Development Genes and Evolution

, Volume 214, Issue 2, pp 81–88

The evolutionary origin of animal cellulose synthase

  • Keisuke Nakashima
  • Lixy Yamada
  • Yutaka Satou
  • Jun-ichi Azuma
  • Nori Satoh
Short Communication

Abstract

Urochordates are the only animals that produce cellulose, a polysaccharide existing primarily in the extracellular matrices of plant, algal, and bacterial cells. Here we report a Ciona intestinalis homolog of cellulose synthase, which is the core catalytic subunit of multi-enzyme complexes where cellulose biosynthesis occurs. The Ciona cellulose synthase gene, Ci-CesA, is a fusion of a cellulose synthase domain and a cellulase (cellulose-hydrolyzing enzyme) domain. Both the domains have no animal homologs in public databases. Exploiting this fusion of atypical genes, we provided evidence of a likely lateral transfer of a bacterial cellulose synthase gene into the urochordate lineage. According to fossil records, this likely lateral acquisition of the cellulose synthase gene may have occurred in the last common ancestor of extant urochordates more than 530 million years ago. Whole-mount in situ hybridization analysis revealed the expression of Ci-CesA in C. intestinalis embryos, and the expression pattern of Ci-CesA was spatiotemporally consistent with observed cellulose synthesis in vivo. We propose here that urochordates may use a laterally acquired “homologous” gene for an analogous process of cellulose synthesis.

Keywords

Cellulose Urochordates Cellulose synthase gene Evolution Lateral gene transfer 

Supplementary material

supp.pdf (22 kb)
Supplementary material (PDF 66 KB)

