Abstract
Extensins are plant cell wall glycoproteins that act as scaffolds for the deposition of the main wall carbohydrate polymers, which are interlocked into the supramolecular wall structure through intra- and inter-molecular iso-di-tyrosine crosslinks within the extensin backbone. In the conserved canonical extensin repeat, Ser-Hyp4, serine and the consecutive C4-hydroxyprolines (Hyps) are substituted with an α-galactose and 1–5 β- or α-linked arabinofuranoses (Arafs), respectively. These modifications are required for correct extended structure and function of the extensin network. Here, we identified a single Arabidopsis thaliana gene, At3g57630, in clade E of the inverting Glycosyltransferase family GT47 as a candidate for the transfer of Araf to Hyp-arabinofuranotriose (Hyp-β1,4Araf-β1,2Araf-β1,2Araf) side chains in an α-linkage, to yield Hyp-Araf4 which is exclusively found in extensins. T-DNA knock-out mutants of At3g57630 showed a truncated root hair phenotype, as seen for mutants of all hitherto characterized extensin glycosylation enzymes; both root hair and glycan phenotypes were restored upon reintroduction of At3g57630. At3g57630 was named Extensin Arabinose Deficient transferase, ExAD, accordingly. The occurrence of ExAD orthologs within the Viridiplantae along with its’ product, Hyp-Araf4, point to ExAD being an evolutionary hallmark of terrestrial plants and charophyte green algae.
Highlights
Protein O-linked glycans in animal and plant cells surround the cell where they function as a surface protectant[1,2,3,4]
The RRA β-arabinosyltransferases in GT77 clade A were discovered by a comparative phylogenetic approach, which relied on the co-existence in this clade of terrestrial plant and C. reinhardtii genes, which we hypothesized to be involved in coat protein glycosylation
The comparative phylogenetic approach used to identify the RRA genes relied on the fact that both Arabidopsis thaliana and C. reinhardtii feature Hyp-Araf[2] in their cell walls and that both species are represented in the A-clade of GT7723
Summary
Protein O-linked glycans in animal and plant cells surround the cell where they function as a surface protectant[1,2,3,4] One group of such O-glycoproteins in plants is the extensins, which define a subgroup of the hydroxyproline rich glycoprotein (HRGP) superfamily and incorporate characteristic β-L-arabinofuranoside repetitive glycosylation motifs[5,6,7]. Elongation of Hyp-Araf[3] with α-linked arabinose in CGAs and terrestrial plants seems to be confined to clustered proline arabinosylation of extensin substrates, and regulated . We report the identification of an extensin specific α-arabinosyltransferase, named ExAD, that extends Hyp-Araf[3] to Hyp-Araf[4] and map the occurrence within Viridiplantae of ExAD orthologs and its product, Hyp-Araf[4], which appears to be hallmark of terrestrial plant and CGA cell wall extensins. The evolution of ExAD and its product Hyp-Araf[4] is addressed and discussed
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