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. 2012 Dec 11:12:235.
doi: 10.1186/1471-2229-12-235.

Endo-(1,4)-β-glucanase gene families in the grasses: temporal and spatial co-transcription of orthologous genes

Margaret Buchanan  1 , Rachel A Burton, Kanwarpal S Dhugga, Antoni J Rafalski, Scott V Tingey, Neil J Shirley, Geoffrey B Fincher
Affiliations

Endo-(1,4)-β-glucanase gene families in the grasses: temporal and spatial co-transcription of orthologous genes

Margaret Buchanan et al. BMC Plant Biol. .

Abstract

Background: Endo-(1,4)-β-glucanase (cellulase) glycosyl hydrolase GH9 enzymes have been implicated in several aspects of cell wall metabolism in higher plants, including cellulose biosynthesis and degradation, modification of other wall polysaccharides that contain contiguous (1,4)-β-glucosyl residues, and wall loosening during cell elongation.

Results: The endo-(1,4)-β-glucanase gene families from barley (Hordeum vulgare), maize (Zea mays), sorghum (Sorghum bicolor), rice (Oryza sativa) and Brachypodium (Brachypodium distachyon) range in size from 23 to 29 members. Phylogenetic analyses show variations in clade structure between the grasses and Arabidopsis, and indicate differential gene loss and gain during evolution. Map positions and comparative studies of gene structures allow orthologous genes in the five species to be identified and synteny between the grasses is found to be high. It is also possible to differentiate between homoeologues resulting from ancient polyploidizations of the maize genome. Transcript analyses using microarray, massively parallel signature sequencing and quantitative PCR data for barley, rice and maize indicate that certain members of the endo-(1,4)-β-glucanase gene family are transcribed across a wide range of tissues, while others are specifically transcribed in particular tissues. There are strong correlations between transcript levels of several members of the endo-(1,4)-β-glucanase family and the data suggest that evolutionary conservation of transcription exists between orthologues across the grass family. There are also strong correlations between certain members of the endo-(1,4)-β-glucanase family and other genes known to be involved in cell wall loosening and cell expansion, such as expansins and xyloglucan endotransglycosylases.

Conclusions: The identification of these groups of genes will now allow us to test hypotheses regarding their functions and joint participation in wall synthesis, re-modelling and degradation, together with their potential role in lignocellulose conversion during biofuel production from grasses and cereal crop residues.

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Figures

Figure 1
Figure 1
A phylogenetic tree of the endo-(1,4)-β-glucanases of cereals and Arabidopsis. Included on this tree are barley (blue), maize (green), rice (purple), sorghum (tan), Brachypodium (black) and Arabidopsis (red). Clades of interest as specified in the text are circled in grey. The bar at the bottom provides a relative measure of branch length. The tree was produced from the Geneious tree builder module of the Geneious Pro 5.6.5 software package (Biomatters Ltd. Level 2 76 Anzac Avenue Auckland 1010 New Zealand) using the nearest neighbor joining method with 1000 replicates to obtain bootstrap values. Clade branches are labeled with % consensus support. The tree was annotated in Treeview [25] .
Figure 2
Figure 2
The approximate chromosomal locations of the endo-(1,4)-β-glucanase genes in maize. Similarly coloured regions indicate areas of homoeology, as determined by linkage mapping, between the two ancient genomes for areas of the maize genome that contain endo-(1,4)-β-glucanase genes [26]. Sections of the chromosomes without endo-(1,4)-β-glucanase genes are coloured black. Hatching indicates areas of possible genome reversal [27]. Coloured lines link homoeologues or duplicate endo-(1,4)-β-glucanase genes.
Figure 3
Figure 3
Codon based evolutionary distances for maize and sorghum genes.A. Synonymous substitutions per synonymous site estimations for maize and sorghum were used to calculate B., estimates of synonymous substitutions per synonymous site per year (KS), by assuming that maize and sorghum separated from rice and barley approximately 50 mya [28]. This allowed the synonymous substitution data to be “normalised”. C. Illustrates the estimated time in years since separation of the maize and sorghum orthologous gene pairs and maize homoeologues. D. Mutation rates for the maize sorghum gene orthologues. E. Comparisons of synonymous substitution rates between maize and maize Cel gene orthologues, maize and sorghum gene orthologues and barley and rice gene orthologues. Orthologous gene sets are presented in the same colour and the graph shows that orthologues across all four species have very similar rates of synonymous substitutions per synonymous site per year.
Figure 4
Figure 4
QPCR levels of 12 endo-(1,4)-β-glucanase genes across the developmental tissue series from barley. The vertical axis is a log10 scale and shows relative transcript levels of the genes normalised against three control genes. The vertical axis crosses the horizontal axis at 1000 copies mRNA per μl normalised cDNA. This is an arbitrary level, below which transcript levels are considered to be unreliable.
Figure 5
Figure 5
Transcript profiles for the endo-(1,4)-β-glucanase genes across the barley tissue developmental series. Transcripts below 1000 copies were considered to be background. QPCR data for HvCEL1 (A), HvCEL3 (B) and HvCEL14 (C), which represent one group of co-trasncribed HvCEL genes. These genes, which are referred to as group 1 in the text, had correlation coefficients of >0.91and showed highest levels of transcripts in tissues with maturing secondary cell walls.
Figure 6
Figure 6
Relative QPCR transcript levels for maize ZmCEL genes in internode 12. Transcript correlations of r2 of 0.9 or greater are shown. A: ZmCEL2, ZmCEL7, ZmCEL10, ZmCEL19 and ZmCEL20 all had high transcript levels in the mature zone of elongating vascular bundles, and B: similarly, ZmCEL1 and ZmCEL3 also showed highest levels of transcript in the mature zone of elongating vascular bundles, however, transcript was present in some elongating tissues. The stages of development examined included EARLY (V11), V14 and V16. P, R and VB refer to pith, rind and vascular bundle, respectively. E, M and T refer to elongation, maturation and transition zones, respectively.
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