Plant Molecular Biology

, Volume 54, Issue 3, pp 353–372 | Cite as

Members of a New Group of Chitinase-Like Genes are Expressed Preferentially in Cotton Cells with Secondary Walls

  • Deshui Zhang
  • Maria Hrmova
  • Chun-Hua Wan
  • Chunfa Wu
  • Jace Balzen
  • Wendy Cai
  • Jing Wang
  • Llewellyn D. Densmore
  • Geoffrey B. Fincher
  • Hong Zhang
  • Candace H. Haigler


Two homologous cotton (Gossypium hirsutum L.) genes, GhCTL1 and GhCTL2, encode members of a new group of chitinase-like proteins (called the GhCTL group) that includes other proteins from two cotton species, Arabidopsis, rice, and pea. Members of the GhCTL group are assigned to family GH19 glycoside hydrolases along with numerous authentic chitinases (, but the proteins have novel consensus sequences in two regions that are essential for chitinase activity and that were previously thought to be conserved. Maximum parsimony phylogenetic analyses, as well as Neighbor-Joining distance analyses, of numerous chitinases confirmed that the GhCTL group is distinct. A molecular model of GhCTL2 (based on the three-dimensional structure of a barley chitinase) had changes in the catalytic site that are likely to abolish catalytic activity while retaining potential to bind chitin oligosaccharides. RNA blot analysis showed that members of the GhCTL group had preferential expression during secondary wall deposition in cotton lint fiber. Cotton transformed with a fusion of the GhCTL2 promoter to the β-d-glucuronidase gene showed preferential reporter gene activity in numerous cells during secondary wall deposition. Together with evidence from other researchers that mutants in an Arabidopsis gene within the GhCTL group are cellulose-deficient with phenotypes indicative of altered primary cell walls, these data suggest that members of the GhCTL group of chitinase-like proteins are essential for cellulose synthesis in primary and secondary cell walls. However, the mechanism by which they act is more likely to involve binding of chitin oligosaccharides than catalysis.

cellulose chitin binding cotton fiber molecular modeling promoter activity secondary cell wall 


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  1. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 25: 3389–3402.CrossRefPubMedGoogle Scholar
  2. Ancillo, G., Witte, B., Schmelzer, E. and Kombrink, E. 1999. A distinct member of the basic (class I) chitinase gene family in potato is specifically expressed in epidermal cells. Plant Mol. Biol. 39: 1137–1151.CrossRefPubMedGoogle Scholar
  3. Bakkers, J., Kijne, J.W. and Spaink, H.P. 1999. Function of chitin oligosaccharides in plant and animal development. In: P. Jolles and R.A.A. Muzzarelli (Eds.), Chitin and Chitinases, Birkhaüser Verlag, Basel, pp. 71–84.Google Scholar
  4. Bayley, C., Trolinder, N., Ray, C., Morgan, M., Quisenberry, J.E. and Ow, D.W. 1992. Engineering 2,4-D resistance in cotton. Theor. Appl. Genet. 83: 645–649.CrossRefGoogle Scholar
  5. Benhamou, N. and Asselin, A. 1989. Attempted localization of substrate for chitinases in plant cells reveals abundant Nacetyl-D-glucosamine residues in secondary walls. Biol. Cell. 67: 341–350.CrossRefGoogle Scholar
  6. Berlin, J.D. 1986. The outer epidermis of the cotton seed. In: J.R. Mauney et al. (Eds.), Cotton Physiology, Cotton Foundation, Memphis, pp. 375–414.Google Scholar
