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