Abstract
Chitin synthases (CHSs) are key enzymes in the biosynthesis of chitin, an important structural component of fungal cell walls that can trigger innate immune responses in host plants and animals. Members of CHS gene family perform various functions in fungal cellular processes. Previous studies focused primarily on classifying diverse CHSs into different classes, regardless of their functional diversification, or on characterizing their functions in individual fungal species. A complete and systematic comparative analysis of CHS genes based on their orthologous relationships will be valuable for elucidating the evolution and functions of different CHS genes in fungi. Here, we identified and compared members of the CHS gene family across the fungal tree of life, including 18 divergent fungal lineages. Phylogenetic analysis revealed that the fungal CHS gene family is comprised of at least 10 ancestral orthologous clades, which have undergone multiple independent duplications and losses in different fungal lineages during evolution. Interestingly, one of these CHS clades (class III) was expanded in plant or animal pathogenic fungi belonging to different fungal lineages. Two clades (classes VIb and VIc) identified for the first time in this study occurred mainly in plant pathogenic fungi from Sordariomycetes and Dothideomycetes. Moreover, members of classes III and VIb were specifically up-regulated during plant infection, suggesting important roles in pathogenesis. In addition, CHS-associated networks conserved among plant pathogenic fungi are involved in various biological processes, including sexual reproduction and plant infection. We also identified specificity-determining sites, many of which are located at or adjacent to important structural and functional sites that are potentially responsible for functional divergence of different CHS classes. Overall, our results provide new insights into the evolution and function of members of CHS gene family in the fungal kingdom. Specificity-determining sites identified here may be attractive targets for further structural and experimental studies.
Highlights
Chitin synthases (CHSs) are key enzymes in the biosynthesis of chitin, an important structural component of fungal cell walls that can trigger innate immune responses in host plants and animals
Phylogenetic analysis revealed that the fungal CHS gene family is comprised of at least 10 ancestral orthologous clades, which have undergone multiple independent duplications and losses in different fungal lineages during evolution
We found that one orthologous clade of CHS genes was expanded mainly in important animal or plant pathogenic fungi from different fungal lineages
Summary
Daughter cells after cell division as a repair enzyme (Cabib et al., 1989). ScCHS2 participates in the processes of primary septum formation and cell division (Silverman et al, 1988). We found that one orthologous clade of CHS genes (class III) was expanded mainly in important animal or plant pathogenic fungi from different fungal lineages. Previous studies focused primarily on classifying diverse CHSs into different classes (Choquer et al, 2004; Mandel et al, 2006; Ruiz-Herrera and Ortiz-Castellanos, 2010). The majority of these studies employed a limited number of fungal species from a narrow range of fungal lineages (mostly later-branching fungi), which could lead to difficulty in establishing the relationships among different classes and even ambiguously classifying some CHSs into different or multiple classes. ScCHS1 replenishes chitin in the cell wall of Frontiers in Plant Science | www.frontiersin.org
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