  7. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N. and Bourne, P.E. 2000. The protein data bank. Nucl. Acids Res. 28: 235–242.CrossRefPubMedGoogle Scholar
  8. Bishop, J.G., Dean, A.M. and Mitchell-Olds, T. 2000. Rapid evolution in plant chitinases: molecular targets of selection in plant-pathogen coevolution. Proc. Natl. Acad. Sci. USA 97: 5322–5327.CrossRefPubMedGoogle Scholar
  9. Blundell, T., Carney, D., Gardner, S., Hayes, F., Howlin, B., Hubbard, T., Overington, J., Singh, D.A., Sibanda, B.L. and Sutcliffe, M. 1988. 18th Sir Hans Krebs lecture. Knowledge-based protein modelling and design. Eur. J. Biochem. 172: 513–520.PubMedGoogle Scholar
  10. Brameld, K.A. and Goddard, W.A. III. 1998. The role of enzyme distortion in the single displacement mechanism of Family 19 chitinases. Proc. Natl. Acad. Sci. USA 95: 4276–4281.CrossRefPubMedGoogle Scholar
  11. Broglie, K.E., Biddle, P., Cressman, R. and Broglie, R. 1989. Functional analysis of DNA sequences responsible for ethylene regulation of a bean chitinase gene in transgenic tobacco. Plant Cell 1: 599–607.CrossRefPubMedGoogle Scholar
  12. Burge, C.B. and Karlin, S. 1998. Finding the genes in genomic DNA. Curr. Opin. Struct. Biol. 8: 346–354.CrossRefPubMedGoogle Scholar
  13. Callebaut, I., Labesse, G., Durand, P., Poupon, A., Canard, L., Chomilier, J., Henrissat, B. and Mornon, J.P. 1997. Deciphering protein sequence information through hydrophobic cluster analysis (hca): current status and perspectives. Cell Mol. Life Sci. 53: 621–645.CrossRefPubMedGoogle Scholar
  14. Collinge, C.B., Kragh, K.M., Mikkelsen, J.D., Nielsen, K.K., Rasumussen, U. and Vad, K. 1993. Plant chitinases. Plant J. 3: 31–40.CrossRefPubMedGoogle Scholar
  15. Coupe, S.A., Taylor, J.E. and Roberts, J.A. 1997. Temporal and spatial expression of mRNAs encoding pathogenesis-related proteins during ethylene-promoted leaflet abscission in Sambucus nigra. Plant Cell Environ. 20: 1517–1524.CrossRefGoogle Scholar
  16. Danhash, N., Wagemakers, C.A., van Kan, J.A. and de Wit, P.J. 1993. Molecular characterization of four chitinase cDNAs obtained from Cladosporium fulvum-infected tomato. Plant Mol. Biol. 22: 1017–1029.PubMedGoogle Scholar
  17. Day, R.B., Okada, M., Ito, Y., Tsukada, K., Zaghouani, H., Shibuya, N. and Stacey, G. 2001. Binding site for chitin oligosaccharides in the soybean plasma membrane. Plant Physiol. 126: 1162–1173.CrossRefPubMedGoogle Scholar
  18. de Gehardt, L.B.A., Sachetto-Martins, G., Contarini, M.G., Sandroni, M., de Ferreira, R.P., de Lima, V.M., Cordeiro, M.C., de Oliveira, D.E. and Margis-Pinheiro, M. 1997. Arabidopsis thaliana class IV chitinase is early induced during interaction with Xanthomonas campestris. FEBS Lett. 419: 69–75.CrossRefPubMedGoogle Scholar
  19. DeLano, W.L. The PyMOL Molecular Graphics System. 2002. Scholar
  20. Devereux, J., Haeberli, P. and Smithies, O. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucl. Acids Res. 12: 387–395.PubMedGoogle Scholar
  21. Divne, C., Stahlberg, J., Teeri, T.T. and Jones, T.A. 1998. High resolution crystal structures reveal how a cellulose chain is bound in the 50 </del>Ålong tunnel of cellobiohydrolase I from Trichoderma reesei. J. Mol. Biol. 275: 309–325.CrossRefPubMedGoogle Scholar
