Functional specialization of cellulose synthase genes of prokaryotic origin in chordate larvaceans

Development

Volumn 137, Issue 9, 2010, Pages 1483-1492

  Sagane, Yoshimasa ^a   Zech, Karin ^a   Bouquet, Jean Marie ^a   Schmid, Martina ^a   Bal, Ugur ^a,c   Thompson, Eric M ^a,b  

^a Sars International Centre for Marine Molecular Biology   (Norway)

^b UNIVERSITY OF BERGEN   (Norway)

^c NAMIK KEMAL UNIVERSITY   (Turkey)

Author keywords

Appendicularian; Extracellular matrix; Lateral gene transfer; Metamorphosis; Notochord; Oikopleura; Tunicate

Indexed keywords

CELLULOSE; CELLULOSE SYNTHASE 1; CELLULOSE SYNTHASE 2; GLYCOSIDASE; SYNTHETASE; UNCLASSIFIED DRUG; CELLULOSE SYNTHASE; GLUCOSYLTRANSFERASE;

ARTICLE; ASCIDIACEA; CHORDATA; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FIBER; GENE EXPRESSION; HORIZONTAL GENE TRANSFER; KNOCKOUT GENE; MORPHOGENESIS; NONHUMAN; NOTOCHORD; OIKOPLEURA DIOICA; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; PROKARYOTE; PROTEIN DOMAIN; ANIMAL; CLASSIFICATION; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; MOLECULAR EVOLUTION; PRENATAL DEVELOPMENT; PROKARYOTIC CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

APPENDICULARIA (CLASS); ASCIDIA; ASCIDIACEA; CIONA; METAZOA; OIKOPLEURA; OIKOPLEURA DIOICA; PROKARYOTA; UROCHORDATA;

ANIMALS; CELLULOSE; CHORDATA; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; GLUCOSYLTRANSFERASES; IN SITU HYBRIDIZATION; PHYLOGENY; PROKARYOTIC CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 77951213056     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.044503     Document Type: Article

References (47)

