Plant cellulose synthases (CesAs) are the key enzymes necessary for cellulose biosynthesis. In Arabidopsis, two distinct groups of three CesAs each are necessary for cellulose synthesis during primary and secondary cell wall formation. It has also been suggested that such three CesAs interact with each other to form plasma-membrane bound rosette complexes that are functional during cellulose production. However, in vivo demonstration of such assemblies of three CesAs into rosettes has not been possible. We used yeast two-hybrid assays to demonstrate the possible interactions among several CesAs from Arabidopsis and aspen via their N-terminal zinc-binding domains (ZnBDs). While strong positive interactions were detected among ZnBDs from secondary wall associated CesAs of both Arabidopsis and aspen, the intergeneric interactions between Arabidopsis and aspen CesAs were weak. Moreover, in aspen, three primary wall associated CesA ZnBDs positively interacted with each other as well as with secondary CesAs. These results suggest that ZnBDs from either primary or secondary CesAs, and even from different plant species could interact but are perhaps insufficient for specificities of such interactions among CesAs. These observations suggest that some other more specific interacting regions might exist within CesAs. It is also possible that some hitherto unknown mechanism exists in plants for assembling the rosette complexes with different compositions of CesAs. Understanding how cellulose is synthesized will have a direct impact on utilization of lignocellulosic biomass for bioenergy production.
Somerville, C. (2006) Cellulose synthesis in higher plants. Annual Review of Cell and Developmental Biology, 22(1), 53-78.
Joshi, C.P. and Mansfield, S.D. (2007) The cellulose paradox—simple molecule, complex biosynthesis. Current Opinion in Plant Biology, 10(3), 220-226.
Delmer, D.P. (1999) Cellulose biosynthesis: Exciting times for a difficult field of study. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 245- 276.
Doblin, M.S., Kurek, I., Jacob-Wilk, D. and Delmer, D.P. (2002) Cellulose biosynthesis in plants: From genes to rosettes. Plant Cell Physiology, 43(12), 1407-1420.
Kimura, S., Laosinchai, W., Itoh, T., Cui, X., Linder, C.R. and Brown, R.M. Jr. (1999) Immunogold labeling of rosette terminal cellulose-synthesizing complexes in the vascular plant vigna angularis. Plant Cell, 11(11), 2075- 2086.
Itoh, T., Kimura, S. and Brown, R.M. (2004) Theoretical considerations of immunogold labeling of cellulose synthesizing terminal complexes. Cellulose, 11(3-4), 385-394.
Arioli, T., Peng, L.C., Betzner, A.S., Burn, J., Wittke, W., Herth, W., Camilleri, C., Hofte, H., Plazinski, J., Birch, R., Cork, A., Glover, J., Redmond, J. and Williamson, R. E. (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science, 279(5351), 717-720.
Scheible, W.R., Eshed, R., Richmond, T., Delmer, D. and Somerville, C. (2001) Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis Ixr1 mutants. Proceedings of the National Academy of Sciences of the United States of America, 98(18), 10079-10084.
Taylor, N.G., Scheible, W.R., Cutler, S., Somerville, C.R. and Turner, S.R. (1999) The irregular xylem3 locus of arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. Plant Cell, 11(5), 769-779.
Taylor, N.G., Howells, R.M., Huttly, A.K., Vickers, K. and Turner, S.R. (2003) Interactions among three distinct CesA proteins essential for cellulose synthesis. Proceed- ings of the National Academy of Sciences of the United States of America, 100(3), 1450-1455.
Taylor, N.G., Laurie, S. and Turner, S.R. (2000) Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell, 12(12), 2529-2540.
Fagard, M., Desnos, T., Desprez, T., Goubet, F., Refregier, G., Mouille, G., McCann, M., Rayon, C., Vernhettes, S. and Hofte, H. (2000) ROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell, 12(12), 2409-2424.
Gardiner, J. C., Taylor, N.G. and Turner, S.R. (2003) Control of cellulose synthase complex localization in developing xylem. Plant Cell, 15(8), 1740-1748.
Desprez, T., Juraniec, M., Crowell, E.F., Jouy, H., Pochylova, Z., Parcy, F., Hofte, H., Gonneau, M. and Vernhettes, S. (2007) Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 104(39), 15572-15577.
Tanaka, K., Murata, K., Yamazaki, M., Onosato, K., Miyao, A. and Hirochika, H. (2003) Three distinct rice cellulose synthase catalytic subunit genes required for cellulose synthesis in the secondary wall. Plant Physiology, 133(1), 73-83.
Burton, R.A., Shirley, N.J., King, B.J., Harvey, A.J. and Fincher, G.B. (2004) The CesA gene family of barley. Quantitative analysis of transcripts reveals two groups of co-expressed genes. Plant Physiology, 134(1), 224-236.
Bhandari, S., Fujino, T., Thammanagowda, S., Zhang, D. Y., Xu, F.Y. and Joshi, C.P. (2006) Xylem-specific and tension stress-responsive coexpression of KORRIGAN endoglucanase and three secondary wall-associated cellulose synthase genes in aspen trees. Planta, 224(4), 828-837.
