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

Abstract

SUMMARYExtracellular matrices play important, but poorly investigated, roles in morphogenesis. Extracellular cellulose is central to regulation of pattern formation in plants, but among metazoans only tunicates are capable of cellulose biosynthesis. Cellulose synthase (CesA) gene products are present in filter-feeding structures of all tunicates and also regulate metamorphosis in the ascidian Ciona. Ciona CesA is proposed to have been acquired by lateral gene transfer from a prokaryote. We identified two CesA genes in the sister-class larvacean Oikopleura dioica. Each has a mosaic structure of a glycoslyltransferase 2 domain upstream of a glycosyl hydrolase family 6 cellulase-like domain, a signature thus far unique to tunicates. Spatial-temporal expression analysis revealed that Od-CesA1 produces long cellulose fibrils along the larval tail, whereas Od-CesA2 is responsible for the cellulose scaffold of the postmetamorphic filter-feeding house. Knockdown of Od-CesA1 inhibited cellulose production in the extracellular matrix of the larval tail. Notochord cells either failed to align or were misaligned, the tail did not elongate properly and tailbud embryos also exhibited a failure to hatch. Knockdown of Od-CesA2 did not elicit any of these phenotypes and instead caused a mild delay in pre-house formation. Phylogenetic analyses including Od-CesAs indicate that a single lateral gene transfer event from a prokaryote at the base of the lineage conferred biosynthetic capacity in all tunicates. Ascidians possess one CesA gene, whereas duplicated larvacean genes have evolved distinct temporal and functional specializations. Extracellular cellulose microfibrils produced by the premetamorphic Od-CesA1 duplicate have a role in notochord and tail morphogenesis.

Germline Transformation in the Ascidian Ciona intestinalis

“…38.1a ), which surrounds the body to protect it from predators. In larvaceans, cellulose is found in the 'house,' which acts as a fi lter for collecting small particles in the seawater to feed (Sagane et al 2010 ). The swimming juvenile mutants of C. intestinalis have a malformed and soft tunic compared to that of wild types, suggesting that cellulose gives tunics the physical strength to withstand attack from predators.…”

Evolutionary crossroads in developmental biology: the tunicates

“…It can be bred in the laboratory, has an extremely short life cycle (4 days), and is not seasonal (Nishida, 2008). Its embryos are small (65-75 m) and transparent and can be microinjected with antisense morpholino oligonucleotides (Sagane et al, 2010).…”

“…It can be bred in the laboratory, has an extremely short life cycle (4 days), and is not seasonal (Nishida, 2008). Its embryos are small (65-75 m) and transparent and can be microinjected with antisense morpholino oligonucleotides (Sagane et al, 2010).The embryos of thaliaceans can only be obtained in small numbers and have received little attention since the 1960s. No established experimental protocols exist to collect or study the development of these embryos, and few molecular data have been collected.…”

Microarray Glycan Profiling Reveals Algal Fucoidan Epitopes in Diverse Marine Metazoans

“…The most remarkable example is tunicin-a cellulose-like compound present in tunicates. Synthesis of tunicin in tunicates is supposedly the result of a horizontal gene transfer event dating to ∼300 million years ago (Belton et al, 1989;Nakashima et al, 2004;Sagane et al, 2010).…”