  22. Dong, J.-Z. and Dunstan, D.I. 1997. Endochitinase and b-1,3-glucanase genes are developmentally regulated during somatic embryogenesis in Picea glauca. Planta 201: 189–194.PubMedGoogle Scholar
  23. Dubery, I.A. and Slater, V. 1997. Induced defense responses in cotton leaf disks by elicitors from Verticillium dahliae. Phytochemistry 44: 1429–1434.CrossRefGoogle Scholar
  24. Engh, R.A. and Huber, R. 1991. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Cryst. A47: 392–400.Google Scholar
  25. Gijzen, M., Kuflu, K., Qutob, D. and Chernys, J.T. 2001. A class chitinase from soybean seed coat. J. Exp. Bot. 52: 2283–2289.CrossRefPubMedGoogle Scholar
  26. Gooday, G.W. 1999. Aggressive and defensive roles for chitinases. In: P. Jolles and R.A.A. Muzzarelli (Eds.), Chitin and Chitinases, Birkhaüser Verlag, Basel, pp. 157–170.Google Scholar
  27. Goormachtig, S., Van de Velde, W., Lievens, S., Verplanke, C., Herman, S., De Keyser, A. and Holsters, M. 2001. Srchi24, a chitinase homolog lacking an essential glutamic acid residue for hydrolytic activity, is induced during nodule development in Sesbania rostrata. Plant Physiol. 127: 78–89.CrossRefPubMedGoogle Scholar
  28. Hamel, F., Boivin, R., Tremblay, C. and Bellemare, G. 1997. Structural and evolutionary relationships among chitinases of flowering plants. J. Mol. Evol. 44: 614–624.PubMedGoogle Scholar
  29. Hamel, F. and Bellemare, G. 1993. Nucleotide sequence of a Brassica napus endochitinase gene. Plant Physiol. 101: 140.CrossRefGoogle Scholar
  30. Hanfrey, C., Fife, M. and Buchanan-Wollaston, V. 1996. Leaf senescence in Brassica napus: expression of genes encoding pathogenesis-related proteins. Plant Mol. Biol. 30: 597–609.PubMedGoogle Scholar
  31. Harikrishna, K., Jampates-Beale, R., Milligan, S.B. and Gasser, C.S. 1996. An endochitinase gene expressed at high levels in the stylar transmitting tissue of tomatoes. Plant Mol. Biol. 30: 899–911.PubMedGoogle Scholar
  32. Hauser, M.-T., Morikami, A. and Benfey, P.N. 1995. Conditional root expansion mutants of Arabidopsis. Development 121: 1237–1252.PubMedGoogle Scholar
  33. Henrissat, B., Coutinho, P.M. and Davies, G.J. 2001. A census of carbohydrate-active enzymes in the genome of Arabidopsis thaliana. Plant Mol. Biol. 47: 55–72.CrossRefPubMedGoogle Scholar
  34. Higgins, D.G., Thompson, J.D. and Gibson, T.J. 1996. Using CLUSTAL for multiple sequence alignments. Meth. Enzymol. 266: 383–402.CrossRefPubMedGoogle Scholar
  35. Hood, E.E., Gelvin, S.B., Melchers, L.S. and Hoekema, A. 1993. New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res. 2: 208–218.Google Scholar
  36. Hrmova, M., De Gori, R., Smith, B.J., Fairweather, J.K., Driguez, H., Varghese, J.N. and Fincher, G.B. 2002. Structural basis for a broad specificity in higher plant β-D-glucan glucohydrolases. Plant Cell 14: 1033–1052.CrossRefPubMedGoogle Scholar
  37. Hudspeth, R.L., Hobbs, S.L., Anderson, D.M. and Grula, J.W. 1996. Characterization and expression of chitinase and 1,3-β-glucanase genes in cotton. Plant Mol. Biol. 31: 911–916.PubMedGoogle Scholar
  38. Huynh, Q.K., Hironaka, C.M., Levine, E.B., Smith, C.E., Borgmeyer, J.R. and Shah, D.M. 1992. Antifungal proteins from plants. Purification, molecular cloning, and antifungal properties of chitinases from maize seed. J. Biol. Chem. 267: 6635–6640.PubMedGoogle Scholar