1. Blanton, R. L., Fuller, D., Iranfar, N., Grimson, M. J. and Loomis, W. F. (2000). The cellulose synthase gene of Dictyostelium. Proc. Natl. Acad. Sci. USA 97, 2391-2396.
2. Bouquet, J.-M., Spriet, E., Troedsson, C., Otterå, H., Chourrout. D. and Thompson, E. M. (2009). Culture optimization for the emergent zooplanktonic model organism Oikopleura dioica. J. Plankton Res. 31, 359-370.
3. Brown, R. M., Jr (1996). The biosynthesis of cellulose. Pure Appl. Chem. 10, 1345-1373.
4. Brown, R. M., Jr (1999). Cellulose structure and biosynthesis. Pure Appl. Chem. 71, 767-776.
5. Brown, R. M., Jr and Montezinos, D. (1976). Cellulose microfibrils: visualization of biosynthetic and orienting complexes in association with the plasma membrane. Proc. Natl. Acad. Sci. USA 73, 143-147.
6. Brown, R. M., Jr, Willison, J. H. and Richardson, C. L. (1976). Cellulose biosynthesis in Acetobacter xylinum: visualization of the site of synthesis and direct measurement of the in vivo process. Proc. Natl. Acad. Sci. USA 73, 4565-4569.
7. Clarke, T., Bouquet, J.-M., Fu, X., Kallesøe, T. and Thompson, E. M. (2007). Rapidly evolving lamins in a chordate, Oikopleura dioica, with unusual nuclear architecture. Gene 396, 159-169. (Pubitemid 46818787)
8. Davidson, A. and Blaxter, M. (2005). Ancient origin of glycosyl hydrolase family 9 cellulase genes. Mol. Biol. Evol. 22, 1273-1284.
9. Delmer, D. P. (1999). Cellulose biosynthesis: exciting times for a difficult field of study. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 245-276. (Pubitemid 129491963)
10. Delsuc, F., Brinkmann, H., Chourrout, D. and Philippe, H. (2006). Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439, 965-968. (Pubitemid 43292413)
11. Delsuc, F., Tsagkogeorga, G., Lartillot, N. and Philippe, H. (2008). Additional molecular support for the new chordate phylogeny. Genesis 46, 592-604.
12. Ganot, P. and Thompson, E. M. (2002). Patterning through differential endoreduplication in epithelial organogenesis of the chordate, Oikopleura dioica. Dev. Biol. 252, 59-71. (Pubitemid 35373736)
13. Garstang, W. (1928). The morphology of the Tunicata, and its bearings on the phylogeny of the Chordata. Q. J. Microsc. Sci. 72, 51-187.
14. Hirose, E., Kimura, S., Itoh, T. and Nishikawa, J. (1999). Tunic morphology and cellulose components of pyrosomas, doliolids, and salps (thaliacea, urochordate). Biol. Bull. 196, 113-120.
15. Itoh, T. (1990). Cellulose-synthesizing complexes in some giant marine algae. J. Cell Sci. 95, 309-319. (Pubitemid 20067651)
16. Jones, D. T., Taylor, W. R. and Thornton, J. M. (1992). The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8, 275-282.
17. Kimura, S. and Ito, T. (1996). New cellulose-synthesizing complexes (=terminal complexes) involved in animal cellulose biosynthesis in the tunicate, Metandrocarpa uedai. Protoplasma 194, 151-163. (Pubitemid 27012684)
18. Kimura, S. and Itoh, T. (2004). Cellulose synthesizing terminal complexes on the ascidians. Cellulose 11, 377-383.
19. Kimura, S., Ohshima, C., Hirose, E., Nishikawa, J. and Itoh, T. (2001). Cellulose in the house of the appendicularian Oikopleura rufescens. Protoplasma 216, 71-74. (Pubitemid 32324697)
20. Koivula, A., Ruohonen, L., Wohlfahrt, G., Reinikainen, T., Teeri, T. T., Piens, K., Claeyssens, M., Weber, M., Vasella, A., Becker, D. et al.(2002). The active site of cellobiohydrolase Cel6A from Trichoderma reesei: the roles of aspartic acids D221 and D175. J. Am. Chem. Soc. 124, 10015-10024. (Pubitemid 34919737)
21. Krogh, A., Larsson, B., von Heijne, G. and Sonnhammer, E. L. L. (2001). Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567-580. (Pubitemid 33032862)
22. Lacalli, T. C. (2005). Protochordate body plan and the evolutionary role of larvae: Old controversies resolved? Can. J. Zool. 83, 216-224.
23. Matthysse, A. G. (1983). Role of bacterial cellulose fibrils in Agrobacterium tumefaciens infection. J. Bacteriol. 154, 906-915.
24. Matthysse, A. G., Deschet, K., Williams, M., Marry, M., White, A. R. and Smith, W. C. (2004). A functional cellulose synthase from ascidian epidermis. Proc. Natl. Acad. Sci. USA 101, 986-991. (Pubitemid 38160571)