References

  1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedGoogle Scholar
  2. Andersson JO, Roger AJ (2002) Evolutionary analyses of the small subunit of glutamate synthase: gene order conservation, gene fusions, and prokaryote-to-eukaryote lateral gene transfers. Eukaryot Cell 1:304–310CrossRefPubMedGoogle Scholar
  3. Blanton RL, Fuller D, Iranfar N, Grimson MJ, Loomis WF (2000) The cellulose synthase gene of Dictyostelium. Proc Natl Acad Sci USA 97:2391–2396CrossRefPubMedGoogle Scholar
  4. Brown JR (2003) Ancient horizontal gene transfer. Nat Rev Genet 4:121–132CrossRefPubMedGoogle Scholar
  5. Brown RM Jr (1996) The biosynthesis of cellulose. J Macromol Sci Pure Appl Chem A33:1345–1373Google Scholar
  6. Bushman F (2002) Lateral DNA transfer. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.Google Scholar
  7. Cameron CB, Garey JR, Swalla BJ (2000) Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla. Proc Natl Acad Sci USA 97:4469–4474PubMedGoogle Scholar
  8. Charnock SJ, Henrissat B, Davies GJ (2001) Three-dimensional structures of UDP sugar glycosyltransferases illuminate the biosynthesis of plant polysaccharides. Plant Physiol 125:527–531CrossRefPubMedGoogle Scholar
  9. Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, De Tomaso A, Davidson B, Di Gregorio A, Gelpke M, Goodstein DM et al. (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167CrossRefPubMedGoogle Scholar
  10. Delmer DP (1999) Cellulose biosynthesis: exciting times for a difficult field of study. Ann Rev Plant Physiol Plant Mol Biol 50:245–276CrossRefGoogle Scholar
  11. Felsenstein J (1993) PHYLIP (Phylogeny Inference Package) version 3.5c. http://evolution.genetics.washington.edu/phylip.html
  12. Gascuel O (1997) BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 14:685–695PubMedGoogle Scholar
  13. Gianguzza M, Dolcemascolo G (1980) Morphological and cytochemical investigations on the formation of the test during the embryonic development of Ciona intestinalis. Acta Embryol Morphol Exp (ns) 1:225–239Google Scholar
  14. Henrissat B, Davies G (1997) Structural and sequence-based classification of glycoside hydrolases. Curr Opin Struct Biol 7:637–644PubMedGoogle Scholar
  15. Hirose E, Kimura S, Itoh T, Nishikawa J (1999) Tunic of pyrosomas, doliolids and salps (Thaliacea, Urochordata): morphology and cellulosic components. Biol Bull 196:113–120Google Scholar
  16. Holder M, Roger AJ (2003) PUZZLEBOOT version 1.03. http://hades.biochem.dal.ca/Rogerlab/Software/software.html. Cited November 2003
  17. Kimura S, Itoh T (1996) New cellulose synthesizing complexes (terminal complexes) involved in animal cellulose biosynthesis in the tunicate Metandrocarpa uedai. Protoplasma 194:151–163Google Scholar
  18. Kimura S, Ohshima C, Hirose E, Nishikawa J, Itoh T (2001) Cellulose in the house of the appendicularian Oikopleura rufescens. Protoplasma 216:71–74PubMedGoogle Scholar
  19. Koivula A, Ruohonen L, Wohlfahrt G, Reinikainen T, Teeri TT, Piens K, Claeyssens M, Weber M, Vasella A, Becker D et al. (2002) The active site of cellobiohydrolase Cel6 from Trichoderma reesei: the roles of aspartic acids D221 and D175. J Am Chem Soc 124:10015–10024CrossRefPubMedGoogle Scholar
  20. Koski LB, Golding GB (2001) The closest BLAST hit is often not the nearest neighbor. J Mol Evol 52:540–542PubMedGoogle Scholar
  21. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580CrossRefPubMedGoogle Scholar
  22. Kurland CG (2000) Something for everyone. EMBO Rep 1:92–95CrossRefPubMedGoogle Scholar
  23. Lacalli TC (2002) Vetulicolians—are they deuterostomes? Chordates? BioEssays 24:208–211CrossRefPubMedGoogle Scholar
  24. Lawrence JG, Ochman H (2002) Reconciling the many faces of lateral gene transfer. Trends Microbiol 10:1–4CrossRefPubMedGoogle Scholar
  25. Marks DL, Dominguez M, Wu K, Pagano RE (2001) Identification of active site residues in glucosylceramide synthase. J Biol Chem 276:26492–26498CrossRefPubMedGoogle Scholar
  26. Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 99:12246–12251CrossRefPubMedGoogle Scholar
  27. Nobles DR, Romanovicz DK, Brown RM Jr (2001) Cellulose in cyanobacteria. Origin of vascular plant cellulose synthase? Plant Physiol 127:529–542CrossRefPubMedGoogle Scholar
  28. Rånby BG (1952) Physico-chemical investigations on animal cellulose (Tunicin). Ark Kemi 4:241–248Google Scholar
  29. Read SM, Bacic T (2002) Prime time for cellulose. Science 295:59–60PubMedGoogle Scholar
  30. Richmond PA (1991) Occurrence and functions of native cellulose. In: Haigler CH, Weimer PJ (eds) Biosynthesis and biodegradation of cellulose. Dekker, New York, pp 5–23Google Scholar
  31. Richmond TA, Somerville CR (2000) The cellulose synthase superfamily. Plant Physiol 124:495–498PubMedGoogle Scholar
  32. Rieppel O (1994) Homology, topology, and typology: the history of modern debates. In: Hall BK (eds) Homology: the hierarchical basis of comparative biology. Academic Press, LondonGoogle Scholar
  33. Roberts AW, Roberts EM, Delmer DP (2002) Cellulose synthase (CesA) genes in the green alga Mesotaenium caldariorum. Eukaryot Cell 1:847–855CrossRefPubMedGoogle Scholar
  34. Romling U (2002) Molecular biology of cellulose production in bacteria. Res Microbiol 153:205–212CrossRefPubMedGoogle Scholar
  35. Satoh N (2003) The ascidian tadpole larva: comparative molecular development and genomics. Nat Rev Genet 4:285–295CrossRefPubMedGoogle Scholar
  36. Satou Y, Satoh N (1997) posterior end mark 2 (pem-2), pem-4, pem-5 and pem-6: Maternal genes with localized mRNA in the ascidian embryo. Dev Biol 192:467–481CrossRefPubMedGoogle Scholar
  37. Satou Y, Yamada L, Mochizuki Y, Takatori N, Kawashima T, Sasaki A, Hamaguchi M, Awazu S, Yagi K, Sasakura Y et al. (2002a) A cDNA resource from the basal chordate Ciona intestinalis. Genesis 33:153–154CrossRefPubMedGoogle Scholar
  38. Satou Y, Takatori N, Fujiwara S, Nishikata T, Saiga H, Kusakabe T, Shin-I T, Kohara Y, Satoh N (2002b) Ciona intestinalis cDNA projects: expressed sequence tag analyses and gene expression profiles during embryogenesis. Gene 287:83–96PubMedGoogle Scholar
  39. Satou Y, Kawashima T, Kohara Y, Satoh N (2003) Large scale EST analyses in Ciona intestinalis: its application as northern blot analyses. Dev Genes Evol 213:314–318PubMedGoogle Scholar
  40. Saxena IM, Brown RM Jr (2000) Cellulose synthases and related enzymes. Curr Opin Plant Biol 3:523–531CrossRefPubMedGoogle Scholar
  41. Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504CrossRefPubMedGoogle Scholar
  42. Shu DG, Chen L, Han J, Zhang XL (2001) An early Cambrian tunicate from China. Nature 411:472–473CrossRefPubMedGoogle Scholar
  43. Stasinopoulos SJ, Fisher PR, Stone BA, Stanisich VA (1999) Detection of two loci involved in (1→3)-β-glucan (curdlan) biosynthesis by Agrobacterium sp. ATCC31749, and comparative sequence analysis of the putative curdlan synthase gene. Glycobiology 9:31–41CrossRefPubMedGoogle Scholar
  44. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedGoogle Scholar
  45. Tusnády GE, Simon I (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17:849–850CrossRefPubMedGoogle Scholar
  46. Villarreal LP, DeFilippis VR (2000) A hypothesis for DNA viruses as the origin of eukaryotic replication proteins. J Virol 74:7079–7084CrossRefPubMedGoogle Scholar
  47. Williamson RE, Burn JE, Hocart CH (2002) Towards the mechanism of cellulose synthesis. Trends Plant Sci 7:461–467CrossRefPubMedGoogle Scholar
  48. Zhang MQ (2002) Computational prediction of eukaryotic protein-coding genes. Nat Rev Genet 3:698–709CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Keisuke Nakashima
    • 1
  • Lixy Yamada
    • 2
  • Yutaka Satou
    • 2
  • Jun-ichi Azuma
    • 1
  • Nori Satoh
    • 2
  1. 1.Laboratory of Forest Biochemistry, Division of Environmental Science and Technology, Graduate School of AgricultureKyoto UniversityKyoto 606-8502Japan
  2. 2.Department of Zoology, Graduate School of ScienceKyoto UniversityKyoto 606-8502Japan

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