  39. Iseli-Gamboni, G., Boller, T. and Neuhaus, J.-M. 1998. Mutation of either of two essential glutamates converts the catalytic domain of tobacco Class I chitinase into a chitinbinding lectin. Plant Sci. 134: 45–51.CrossRefGoogle Scholar
  40. Jeanmougin, F., Thompson, J.D., Gouy, M., Higgins, D.G. and Thompson, T.J. 1998. Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23: 403–405.CrossRefPubMedGoogle Scholar
  41. John, M. and Keller, G. 1995. Characterization of mRNA for a proline-rich protein of cotton fiber. Plant Physiol. 108: 669–676.CrossRefPubMedGoogle Scholar
  42. Jones, T.A., Zou, J.-Y., Cowan, S.W. and Kjeldgaard, M. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Cryst. A 47: 110–119.CrossRefGoogle Scholar
  43. Kellman, J.W., Kleinow, T., Engelhardt, K., Philipp, C., Wegener, D., Schell, J. and Schreier, P.H. 1996. Characterization of two class II chitinase genes from peanut and expression studies in transgenic tobacco plants. Plant Mol. Biol. 30: 351–358.PubMedGoogle Scholar
  44. Kragh, K.M., Hendriks, T., de Jong, A.J., Schiavo, F.L., Bucherna, N., Hojrup, P., Mikkelsen, J.D. and de Vries, S.C. 1996. Characterization of chitinases able to rescue somatic embryos of the temperature-sensitive carrot variant ts11. Plant Mol. Biol. 31: 631–645.PubMedGoogle Scholar
  45. Laskowski, R.A., MacArthur, M.W., Moss, D.S. and Thornton, J.M. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26: 283–291.CrossRefGoogle Scholar
  46. Leah, R., Skriver, K., Knudsen, S., Ruud-Hansen, J., Raikhel, N.V. and Mundy, J. 1994. Identification of an enhancer/ silencer sequence directing the aleurone-specific expression of a barley chitinase gene. Plant J. 6: 579–589.CrossRefPubMedGoogle Scholar
  47. Liang, P. and Pardee, A.B. 1992. Differential display of eukaryotic DNA by means of the polymerase chain reaction. Science 257: 967–970.PubMedGoogle Scholar
  48. Liao, Y.C., Kreuzaler, F., Fischer, R., Reisener, H.-J. and Tiburzy, R. 1994. Characterization of a wheat class Ib chitinase gene differentially induced in isogenic lines by infection with Puccinia graminis. Plant Sci. 103: 177–187.CrossRefGoogle Scholar
  49. Lim, A. and Zhang, L. 1999. WebPHYLIP: a web interface to PHYLIP. Bioinformatics 15: 1068–1069.CrossRefPubMedGoogle Scholar
  50. Liu, R.J., Li, H.F., Shen, C.Y. and Chiu, W.F. 1995. Detection of pathogenesis-related proteins in cotton plants. Physiol. Mol. Plant Path. 47: 357–363.CrossRefGoogle Scholar
  51. Margis-Pinheiro, M., Metz-Boutique, M.H., Awade, A., de Tapia, M., le Ret, M. and Burkhard, G. 1996. Isolation of a complementary DNA encoding the bean PR4 chitinase: an acidic enzyme with an amino terminus cysteine-rich domain. Plant Mol. Biol. 17: 243–253.Google Scholar
  52. Mauch, F., Hadwiger, L.A. and Boller, T. 1988. Antifungal hydrolases in pea tissue. I. purification and characterization of two chitinases and two β-1,3-glucanases differentially regulated during development and in response to fungal infection. Plant Physiol. 87: 325–333.Google Scholar
  53. Meins, F. Jr., Neuhaus, J.-M., Sperisen, C. and Ryals, J. 1992. The primary structure of plant pathogenesis-related glucanohydrolases and their genes. In: T. Boller and F. Meins (Eds.), Genes Involved in Plant Defense, Springer-Verlag, New York, pp. 245–282.Google Scholar
