Understanding plant cellulose synthases through a comprehensive investigation of the cellulose synthase family sequences

Frontiers in Plant Science

Volumn 2, Issue MAR, 2011, Pages

  Carroll, Andrew ^a,b   Specht, Chelsea D ^c  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cellulose; Cellulose synthase; Cellulose synthase superfamily; CesA; Comparative phylogenetics; CslD; CslF; Sequence based analysis

Indexed keywords

EID: 81255180288     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2011.00005     Document Type: Article

References (52)

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. Nucleic Acids Res. 25, 3389-3402.
2. Arabidopsis Genome Institute. (2000). Analysis of the genome sequence of the fowering plant Arabidopsis thal-iana. Nature 408, 796-815.
3. Baskin, T. I., Betzner, A. S., Hoggart, R., Cork, A., and Williamson, R. E. (1992). Root morphology mutants in Arabidopsis thaliana. Funct. Plant Biol. 19, 427-437.
4. Beeckman, T., Przemeck, G. K. H., 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 Physiol. 130, 1883-1893.
5. 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 Physiol. 142, 1353-1363.
6. Bowling, A. J., and Brown, R. M. (2008). The cytoplasmic domain of the cellulose-synthesizing complex in vascular plants. Protoplasma 233, 115-127.
7. Brown, R. M., and Montezinos, D. (1976). Cellulose microfbrils: visualization of biosynthetic and orienting complexes in association with the plasma membrane. Proc. Natl. Acad. Sci. U.S.A. 73, 143-147.
8. Burton, R. A., Wilson, S. M., Hrmova, M., Harvey, A. J., Shirley, N. J., Medhurst, A., Stone, B. A., Newbigin, E. J., Bacic, A., and Fincher, G. B. (2006). Cellulose synthase-like CslF genes mediate the synthesis of cell wall (1,3;1,4)-β-D-glucans. Science 311, 1940-1942.
9. Cano-Delgado, A. I., Metzlaff, K., and Bevan, M. W. (2000). The eli1 mutation reveals a link between cell expansion and secondary cell wall formation in Arabidopsis thaliana. Development 127, 3395-3405.
10. Carpita, N. C., and McCann, M. C. (2010). The maize mixed-linkage (1->3),(1->4)-β-D-glucan polysac-charide is synthesized at the Golgi membrane. Plant Physiol. 153, 1362-1371.
11. Chen, S., Ehrhardt, D. W., and Somerville, C. R. (2010). Mutations of cellulose synthase (CESA1) phosphorylation sites modulate anisotropic cell expansion and bidirectional mobility of cellulose synthase. Proc. Natl. Acad. Sci. U.S.A. 107, 17188-17193.
12. Chen, Z., Hong, X., Zhang, H., Wang, Y., Li, X., Zhu, J.-K., and Gong, Z. (2005). Disruption of the cellulose synthase gene, AtCesA8/IRX1, enhances drought and osmotic stress tolerance in Arabidopsis. Plant J. 43, 273-283.
13. Crooks, G. E., Hon, G., Chandonia, J.-M., and Brenner, S. E. (2004). WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190.
14. Crowell, E. F., Bischoff, V., Desprez, T., Rolland, A., Stierhof, Y.-D., Schumacher, K., Gonneau, M., Höfte, H., and Vernhettes, S. (2009). Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell 21, 1141-1154.
15. Daras, G., Rigas, S., Penning, B., Milioni, D., McCann, M. C., Carpita, N. C., Fasseas, C., and Hatzopoulos, P. (2009). The thanatos mutation in Arabidopsis thaliana cellulose synthase 3 (AtCesA3) has a dominant-negative effect on cellulose synthesis and plant growth. New Phytol. 184, 114-126.
16. Desnos, T., Orbovic, V., Bellini, C., Kronenberger, J., Caboche, M., Traas, J., and Hofte, H. (1996). Procuste1 mutants identify two distinct genetic pathways controlling hypocotyl cell elongation, respectively in dark- and light-grown Arabidopsis seedlings. Development 122, 683-693.
