Functional Divergence in the Arabidopsis  -1,3-Glucanase Gene Family Inferred by Phylogenetic Reconstruction of Expression States

Abstract

Plant beta-1,3-glucanases (beta-1,3-Gs) (E.C. 3.2.1.39) comprise large, highly complex gene families involved in pathogen defense as well as a wide range of normal developmental processes. In spite of previous phylogenetic analyses that classify beta-1,3-Gs by sequence relatedness, the functional evolution of beta-1,3-Gs remains unclear. Here, expression and phylogenetic analyses have been integrated in order to investigate patterns of functional divergence in the Arabidopsis beta-1,3-G gene family. Fifty beta-1,3-G genes were grouped into expression classes through clustering of microarray data, and functions were inferred based on knowledge of coexpressed genes and existing literature. The resulting expression classes were mapped as discrete states onto a phylogenetic tree and parsimony reconstruction of ancestral expression states was performed, providing a model of expression divergence. Results showed a highly nonrandom distribution of developmental expression states in the phylogeny (P = 0.0002) indicating a significant degree of coupling between sequence and developmental expression divergence. A weaker, yet significant level of coupling was found using stress response data, but not using hormone-response or pathogen-response data. According to the model of developmental expression divergence, the ancestral function was most likely involved in cell division and/or cell wall remodeling. The associated expression state is widely distributed in the phylogeny, is retained by over 25% of gene family members, and is consistent with the known functions of beta-1,3-Gs in distantly related species and gene families. Consistent with previous hypotheses, pathogenesis-related (PR) beta-1,3-Gs appear to have evolved from ancestral developmentally regulated beta-1,3-Gs, acquiring PR function through a number of evolutionary events: divergence from the ancestral expression state, acquisition of pathogen/stress-responsive expression patterns, and loss of the C-terminal region including the glycosylphosphatidylinisotol (GPI)-anchoring site thus allowing for extracellular secretion.

Glycoside Hydrolases in Plant Cell Wall Proteomes: Predicting Functions That Could Be Relevant for Improving Biomass Transformation Processes

“…According to phylogenic analyses, the GH17 family is divided into three distinct clades (denoted α, β, and γ) [61,62], with 10% of its members having cell wall-related functions [61]. GH17 of the α clade are more related to stem elongation, but also responsive to gibberellin, those of the β and γ clades are more related to stress response and defense against pathogens [62][63][64][65].…”

“…GH17 of the α clade are more related to stem elongation, but also responsive to gibberellin, those of the β and γ clades are more related to stress response and defense against pathogens [62][63][64][65]. In addition to the GH17 domain per se, proteins of the GH17 family comprise other domains as shown by [61] studying the β-1,3-glucanase sequences of A. thaliana. They noted that all the sequences had a predicted N-terminal signal peptide linking them to the secretory pathway.…”

“…All the γ clade members and more than half of the α clade members retained the CBM43 domain, whereas all the members of the β clade lost it through evolution. It is thought that the loss of this domain facilitates the extracellular secretion induced by biotic stresses, thus improving the response to pathogens [61,62].…”

The Arabidopsis CALLOSE DEFECTIVE MICROSPORE1 Gene Is Required for Male Fertility through Regulating Callose Metabolism during Microsporogenesis

“…Although only the A6 gene was thought to be a potential major component of the callase enzyme mixture (Hird et al, 1993), Arabidopsis has .50 genes encoding putative b-1,3-Gs (Doxey et al, 2007), suggesting that the metabolism of b-1,3-glucan in plants is more complex than previously understood. We identified three other b-1,3-G genes (At3g24330, At3g55780, and At3g61810) showing different extents of reduced expression in cdm1, including two anther-specific ones (Supplemental Fig.…”

“…In Lilium, it was shown that endo-b-1,3-Gs were responsible for callose wall degradation during microsporogenesis (Stieglitz, 1977). Although the Arabidopsis genome has .50 genes encoding b-1,3-Gs (Doxey et al, 2007), only the A6 gene was suggested to be a major component of the callase mixture secreted by the tapetum (Hird et al, 1993). Among known regulatory genes for anther development, only the AtMYB80 (formally AtMYB103) gene encoding a putative transcription factor was identified as a positive regulator of the A6 gene, affecting callose metabolism during microsporogenesis .…”