  54. Mouille, G, Robin, S., Lecomte, M., Pagant, S. and Hofte, H. 2003. Classification and identification of Arabidopsis cell wall mutants using Fourier-Tranform InfraRed (FT-IR) microspectroscopy. Plant J. 35: 393–4004.CrossRefPubMedGoogle Scholar
  55. Nairn, C.J., Niedz, R.P., Hearn, C.J., Osswald, W.F. and Mayer, R.T. 1997. cDNA cloning and expression of a class II acidic chitinase from sweet orange. Biochim. Biophys. Acta 1351: 22–26.CrossRefPubMedGoogle Scholar
  56. Neale, A.D., Wahleithner, J.A., Lund, M., Bonnett, H.T., Kelly, A., Meeks-Wagner, D.R., Peacock, W.J. and Dennis, E.S. 1990. Chitinase, 1,3-glucanase, osmotin, and extensin are expressed in tobacco explants during flower formation. Plant Cell 2: 673–684.CrossRefPubMedGoogle Scholar
  57. Nicolls, A., Sharp, K. and Honig, B. 1991. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 4: 281–296.Google Scholar
  58. Nielsen, K.K., Bojsen, K., Roepstorff, P. and Mikkelsen, J.D. 1994. A hydroxyproline-containing class IV chitinase of sugar beet is glycosylated with xylose. Plant Mol. Biol. 25: 241–257.PubMedGoogle Scholar
  59. Notredame, C., Higgins, D. and Heringa, J. 2000. T-Coffee: a novel method for multiple sequence alignment. J. Mol. Biol. 302: 205–217.CrossRefPubMedGoogle Scholar
  60. Ohme-Takagi, M., Meins, F. Jr. and Shinshi, H. 1998. A tobacco gene encoding a novel basic class II chitinase: the putative ancestor of basic class I and acidic class II chitinase genes. Mol. Gen. Genet. 259: 511–515.CrossRefPubMedGoogle Scholar
  61. Ohnuma, T., Yagi, M., Yamagami, T., Taira, T., Aso, Y. and Ishiguro, M. 2002. Molecular cloning, functional expression, and mutagenesis of cDNA encoding rye (Secale cereale) seed chitinase-c. Biosci. Biotechnol. Biochem. 66: 277–284.CrossRefPubMedGoogle Scholar
  62. Page, R.D.M. 1996. TREEVIEW: an application to display phylogenetic trees on personal computers. Comp. Appl. Biosci. 12: 357–358.PubMedGoogle Scholar
  63. Pilling, E. and Hofte H. 2003. Feedback from the wall. Curr. Opin. Plant Biol. 6: 611–616.CrossRefPubMedGoogle Scholar
  64. Potikha, T.S., Collins, C.C., Johnson, D.I., Delmer, D.P. and Levine, A. 1999. The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers. Plant Physiol. 119: 849–858.CrossRefPubMedGoogle Scholar
  65. Quiocho, F.A. 1986. Carbohydrate-binding proteins: tertiary structures and protein-sugar interactions. Annu. Rev. Biochem. 55: 287–315.CrossRefPubMedGoogle Scholar
  66. Ramachandran, G.N., Ramakrishnan, C. and Sasisekharan, V. 1963. Stereochemistry of polypeptide chain configurations. J. Mol. Biol. 7: 95–99.PubMedGoogle Scholar
  67. Robertus, J.D. and Monzingo, A.F. 1999. The structure and action of chitinases, In: P. Jolles and R.A.A. Muzzarelli (Eds.), Chitin and Chitinases, Birkhaüser Verlag, Basel, pp. 125–136.Google Scholar
  68. Robinson, S.P., Jacobs, A.K. and Dry, I.B. 1997. A class IV chitinase is highly expressed in grape berries during ripening. Plant Physiol. 114: 771–778.CrossRefPubMedGoogle Scholar
  69. Ruzin, S. 1999. Plant Microtechnique and Microscopy. Oxford University Press, Oxford, 322 pp.Google Scholar
  70. Sahai, A.S. and Manocha, M.S. 1993. Chitinases of fungi and plants: their involvement in morphogenesis and host-parasite interaction. FEMS Microbiol. Rev. 11: 317–338.CrossRefGoogle Scholar
