamport, D.T.A., Kieliszewski, M.J. (2002) Tomato LeAGP-1 arabinogalactan-protein purified from transgenic tobacco corroborates the Hyp contiguity hypothesis. Plant Journal, 31(4), 431-444.
106. Zhou, J., Rumeau, D., Showalter, A.M. (1992) Isolation and characterization of two wound-regulated tomato extensin genes. Plant Molecular Biology, 20, 5-17.