17. Desprez, T., Juraniec, M., Crowell, E. F., Jouy, H., Pochylova, Z., Parcy, F., Höfte, H., Gonneau, M., and Vernhettes, S. (2007). Organization of cellulose syn-thase complexes involved in primary cell wall synthesis in Arabidopsis thal-iana. Proc. Natl. Acad. Sci. U.S.A. 104, 15572-15577.
18. Desprez, T., Vernhettes, S., Fagard, M., Refrégier, G., Desnos, T., Aletti, E., Py, N., Pelletier, S., and Höfte, H. (2002). Resistance against herbicide isoxaben and cellulose defciency caused by distinct mutations in same cellulose syn-thase isoform CESA6. Plant Physiol. 128, 482-490.
19. Doblin, M. S., Kurek, I., Jacob-Wilk, D., and Delmer, D. P. (2002). Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol. 43, 1407-1420.
20. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797.
21. 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, 1557-1566.
22. Gillmor, C. S., Poindexter, P., Lorieau, J., Palcic, M. M., and Somerville, C. (2002). α-Glucosidase I is required for cellulose biosynthesis and morphogenesis in Arabidopsis. J. Cell Biol. 156, 1003-1013.
23. Goff, S. A., Ricke, D., Lan, T. H., Presting, G., Wang, R., Dunn, M., Glazebrook, J., Sessions, A., Oeller, P., Varma, H., Hadley, D., Hutchison, D., Martin, C., Katagiri, F., Lange, B. M., Moughamer, T., Xia, Y., Budworth, P., Zhong, J., Miguel, T., Paszkowski, U., Zhang, S., Colbert, M., Sun, W. L., Chen, L., Cooper, B., Park, S., Wood, T. C., Mao, L., Quail, P., Wing, R., Dean, R., Yu, Y., Zharkikh, A., Shen, R., Sahasrabudhe, S., Thomas, A., Cannings, R., Gutin, A., Pruss, D., Reid, J., Tavtigian, S., Mitchell, J., Eldredge, G., Scholl, T., Miller, R. M., Bhatnagar, S., Adey, N., Rubano, T., Tusneem, N., Robinson, R., Feldhaus, J., Macalma, T., Oliphant, A., and Briggs, S. (2002). A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296, 92-100.
24. Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704.
25. Gupta, S. K., Kececioglu, J. D., and Schäffer, A. A. (1995). Improving the practical space and time effciency of the shortest-paths approach to sum-of-pairs multiple sequence alignment. J. Comput. Biol. 2, 459-472.
26. Gutierrez, R., Lindeboom, J. J., Paredez, A. R., Emons, A. M. C., and Ehrhardt, D. W. (2009). Arabidopsis cortical micro-tubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase traffcking compartments. Nat. Cell Biol. 11, 797-806.
27. Haga, K., Kanai, R., Sakamoto, O., Aoyagi, M., Harata, K., and Yamane, K. (2003). Effects of essential carbohydrate/aromatic stacking interaction with Tyr100 and Phe259 on substrate binding of cyclodextrin glycosyltransferase from Alkalophilic Bacillus sp. 1011. J. Biochem. 134, 881-891.
28. Heazlewood, J. L., Durek, P., Hummel, J., Selbig, J., Weckwerth, W., Walther, D., and Schulze, W. X. (2008). PhosPhAt: a database of phosphorylation sites in Arabidopsis thaliana and a plant-specific phosphorylation site predictor. Nucleic Acids Res. 36, D1015-1021-D1015-1021.
29. Henikoff, S., and Henikoff, J. G. (1992). Amino acid substitution matrices from protein blocks. Proc. Natl. Acad. Sci. U.S.A. 89, 10915-10919.
