Cellulose synthase superfamily
From Purdue Genomics Database Facility
Alison Roberts, Department of Biological Sciences, University of Rhode Island, aroberts@uri.edu
Analysis of the CELLULOSE SYNTHASE (CESA) gene superfamily in Selaginella moellendorfii revealed many similarities with that of Physcomitrella patens (Roberts & Bushoven, 2007), including 1) absence of orthologs of the spermatophyte CESA genes that are specialized for primary and secondary cell wall biosynthesis, 2) presence of only three CELLULOSE SYNTHASE-LIKE (CSL) gene families, compared to seven or eight in spermatophytes (Hazen et al., 2002, Richmond & Somerville, 2000) and 3) presence of genes with similarity to cyanobacterial and red algal CESA genes, which are absent in spermatophytes. The CESA, CSLA, CSLC and CSLD gene families of S. moellendorfii are smaller than those of either P. patens or spermatophytes and phylogenetic analysis revealed that each of these families diversified independently within the bryomorph, lycopsid and spermatophyte lines. These observations provide insight into the specialization of cellulose synthases for primary and secondary cell wall biosynthesis, diversification of the CSL gene families, and the origin of rosette-forming cellulose synthases.
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Cellulose synthase (CESA) genes
The CESA gene superfamily took its name from the CESA genes, which encode the catalytic subunits of cellulose synthase (Richmond & Somerville, 2000). In Arabidopsis, the proteins encoded by three CESA genes are required for secondary cell wall biosynthesis in vascular tissue. Proteins encoded by three different CESA genes are required for primary cell wall biosynthesis (Doblin et al., 2002). All spermatophytes examined to date have orthologs of these six Arabidopsis CESA genes (Nairn & Haselkorn, 2005). Physcomitrella patens lacks orthologs of these specialized CESA genes, as might be expected for a non-vascular plant (Roberts & Bushoven, 2007). Surprisingly, these orthologs are also lacking in S. moellendorfii Media: CesA_tree.png, Media: Ces_rooted.gif indicating that CESA diversification and specialization for primary and secondary cell wall biosynthesis was not necessary for the evolution of vascular tissue.
Cellulose synthase-like (CSL) genes
The CESA gene superfamily also includes CSLA genes, which encode mannan synthases (Dhugga et al., 2004); CSLC genes, which putatively encode xyloglucan synthases (Cocuron et al., 2007); CSLF genes, which encode mixed-linkage beta-glucans; and five additional families of CSL genes, which have been proposed to encode the synthases that polymerize other cell wall polysaccharides (Richmond & Somerville, 2000). Only the CSLA, CSLC and CSLD gene families are represented in the genomes of P. patens (Roberts & Bushoven, 2007) and S. moellendorfii (Table 1). This indicates that the CSLB, CSLE, CSLF, CSLG and CSLH gene families, and presumably novel cell wall polysaccharides synthesized by their encoded proteins, originated after divergence of the lycopsids from the vascular plant lineage. Phylogenetic analysis revealed independent diversification of the CSLC Media:CslC_tree.png, Media:CslC_rooted.gif and CSLD Media:CslD_tree.png, Media:CslD_rooted.gif gene families within the bryomorph and lycopsid lineages. Selaginella moellendorfii has only one CSLA Media:CslA_tree.png, Media:CslA_rooted.gif. Thus, each of these CSL families may have been represented by a single gene in the common ancestor of lycopsids and moniliforms. It is also noteworthy that the CESA and CSL gene families are substantially smaller in S. moellendorfii than in either P. patens or spermatophytes (see Table of genes).
Genes with similarity to cyanobacterial and red algal cellulose synthase genes
The CESA genes of cyanobacteria (Nobles et al., 2001) and the red alga Porphyra yezoensis (Roberts and Robert, 2009) lack three defined regions that are conserved in streptophyte CESAs. Only the streptophyte-type CESA proteins are known to form rosette terminal complexes and the P. yezoensis CESA proteins form linear terminal complexes. In addition to seven streptophyte-type CESA sequences, P. patens has one gene that is similar to cyanobacterial and red algal CESAs and sequences from ascomycete fungi. Similar sequences are not found in spermatophytes, but were identified in the genome sequence of S. moellendorfii where they exist as a tandem duplicate and a group of four tandem genes. Of the 12 genes (including allelic variants), four are pseudogenes and one appears to be a fusion between GT2-5-2 and GT2-6-2 (see Table of genes).