Joshi, C.P., Bhandari, S., Ranjan, P., Kalluri, U.C., Liang, X., Fujino, T. and Samuga, A. (2004) Genomics of cellu- lose biosynthesis in poplars. New Phytologist, 164(1), 53-61.
Ranik, M. and Myburg, A.A. (2006) Six new cellulose synthase genes from Eucalyptus are associated with primary and secondary cell wall biosynthesis. Tree Physiology, 26(5), 545-556.
Kurek, I., Kawagoe, Y., Jacob-Wilk, D., Doblin, M. and Delmer, D. (2002) Dimerization of cotton fiber cellulose synthase catalytic subunits occurs via oxidation of the zinc-binding domains. Proceedings of the National Academy of Sciences of the United States of America, 99 (17), 11109-11114.
Jacob-Wilk, D., Kurek, I., Hogan, P. and Delmer, D.P. (2006) The cotton fiber zinc-binding domain of cellulose synthase A1 from Gossypium hirsutum displays rapid turnover in vitro and in vivo. Proceedings of the National Academy of Sciences of the United States of America, 103(32), 12191-12196.
Timmers, J., Vernhettes, S., Desprez, T., Vincken, J.P., Visser, R.G. and Trindade, L.M. (2009) Interactions between membrane-bound cellulose synthases involved in the synthesis of the secondary cell wall. FEBS Letters, 583(6), 978-982.
Atanassov, II, Pittman, J.K. and Turner, S.R. (2009) Elucidating the mechanisms of assembly and subunit interaction of the cellulose synthase complex of Ara- bidopsis secondary cell walls. Journal of Biological Chemistry, 284(6), 3833-3841.
Persson, S., Wei, H.R., Milne, J., Page G.P. and Somerville, C.R. (2005) Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proceedings of the National Academy of Sciences of the United States of America, 102(24), 8633-8638.
Brown, D.M., Zeef, L.A.H., Ellis, J., Goodacre, R. and Turner, S.R. (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell, 17(8), 2281-2295.
Ding, S.Y. and Himmel, M.E. (2006) The maize primary cell wall microfibril: a new model derived from direct visualization. Journal of Agricultural and Food Chemistry, 54(3), 597-606.
Samuga, A. and Joshi, C.P. (2004) Differential expression patterns of two new primary cell wall-related cellulose synthase cDNAs, PtrCesA6 and PtrCesA7 from aspen trees. Gene, 334, 73-82.
Beeckman, T., Przemeck, G.K., Stamatiou, G., Lau, R., Terryn, N., De Rycke, R., Inze, D. and Berleth, T. (2002) Genetic complexity of cellulose synthase a gene function in Arabidopsis embryogenesis. Plant Physiology, 130(4), 1883-1893.
Gillmor, C.S., Poindexter, P., Lorieau, J., Palcic M.M. and Somerville, C. (2002) Alpha-glucosidase I is required for cellulose biosynthesis and morphogenesis in Arabidopsis. Journal of Cell Biology, 156(6), 1003-1013.
Williamson, R.E., Burn, J.E., Birch, R., Baskin, T.I., Arioli, T., Betzner A.S. and Cork, A. (2001) Morphology of rsw1, a cellulose-deficient mutant of Arabidopsis thaliana. Protoplasma, 215(1-4), 116-127.
Ellis, C., Karafyllidis, I., Wasternack, C. and Turner, J.G. (2002) The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell, 14(7), 1557-1566.
Kalluri, U.C. and Joshi, C.P. (2003) Isolation and characterization of a new, full-length cellulose synthase cDNA, PtrCesA5 from developing xylem of aspen trees. Journal of Experimental Botany, 54(390), 2187- 2188.
Kalluri, U.C. and Joshi, C.P. (2004) Differential expression patterns of two cellulose synthase genes are associated with primary and secondary cell wall development in aspen trees. Planta, 220(1), 47-55.
Pear, J.R., Kawagoe, Y., Schreckengost, W.E., Delmer, D.P. and Stalker, D.M. (1996) Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase," Proceedings of the National Academy of Sciences of the United States of America, 93(22), 12637-12642.
Liang, X. and Joshi, C.P. (2004) Molecular cloning of ten distinct hypervariable regions from the cellulose synthase gene superfamily in aspen trees. Tree Physiology, 24(5), 543-550.
Zhong, R., Morrison, W.H., 3rd, Freshour, G.D., Hahn, M.G. and Ye, Z.H. (2003) Expression of a mutant form of cellulose synthase AtCesA7 causes dominant negative effect on cellulose biosynthesis. Plant physiology, 132 (2), 786-795.
Bosca, S., Barton, C.J., Taylor, N.G., Ryden, P., Neumetzler, L., Pauly, M., Roberts, K. and Seifert, G.J. (2006) Interactions between MUR10/CesA7-dependent secondary cellulose biosynthesis and primary cell wall structure. Plant physiology, 142(4), 1353-1363.
Wang, J., Howles, P.A., Cork, A.H., Birch, R.J. and Williamson, R.E. (2006) Chimeric proteins suggest that the catalytic and/or C-terminal domains give CesA1 and CesA3 access to their specific sites in the cellulose synthase of primary walls. Plant Physiol, 142(2), 685- 695.