30. Jaillon, O., Aury, J. M., Noel, B., Policriti, A., Clepet, C., Casagrande, A., Choisne, N., Aubourg, S., Vitulo, N., Jubin, C., Vezzi, A., Legeai, F., Hugueney, P., Dasilva, C., Horner, D., Mica, E., Jublot, D., Poulain, J., Bruyère, C., Billault, A., Segurens, B., Gouyvenoux, M., Ugarte, E., Cattonaro, F., Anthouard, V., Vico, V., Del Fabbro, C., Alaux, M., Di Gaspero, G., Dumas, V., Felice, N., Paillard, S., Juman, I., Moroldo, M., Scalabrin, S., Canaguier, A., Le Clainche, I., Malacrida, G., Durand, E., Pesole, G., Laucou, V., Chatelet, P., Merdinoglu, D., Delledonne, M., Pezzotti, M., Lecharny, A., Scarpelli, C., Artiguenave, F., Pè, M. E., Valle, G., Morgante, M., Caboche, M., Adam-Blondon, A. F., Weissenbach, J., Quétier, F., Wincker, P., and French-Italian Public Consortium for Grapevine Genome Characterization. (2007). The grapevine genome sequence suggests ancestral hexa-ploidization in major angiosperm phyla. Nature 449, 463-467.
31. Paterson, A. H., Bowers, J. E., Bruggmann, R., Dubchak, I., Grimwood, J., Gundlach, H., Haberer, G., Hellsten, U., Mitros, T., Poliakov, A., Schmutz, J., Spannagl, M., Tang, H., Wang, X., Wicker, T., Bharti, A. K., Chapman, J., Feltus, F. A., Gowik, U., Grigoriev, I. V., Lyons, E., Maher, C. A., Martis, M., Narechania, A., Otillar, R. P., Penning, B. W., Salamov, A. A., Wang, Y., Zhang, L., Carpita, N. C., Freeling, M., Gingle, A. R., Hash, C. T., Keller, B., Klein, P., Kresovich, S., McCann, M. C., Ming, R., Peterson, D. G., Mehboob-ur-Rahman, Ware, D., Westhoff, P., Mayer, K. F., Messing, J., and Rokhsar, D. S. (2009). The Sorghum bicolor genome and the diversification of grasses. Nature 457, 551-556.
32. 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 cel lulose synthase. Proc. Natl. Acad. Sci. U.S.A. 93, 12637-12642.
33. Persson, B., and Argos, P. (1994). Prediction of transmembrane segments in proteins utilising multiple sequence alignments. J. Mol. Biol. 237, 182-192.
34. Persson, S., Paredez, A., Carroll, A., Palsdottir, H., Doblin, M., Poindexter, P., Khitrov, N., Auer, M., and Somerville, C. R. (2007). Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 104, 15566-15571.
35. Popper, Z. A. (2008). Evolution and diversity of green plant cell walls. Curr. Opin. Plant Biol. 11, 286-292.
36. Rensing, S. A., Lang, D., Zimmer, A. D., Terry, A., Salamov, A., Shapiro, H., Nishiyama, T., Perroud, P. F., Lindquist, E. A., Kamisugi, Y., Tanahashi, T., Sakakibara, K., Fujita, T., Oishi, K., Shini, T., Kuroki, Y., Toyoda, A., Suzuki, Y., Hashimoto, S., Yamaguchi, K., Sugano, S., Kohara, Y., Fujiyama, A., Anterola, A., Aoki, S., Ashton, N., Barbazuk, W. B., Barker, E., Bennetzen, J. L., Blankenship, R., Cho, S. H., Dutcher, S. K., Estelle, M., Fawcett, J. A., Gundlach, H., Hanada, K., Heyl, A., Hicks, K. A., Hughes, J., Lohr, M., Mayer, K., Melkozernov, A., Murata, T., Nelson, D. R., Pils, B., Prigge, M., Reiss, B., Renner, T., Rombauts, S., Rushton, P. J., Sanderfoot, A., Schween, G., Shiu, S. H., Stueber, K., Theodoulou, F. L., Tu, H., Van de Peer, Y., Verrier, P. J., Waters, E., Wood, A., Yang, L., Cove, D., Cuming, A. C., Hasebe, M., Lucas, S., Mishler, B. D., Reski, R., Grigoriev, I. V., Quatrano, R. S., and Boore, J. L. (2008). The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319, 64-69.
