Analysis of cellulose synthase genes from domesticated apple identifies collinear genes WDR53 and CesA8A: partial co-expression, bicistronic mRNA, and alternative splicing of CESA8A

Abstract

Cellulose synthase (CesA) genes constitute a complex multigene family with six major phylogenetic clades in angiosperms. The recently sequenced genome of domestic apple, Malus×domestica, was mined for CesA genes, by blasting full-length cellulose synthase protein (CESA) sequences annotated in the apple genome against protein databases from the plant models Arabidopsis thaliana and Populus trichocarpa. Thirteen genes belonging to the six angiosperm CesA clades and coding for proteins with conserved residues typical of processive glycosyltransferases from family 2 were detected. Based on their phylogenetic relationship to Arabidopsis CESAs, as well as expression patterns, a nomenclature is proposed to facilitate further studies. Examination of their genomic organization revealed that MdCesA8-A is closely linked and co-oriented with WDR53, a gene coding for a WD40 repeat protein. The WDR53 and CesA8 genes display conserved collinearity in dicots and are partially co-expressed in the apple xylem. Interestingly, the presence of a bicistronic WDR53-CesA8A transcript was detected in phytoplasma-infected phloem tissues of apple. The bicistronic transcript contains a spliced intergenic sequence that is predicted to fold into hairpin structures typical of internal ribosome entry sites, suggesting its potential cap-independent translation. Surprisingly, the CesA8A cistron is alternatively spliced and lacks the zinc-binding domain. The possible roles of WDR53 and the alternatively spliced CESA8 variant during cellulose biosynthesis in M.×domestica are discussed.

WD40-Repeat Proteins in Plant Cell Wall Formation: Current Evidence and Research Prospects

“…Specifically, a plant WDR53 gene (represented by At5g45760 in Arabidopsis ) is collinear with the secondary cell wall CesA8 , while a WDR83 (At5g64730) is adjacent to the primary cell wall CesA6 (schematized in Figure 1D ). We showed that WDR53 and CesA8 are partially co-expressed in apple and Populus ( Guerriero et al, 2012 ). Further, we identified a bicistronic WDR53-CesA8 transcript in phytoplasma-infected apple tissues, where the CesA8 cistron is alternatively spliced and lacks a portion corresponding the RING-type zinc finger domain.…”

“…We have also showed that the genomic association between a WDR gene and a gene encoding a glycosyltransferase from family 2 (GT2) is a conserved feature in eukaryotes, since, besides dicots, it is reported in metazoans (hyaluronan synthase-WDR microsynteny) and in fungi (chitin synthase-WDR microsynteny; Guerriero et al, 2012 ). In fungi, the genomic collinearity between a chitin synthase ( chs ) and a WDR gene is conserved among several species (Guerriero et al, in revision).…”

“…We previously identified two cases of conserved genomic collinearity between a WDR gene and a CesA in the genomes of several dicots ( Guerriero et al, 2012 ). Specifically, a plant WDR53 gene (represented by At5g45760 in Arabidopsis ) is collinear with the secondary cell wall CesA8 , while a WDR83 (At5g64730) is adjacent to the primary cell wall CesA6 (schematized in Figure 1D ).…”

A WDR Gene Is a Conserved Member of a Chitin Synthase Gene Cluster and Influences the Cell Wall in Aspergillus nidulans

“…We show that FPWD , a gene coding for a WDR protein, is a conserved collinear genomic neighbor of chsD in Ascomycetes. The chsD and FPWD genes, together with a closely linked bf gene, are located within a cell wall metabolic gene cluster recently identified in Aspergilli [ 7 ]. The study identified the fungal wall gene cluster based on the predicted functions of conserved gene neighbors of chsD , which comprise a Chs activator, a myosin V, a GH17 cell wall glucanase, scw11, a serine/threonine kinase, and a type 2A protein phosphatase PP2A.…”

“…Previous results showed conserved genomic microsynteny and partial co-expression of a glycosyltransferase from family 2 (GT2, i.e., a cellulose synthase, CesA ) and a WDR gene in plants [ 6 , 7 ], and that the collinear arrangement of genes coding for a GT2 enzyme and a WDR protein is frequent in eukaryotes’ genomes. Here, we show that conserved collinearity of a GT2-WDR gene pair is also present in fungi, where a gene coding for a WDR protein is a conserved gene neighbor of a class IV chitin synthase ( chsD ).…”