A survey of plant and algal genomes and transcriptomes reveals new insights into the evolution and function of the cellulose synthase superfamily

Abstract

BackgroundEnzymes of the cellulose synthase (CesA) family and CesA-like (Csl) families are responsible for the synthesis of celluloses and hemicelluloses, and thus are of great interest to bioenergy research. We studied the occurrences and phylogenies of CesA/Csl families in diverse plants and algae by comprehensive data mining of 82 genomes and transcriptomes.ResultsWe found that 1) charophytic green algae (CGA) have orthologous genes in CesA, CslC and CslD families; 2) liverwort genes are found in the CesA, CslA, CslC and CslD families; 3) The fern Pteridium aquilinum not only has orthologs in these conserved families but also in the CslB, CslH and CslE families; 4) basal angiosperms, e.g. Aristolochia fimbriata, have orthologs in these families too; 5) gymnosperms have genes forming clusters ancestral to CslB/H and to CslE/J/G respectively; 6) CslG is found in switchgrass and basal angiosperms; 7) CslJ is widely present in dicots and monocots; 8) CesA subfamilies have already diversified in ferns.ConclusionsWe speculate that: (i) ferns and horsetails might both have CslH enzymes, responsible for the synthesis of mixed-linkage glucans and (ii) CslD and similar genes might be responsible for the synthesis of mannans in CGA. Our findings led to a more detailed model of cell wall evolution and suggested that gene loss played an important role in the evolution of Csl families. We also demonstrated the usefulness of transcriptome data in the study of plant cell wall evolution and diversity.

Evolution of the cell wall components during terrestrialization

“…Genes of the CesA family are supposed to be of the ancient cyanobacteria origin [17,26,29,30]. Results of the phylogenetic analyses showed that in CGA the CesA was a single gene, whereas already in basal land plants CesA formed a single monophyletic group of genes.…”

“…Results of the phylogenetic analyses showed that in CGA the CesA was a single gene, whereas already in basal land plants CesA formed a single monophyletic group of genes. Following, due to the duplication and diversification events, many different CesA subfamilies have evolved in the vascular plants before the divergence of ferns [24,26]. The functions of CesA genes were conserved during the evolution, from the cyanobacterial endosymbiont, by algae ancestors of land plants, to extant groups of Tracheophyta [26,31], indicating the significance of cellulose for development and functioning of all plants.…”

“…This polysaccharide is synthesized by the complexes of membrane proteins called cellulose synthase, also named terminal complexes (TCs), which include catalytic subunits encoded by the CesA family genes [24][25][26]. In seed plants, TCs form hetero-oligomeric rosettes, supposedly consist of 36 catalytic subunits that synthesize 36 cellulose chains forming a single microfibril [27], although recent studies suggest that plant microfibril can contain only 18-24 cellulose chains [28].…”

“…During evolution, CesA genes encoding the catalytic subunits of TCs were subjected to specialization [26], which in seed plants had occurred at least at two levels: first -specialization of entire complexes to cellulose biosynthesis for primary and secondary walls; second -diversification of CesA catalytic subunits within a single rosette and formation of hetero-oligomeric complexes [34]. The sequence of specialization events is a crucial aspect necessary for understanding the evolution of cellulose biosynthesis.…”

“…CesA genes, already in ferns, form many subfamilies, which contain genes orthologous to that of extant seed plants, including orthologs of AtCesA4, AtCesA7 and AtCesA8, involved in secondary cell wall formation in Arabidopsis [26,40]. The emergence of hetero-oligomeric complexes in a common ancestor of seed plants [27] suggests their importance for the origin and diversification of this group of plants and for functional specialization at the cellular and tissue level.…”