37. Rice, P., Longden, I., and Bleasby, A. (2000). EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16, 276-277.
38. Scheible, W. R., Eshed, R., Richmond, T., Delmer, D., and Somerville, C. (2001). Modifcations of cellulose synthase confer resistance to isoxaben and thia-zolidinone herbicides in Arabidopsis Ixr1 mutants. Proc. Natl. Acad. Sci. U.S.A. 98, 10079-10084.
39. Schnable, P. S., Ware, D., Fulton, R. S., Stein, J. C., Wei, F., Pasternak, S., Liang, C., Zhang, J., Fulton, L., Graves, T. A., Minx, P., Reily, A. D., Courtney, L., Kruchowski, S. S., Tomlinson, C., Strong, C., Delehaunty, K., Fronick, C., Courtney, B., Rock, S. M., Belter, E., Du, F., Kim, K., Abbott, R. M., Cotton, M., Levy, A., Marchetto, P., Ochoa, K., Jackson, S. M., Gillam, B., Chen, W., Yan, L., Higginbotham, J., Cardenas, M., Waligorski, J., Applebaum, E., Phelps, L., Falcone, J., Kanchi, K., Thane, T., Scimone, A., Thane, N., Henke, J., Wang, T., Ruppert, J., Shah, N., Rotter, K., Hodges, J., Ingenthron, E., Cordes, M., Kohlberg, S., Sgro, J., Delgado, B., Mead, K., Chinwalla, A., Leonard, S., Crouse, K., Collura, K., Kudrna, D., Currie, J., He, R., Angelova, A., Rajasekar, S., Mueller, T., Lomeli, R., Scara, G., Ko, A., Delaney, K., Wissotski, M., Lopez, G., Campos, D., Braidotti, M., Ashley, E., Golser, W., Kim, H., Lee, S., Lin, J., Dujmic, Z., Kim, W., Talag, J., Zuccolo, A., Fan, C., Sebastian, A., Kramer, M., Spiegel, L., Nascimento, L., Zutavern, T., Miller, B., Ambroise, C., Muller, S., Spooner, W., Narechania, A., Ren, L., Wei, S., Kumari, S., Faga, B., Levy, M. J., McMahan, L., Van Buren, P., Vaughn, M. W., Ying, K., Yeh, C. T., Emrich, S. J., Jia, Y., Kalyanaraman, A., Hsia, A. P., Barbazuk, W. B., Baucom, R. S., Brutnell, T. P., Carpita, N. C., Chaparro, C., Chia, J. M., Deragon, J. M., Estill, J. C., Fu, Y., Jeddeloh, J. A., Han, Y., Lee, H., Li, P., Lisch, D. R., Liu, S., Liu, Z., Nagel, D. H., McCann, M. C., SanMiguel, P., Myers, A. M., Nettleton, D., Nguyen, J., Penning, B. W., Ponnala, L., Schneider, K. L., Schwartz, D. C., Sharma, A., Soderlund, C., Springer, N. M., Sun, Q., Wang, H., Waterman, M., Westerman, R., Wolfgruber, T. K., Yang, L., Yu, Y., Zhang, L., Zhou, S., Zhu, Q., Bennetzen, J. L., Dawe, R. K., Jiang, J., Jiang, N., Presting, G. G., Wessler, S. R., Aluru, S., Martienssen, R. A., Clifton, S. W., McCombie, W. R., Wing, R. A., and Wilson, R. K. (2009). The B73 maize genome: complexity, diversity, and dynamics. Science 326, 1112-1115.
40. Somerville, C. (2006). Cellulose synthesis in higher plants. Annu. Rev. Cell Dev. Biol. 22, 53-78.
41. Stork, J., Harris, D., Griffths, J., Williams, B., Beisson, F., Li-Beisson, Y., Mendu, V., Haughn, G., and Debolt, S. (2010). Cellulose Synthase9 serves a nonre-dundant role in secondary cell wall synthesis in Arabidopsis epidermal testa cells. Plant Physiol. 153, 580-589.