  71. Saitou, M. and Nei, N. 1987. The neighbor joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.PubMedGoogle Scholar
  72. Sali, A. and Blundell, T.L. 1993. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234: 779–815.CrossRefPubMedGoogle Scholar
  73. Samak, D.A., Hirnoaka, C.M., Yallaly, P.E. and Shah, D.M. 1990. Isolation and characterization of the genes encoding basic and acidic endochitinases in Arabidopsis thaliana. Plant Physiol. 93: 907–914.Google Scholar
  74. Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Laboratory Press, Plainview, NY.Google Scholar
  75. Sanchez, R. and Sali, A. 1998. Large-scale protein structure modeling of the Saccharomyces cerevisiae genome. Proc. Natl. Acad. Sci. USA 95: 13597–13602.CrossRefPubMedGoogle Scholar
  76. Schneider, K., Wells, B., Dolan, L. and Roberts, K. 1997. Structural and genetic analysis of epidermal cell differentiation in Arabidopsis primary roots. Development 124: 1789–1798.PubMedGoogle Scholar
  77. Sippl, M.J. 1993. Recognition of errors in three-dimensional structures of proteins. Proteins 17: 355–362.PubMedGoogle Scholar
  78. Smith, T.F. and Waterman, M.S. 1981. Identification of common molecular sequences. J. Mol. Biol. 147: 195–197.PubMedGoogle Scholar
  79. Song, H.K., Hwang, K.Y., Kim, K.K. and Suh S.W. 1993. Crystallization and preliminary X-ray crystallographic analysis of chitinase from barley seeds. Proteins 17: 107–109.PubMedGoogle Scholar
  80. Song, P., Yamamoto, E. and Allen, R. 1995. Improved procedures for differential display of transcripts from cotton tissues. Plant Mol. Biol. Rep. 13: 174–181.Google Scholar
  81. Spaink, H.P., Wijfjes, A.H.M., Van Vliet, T.B., Kijne, J. and Lugengerg, B.J.L. 1993. Rhizobial lipo-oligosaccharide signals and their role in plant morphogenesis: are analogous lipophilic chitin derivatives produced by the plant? Aust. J. Plant Physiol. 20: 381–392.Google Scholar
  82. Svab, Z., Hajdukiewiez, P. and Maliga, P. 1995. Generation of transgenic tobacco plants by cocultivation of leaf disks with Agrobacterium binary vector. In: Maliga et al. (Eds.), Methods in Plant Molecular Biology: A Laboratory Course Manual, Cold Spring Harbor Laboratory Press, Plainview, NY, pp. 55–77.Google Scholar
  83. Swofford, D.L. 1998. PAUP*: phylogenetic analysis using parsimony (* and other methods), version 4. Sinauer, Sunderland, MA.Google Scholar
  84. Takakura, Y., Ito, T., Saito, H., Inoue, T., Komari, T. and Kuwata, S. 2000. Flower-predominant expression of a gene encoding a novel class I chitinase in rice. Plant Mol. Biol. 42: 883–897.CrossRefPubMedGoogle Scholar
  85. Terwisscha van Scheltinga, A.C., Armand, S., Kalk, K.H., Isogai, A., Henrissat, B. and Dijkstra, B.W. 1995. Stereochemistry of chitin hydrolysis by a plant chitinase/lysozyme and X-ray structure of a complex with allosamidin: evidence for substrate assisted catalysis. Biochemistry 34: 15619–15623.PubMedGoogle Scholar
  86. Trolinder, N. and Goodin, J.R. 1987. Somatic embryogenesis and plant regeneration in cotton (Gossypium hirsutum L.) Plant Cell Rep. 6: 231–234.CrossRefGoogle Scholar
  87. Trudel, J. and Asselin, A. 1989. Detection of chitinase activity after polyacrylamide gel electrophoresis. Anal. Biochem. 178: 362–366.PubMedGoogle Scholar