25. Nakashima, K., Yamada, L., Satou, Y., Azuma, J. and Satoh, N. (2004). The evolutionary origin of animal cellulose synthase. Dev. Genes Evol. 214, 81-88. (Pubitemid 38324957)
26. Nakayama-Ishimura, A., Chambon, J. P., Horie, T., Satoh, N. and Sasakura, Y. (2009). Delineating metamorphic pathways in the ascidian Ciona intestinalis. Dev. Biol. 326, 357-367.
27. Nicol, F., His, I., Jauneau, A., Vernhettes, S., Canut, H. and Höfte, H. (1998). A plasmamembrane-bound putative endo-1,4-beta-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J. 17, 5563-5576. (Pubitemid 28445968)
28. Nielsen, C. (1999). Origin of the chordate central nervous system - and the origin of the chordates. Dev. Genes. Evol. 209, 198-205. (Pubitemid 29116597)
29. Paredez, A. R., Somerville, C. R. and Ehrhardt, D. W. (2006). Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491-1495.
30. Pedersen, A. G. and Nielsen, H. (1997). Neural network prediction of translation initiation sites in eukaryotes: perspectives for EST and genome analysis. Proc. Int. Conf. Intell. Syst. Mol. Biol. 5, 225-233.
31. Römling, U. (2002). Molecular biology of cellulose production in bacteria. Res. Microbiol. 153, 205-212.
32. Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574. (Pubitemid 37038874)
33. Rouvinen, J., Bergfors, T., Teeri, T., Knowles, J. K. C. and Jones, T. A. (1990). Three-dimensional structure of cellobiohydrolase II from Trichoderma reesei. Science 249, 380-386. (Pubitemid 20248863)
34. Sasakura, Y., Nakashima, K., Awazu, S., Matsuoka, T., Nakayama, A., Azuma, J.-I. and Satoh, N. (2005). Transposon-mediated insertional mutagenesis revealed the functions of animal cellulose synthase in the ascidian Ciona intestinalis. Proc. Natl. Acad. Sci. USA 102, 15134-15139. (Pubitemid 41513347)
35. Satoh, N. (2009). An advanced filter-feeder hypothesis for urochordate evolution. Zool. Sci. 26, 97-111.
36. Seo, H.-C., Edvardsen, R. B., Maeland, A. D., Bjordal, M., Jensen, M. F., Hansen, A., Flaat, M., Weissenbach, J., Lehrach, H., Wincker, P. et al. (2004). Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 431, 67-71. (Pubitemid 39215108)
37. Smith, G., Swart, S., Lugtenberg, B. J. J. and Kijne, J. W. (1992). Molecular mechanisms of attachment of Rhizobium bacteria to plant roots. Mol. Microbiol. 6, 2897-2903.
38. Smith, L. G. and Oppenheimer, D. G. (2005). Spatial control of cell expansion by the plant cytoskeleton. Annu. Rev. Cell. Dev. Biol. 21, 271-295. (Pubitemid 41740636)
39. Spada, F., Steen, H., Troedsson, C., Kallesoe, T., Spriet, E., Mann, M. and Thompson, E. M. (2001). Molecular patterning of the oikoplastic epithelium of the larvacean tunicate Oikopleura dioica. J. Biol. Chem. 276, 20624-20632. (Pubitemid 37411150)
40. Stach, T. (2008a). Chordate phylogeny and evolution: a not so simple three taxon problem. J. Zool. 276, 117-141.
41. Stach, T. (2008b). Anatomy of the trunk mesoderm in tunicates: homology considerations and phylogenetic interpretation. Zoomorphology 126, 203-214.
42. Stone, B. (2005). Cellulose: structure and distribution. In Encyclopedia of Life Sciences. Chichester: John Wiley & Sons. http://www.els.net/ (doi: 10.1038/npg.els.0003892).
43. Thompson, E. M., Kallesøe, T. and Spada, F. (2001). Diverse genes expressed in distinct regions of the trunk epithelium define a monolayer cellular template for construction of the oikopleurid house. Dev. Biol. 238, 260-273. (Pubitemid 32977295)
44. Wada, H. (1998). Evolutionary history of free-swimming and sessile lifestyles in urochordates as deduced from 18S rDNA molecular phylogeny. Mol. Biol. Evol. 15, 1189-1194.
45. Wada, H. and Satoh, N. (1994). Details of the evolutionary history from invertebrates to vertebrates, as deduced from the sequences of 18S rDNA. Proc. Natl. Acad. Sci. USA 91, 1801-1804. (Pubitemid 24080293)
46. Williams, W. S. and Cannon, R. E. (1989). Alternative environmental roles for cellulose produced by Acetobacter xylinum. Appl. Environ. Microbiol. 55, 2448-2452.
47. Xu, H., Chater, K. F., Deng, Z. and Tao, M. (2008). A cellulose synthase-like protein involved in hyphal tip growth and morphological differentiation in Streptomyces. J. Bacteriol. 190, 4971-4978. (Pubitemid 351991065)