42. 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 Physiol. 133, 73-83.
43. Taylor, N. G. (2007). Identifcation of cellulose synthase AtCesA7 (IRX3) in vivo phosphorylation sites-a potential role in regulating protein degradation. Plant Mol. Biol. 64, 161-171.
44. 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. Proc. Natl. Acad. Sci. U.S.A. 100, 1450-1455.
45. Taylor, N. G., Laurie, S., and Turner, S. (2000). Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell 12, 2529-2540.
46. 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 syn-thase required for secondary cell wall synthesis. Plant Cell 11, 769-780.
47. Tuskan, G. A., Difazio, S., Jansson, S., Bohlmann, J., Grigoriev, I., Hellsten, U., Putnam, N., Ralph, S., Rombauts, S., Salamov, A., Schein, J., Sterck, L., Aerts, A., Bhalerao, R. R., Bhalerao, R. P., Blaudez, D., Boerjan, W., Brun, A., Brunner, A., Busov, V., Campbell, M., Carlson, J., Chalot, M., Chapman, J., Chen, G. L., Cooper, D., Coutinho, P. M., Couturier, J., Covert, S., Cronk, Q., Cunningham, R., Davis, J., Degroeve, S., Déjardin, A., Depamphilis, C., Detter, J., Dirks, B., Dubchak, I., Duplessis, S., Ehlting, J., Ellis, B., Gendler, K., Goodstein, D., Gribskov, M., Grimwood, J., Groover, A., Gunter, L., Hamberger, B., Heinze, B., Helariutta, Y., Henrissat, B., Holligan, D., Holt, R., Huang, W., Islam-Faridi, N., Jones, S., Jones-Rhoades, M., Jorgensen, R., Joshi, C., Kangasjärvi, J., Karlsson, J., Kelleher, C., Kirkpatrick, R., Kirst, M., Kohler, A., Kalluri, U., Larimer, F., Leebens-Mack, J., Leplé, J. C., Locascio, P., Lou, Y., Lucas, S., Martin, F., Montanini, B., Napoli, C., Nelson, D. R., Nelson, C., Nieminen, K., Nilsson, O., Pereda, V., Peter, G., Philippe, R., Pilate, G., Poliakov, A., Razumovskaya, J., Richardson, P., Rinaldi, C., Ritland, K., Rouzé, P., Ryaboy, D., Schmutz, J., Schrader, J., Segerman, B., Shin, H., Siddiqui, A., Sterky, F., Terry, A., Tsai, C. J., Uberbacher, E., Unneberg, P., Vahala, J., Wall, K., Wessler, S., Yang, G., Yin, T., Douglas, C., Marra, M., Sandberg, G., Van de Peer, Y., and Rokhsar, D. (2006). The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313, 1596-1604.
48. 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 specifc sites in the cellulose synthase of primary walls. Plant Physiol. 142, 685-695.
49. Wang, L., Guo, K., Li, Y., Tu, Y., Hu, H., Wang, B., Cui, X., and Peng, L. (2010). Expression profling and integrative analysis of the CESA/CSL superfamily in rice. BMC Plant Biol. 10, 282. doi: 10.1186/1471-2229-10-282
50. Yin, Y., Huang, J., and Xu, Y. (2009). The cellulose synthase superfamily in fully sequenced plants and algae. BMC Plant Biol. 9, 99-99. doi: 10.1186/1471-2229-9-99
51. Zhang, B., Deng, L., Qian, Q., Xiong, G., Zeng, D., Li, R., Guo, L., Li, J., and Zhou, Y. (2009). A missense mutation in the transmembrane domain of CESA4 affects protein abundance in the plasma membrane and results in abnormal cell wall biosynthesis in rice. Plant Mol. Biol. 71, 509-524.
52. Zhong, R., Morrison, W. H., 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 Physiol. 132, 786-795.