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

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Abstract

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 (http://afmb.cnrs-mrs.fr/CAZY/index.html), 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.

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References

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Burge, C.B. and Karlin, S. 1998. Finding the genes in genomic DNA. Curr. Opin. Struct. Biol. 8: 346–354.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • DeLano, W.L. The PyMOL Molecular Graphics System. 2002. http://www.pymol.org.

  • Devereux, J., Haeberli, P. and Smithies, O. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucl. Acids Res. 12: 387–395.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Dubery, I.A. and Slater, V. 1997. Induced defense responses in cotton leaf disks by elicitors from Verticillium dahliae. Phytochemistry 44: 1429–1434.

    Article  Google Scholar 

  • 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 

  • Gijzen, M., Kuflu, K., Qutob, D. and Chernys, J.T. 2001. A class chitinase from soybean seed coat. J. Exp. Bot. 52: 2283–2289.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Hamel, F. and Bellemare, G. 1993. Nucleotide sequence of a Brassica napus endochitinase gene. Plant Physiol. 101: 140.

    Article  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Hauser, M.-T., Morikami, A. and Benfey, P.N. 1995. Conditional root expansion mutants of Arabidopsis. Development 121: 1237–1252.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Higgins, D.G., Thompson, J.D. and Gibson, T.J. 1996. Using CLUSTAL for multiple sequence alignments. Meth. Enzymol. 266: 383–402.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • John, M. and Keller, G. 1995. Characterization of mRNA for a proline-rich protein of cotton fiber. Plant Physiol. 108: 669–676.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Liang, P. and Pardee, A.B. 1992. Differential display of eukaryotic DNA by means of the polymerase chain reaction. Science 257: 967–970.

    PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Lim, A. and Zhang, L. 1999. WebPHYLIP: a web interface to PHYLIP. Bioinformatics 15: 1068–1069.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • Notredame, C., Higgins, D. and Heringa, J. 2000. T-Coffee: a novel method for multiple sequence alignment. J. Mol. Biol. 302: 205–217.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Page, R.D.M. 1996. TREEVIEW: an application to display phylogenetic trees on personal computers. Comp. Appl. Biosci. 12: 357–358.

    PubMed  Google Scholar 

  • Pilling, E. and Hofte H. 2003. Feedback from the wall. Curr. Opin. Plant Biol. 6: 611–616.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Quiocho, F.A. 1986. Carbohydrate-binding proteins: tertiary structures and protein-sugar interactions. Annu. Rev. Biochem. 55: 287–315.

    Article  PubMed  Google Scholar 

  • Ramachandran, G.N., Ramakrishnan, C. and Sasisekharan, V. 1963. Stereochemistry of polypeptide chain configurations. J. Mol. Biol. 7: 95–99.

    PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • Ruzin, S. 1999. Plant Microtechnique and Microscopy. Oxford University Press, Oxford, 322 pp.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Saitou, M. and Nei, N. 1987. The neighbor joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.

    PubMed  Google Scholar 

  • Sali, A. and Blundell, T.L. 1993. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234: 779–815.

    Article  PubMed  Google Scholar 

  • 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 

  • Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Laboratory Press, Plainview, NY.

    Google Scholar 

  • Sanchez, R. and Sali, A. 1998. Large-scale protein structure modeling of the Saccharomyces cerevisiae genome. Proc. Natl. Acad. Sci. USA 95: 13597–13602.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Sippl, M.J. 1993. Recognition of errors in three-dimensional structures of proteins. Proteins 17: 355–362.

    PubMed  Google Scholar 

  • Smith, T.F. and Waterman, M.S. 1981. Identification of common molecular sequences. J. Mol. Biol. 147: 195–197.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • 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 

  • 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 

  • Swofford, D.L. 1998. PAUP*: phylogenetic analysis using parsimony (* and other methods), version 4. Sinauer, Sunderland, MA.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Trolinder, N. and Goodin, J.R. 1987. Somatic embryogenesis and plant regeneration in cotton (Gossypium hirsutum L.) Plant Cell Rep. 6: 231–234.

    Article  Google Scholar 

  • Trudel, J. and Asselin, A. 1989. Detection of chitinase activity after polyacrylamide gel electrophoresis. Anal. Biochem. 178: 362–366.

    PubMed  Google Scholar 

  • Umbeck, P., Johnson, G., Barton, K. and Swain, W. 1987. Genetically transformed cotton (Gossypium hirsutum L.). plants. Bio/Technology 5: 263–266.

    Article  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • Wojtaszek, P. and Bolwell, G.P. 1995. Secondary cell-wallspecific glycoprotein(s) from French bean hypocotyls. Plant Physiol. 108: 1001–1012.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

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Author notes

  1. Deshui Zhang

    Present address: Department of Crop Science and Dept. of Botany, North Carolina State University, 4405 Williams Hall, Raleigh, NC, 27695, USA

  2. Candace H. Haigler

    Present address: Plant Stress and Water Conservation Laboratory, 3810 4th Street, Lubbock, TX 79415, USA

Authors and Affiliations

  1. Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409, USA

    Deshui Zhang, Chun-Hua Wan, Chunfa Wu, Jace Balzen, Wendy Cai, Jing Wang, Llewellyn D. Densmore, Hong Zhang & Candace H. Haigler

  2. Faculty of Sciences, School of Agriculture and Wine, and the Australian Centre for Plant Functional Genomics, University of Adelaide, Waite Campus, Glen Osmond, SA, 5064, Australia

    Maria Hrmova & Geoffrey B. Fincher

  3. Content Systems, Celera Genomics, 45 W Gude Drive, Rockville, MD, 20850, USA

    Chun-Hua Wan

  4. Department of Microbiology, Texas Tech University Health Sciences Center, Lubbock, TX 79409, USA

    Chunfa Wu

  5. Plant Stress and Water Conservation Laboratory, 3810 4th Street, Lubbock, TX 79415, USA

    Jing Wang

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  11. Candace H. Haigler
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Zhang, D., Hrmova, M., Wan, CH. et al. Members of a New Group of Chitinase-Like Genes are Expressed Preferentially in Cotton Cells with Secondary Walls. Plant Mol Biol 54, 353–372 (2004). https://doi.org/10.1023/B:PLAN.0000036369.55253.dd

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