  88. Umbeck, P., Johnson, G., Barton, K. and Swain, W. 1987. Genetically transformed cotton (Gossypium hirsutum L.). plants. Bio/Technology 5: 263–266.CrossRefGoogle Scholar
  89. Umbeck, P., Swain, W. and Yang, N.-S. 1989. Inheritance and expression of genes for kanamycin and chloramphenicol resistance in transgenic cotton plants. Crop Sci. 29: 196–201.Google Scholar
  90. van Buuren, M., Neuhaus, J.-M., Shinshi, H., Ryals, J. and Meins, F. Jr. 1992. The structure and regulation of homeologous tobacco endochitinase genes of Nicotiana sylvestris and N. tomentosiformis origin. Mol. Gen. Genet. 232: 460–469.PubMedGoogle Scholar
  91. van Hengel, A.J., Tadesse, Z., Immerzeel, P., Schols, H., van Kammen, A. and de Vries, S.C. 2001. N-acetylglucosamine and glucosamine-containing arabinogalactan proteins control somatic embryogenesis. Plant Physiol. 125: 1880–1890.CrossRefPubMedGoogle Scholar
  92. Verburg, J.G., Smith, C.E., Lisek, C.A. and Huynh, Q.K. 1992. Identification of an essential tyrosine residue in the catalytic site of a chitinase isolated from Zea mays that is selectively modified during inactivation with 1-ethyl-3-(3-dimethylaminopropyl)-carbodiimide. J. Biol. Chem. 267: 3886–3893.PubMedGoogle Scholar
  93. Wemmer, T., Kaufmann, H., Kirch, H.-H., Schneider, K., Lottspeich, F. and Thompson, R.D. 1994. The most abundant soluble basic protein of the stylar transmitting tract in potato (Solanum tuberosum L.) is an endochitinase. Planta 194: 264–273.CrossRefPubMedGoogle Scholar
  94. Wilkins, T.A. and Smart, L.B. 1996. Isolation of RNA from plant tissue. In: Krieg, P.A. (Ed.), A Laboratory Guide to RNA: Isolation, Analysis, and Synthesis, Wiley/Liss, New York, pp. 21–40.Google Scholar
  95. Wojtaszek, P. and Bolwell, G.P. 1995. Secondary cell-wallspecific glycoprotein(s) from French bean hypocotyls. Plant Physiol. 108: 1001–1012.CrossRefPubMedGoogle Scholar
  96. Yeh, S., Moffatt, B., Griffith, M., Xiong, F., Yang, D.S.C., Wiseman, S.B., Sarhan, F., Danyluk, J., Xue, Y.Q., Hew, C.L., Doherty-Kirby, A. and Lajoie, G. 2000. Chitinase genes responsive to cold encode antifreeze proteins in winter cereals. Plant Physiol. 124: 1251–1264.CrossRefPubMedGoogle Scholar
  97. Zhong, R., Kayes, S.J., Schroeder, B.P. and Ye, Z.H. 2002. Mutation of a chitinase-like gene causes ectopic deposition of lignin, aberrant cell shapes, and overproduction of ethylene. Plant Cell 14: 165–179.CrossRefPubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Deshui Zhang
    • 1
    • 2
  • Maria Hrmova
    • 3
  • Chun-Hua Wan
    • 1
    • 4
  • Chunfa Wu
    • 1
    • 5
  • Jace Balzen
    • 1
  • Wendy Cai
    • 1
  • Jing Wang
    • 1
    • 6
  • Llewellyn D. Densmore
    • 1
  • Geoffrey B. Fincher
    • 3
  • Hong Zhang
    • 1
  • Candace H. Haigler
    • 1
    • 6
  1. 1.Department of Biological SciencesTexas Tech UniversityLubbockUSA
  2. 2.Department of Crop Science and Dept. of BotanyNorth Carolina State UniversityRaleighUSA
  3. 3.Faculty of Sciences, School of Agriculture and Wine, and the Australian Centre for Plant Functional GenomicsUniversity of AdelaideGlen OsmondAustralia
  4. 4.Content Systems, Celera GenomicsRockvilleUSA
  5. 5.Department of MicrobiologyTexas Tech University Health Sciences CenterLubbockUSA
  6. 6.Plant Stress and Water Conservation LaboratoryUSA

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