Table of genes
Summary of CESA and CSL genes identified in S. moellendorfii with the number of genes (excluding pseudogenes) identified in the genomes of S. moellendorfii=Sm, P. patens= Pp (Roberts & Bushoven, 2007), Arabidopsis=At (Richmond & Somerville, 2000), rice=Os (Hazen et al., 2002); and Populus trichocarpa=Pt (Suzuki et al., 2006).
| Family | Sm gene | JGI protein ID | Sm | Pp | At | Os | Pt |
| CesA | CesA1-1
CesA1-2 CesA2-1 CesA2-2 CesA3-1 CesA3-2 CesA4-1 CesA4-2 Pseudogene Pseudogene | 141535
178958 73698 119123 75715 86720 163575 156278 235890 231191 | 4 | 7 | 10 | 8 | 18 |
| CslA | CslA1-1
CslA1-2 | 230176
178995 | 1 | 3 | 9 | 9 | 5 |
| CslB | - | - | 0 | 0 | 6 | 0 | 2 |
| CslC | CslC1-1
CslC1-2 CslC2-1 CslC2-2 | 442658
128946 140198 118058 | 2 | 6 | 5 | 6 | 5 |
| CslD | CslD1-1
CslD1-2 CslD2-1 CslD2-2 CslD3-1 CslD3-2 | 230382
427507 84069 120069 85326 417829 | 3 | 8 | 6 | 5 | 10 |
| CslE | - | - | 0 | 0 | 1 | 3 | 3 |
| CslF | - | - | 0 | 0 | 0 | 8 | 0 |
| CslG | - | - | 0 | 0 | 3 | 0 | 5 |
| CslH | - | - | 0 | 0 | 0 | 3 | 0 |
| Similar to red algal
and cyanobacterial cellulose synthase genes | GT2-1-1
GT2-1-2 GT2-2-1 pseudogene GT2-3-1 GT2-3-2 pseudogene pseudogene pseudogene GT2-5/6-2 GT2-6-1 | 452930
452933 452931 452934 452938 452928 452939 452929 452941 452932 452940 | 6 | 1 | 0 | 0 | 0 |
References
Cocuron, J. C., Lerouxel, O., Drakakaki, G., Alonso, A. P., Liepman, A. H., Keegstra, K., Raikhel, N. & Wilkerson, C. G. 2007. A gene from the cellulose synthase-like C family encodes a beta-1,4 glucan synthase. Proc Natl Acad Sci U S A 104:8550-5.
Dhugga, K. S., Barreiro, R., Whitten, B., Stecca, K., Hazebroek, J., Randhawa, G. S., Dolan, M., Kinney, A. J., Tomes, D., Nichols, S. & Anderson, P. 2004. Guar seed b-mannan synthase is a member of the cellulose synthase super gene family. Science 303:363-66.
Doblin, M. S., Kurek, I., Jacob-Wilk, D. & Delmer, D. P. 2002. Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol. 43:1407-20.
Hazen, S. P., Scott-Craig, J. S. & Walton, J. D. 2002. Cellulose synthase-like genes of rice. Plant Physiol 128:336-40.
Nairn, C. J. & Haselkorn, T. 2005. Three loblolly pine CesA genes expressed in developing xylem are orthologous to secondary cell wall CesA genes of angiosperms. New Phytol. 166:907-15.
Nobles, D. R., Romanovicz, D. K. & Brown, R. M., Jr. 2001. Cellulose in cyanobacteria. Origin of vascular plant cellulose synthase? Plant Physiol. 127:529-42.
Richmond, T. A. & Somerville, C. R. 2000. The cellulose synthase superfamily. Plant Physiol. 124:495-98.
Roberts, A. W. & Bushoven, J. T. 2007. The cellulose synthase (CESA) gene superfamily of the moss Physcomitrella patens. Plant Mol. Biol. 63:207-19.
Roberts, E. & Roberts, A. W. 2009. A cellulose synthase (CESA) gene from the red alga Porphyra yezoensis (Rhodophyta). J. Phycol. 45:203-212.
