Comparative molecular evolution of chitinases in ascomycota with emphasis on mycoparasitism lifestyle

Abstract

Chitinases are involved in multiple aspects of fungal life cycle, such as cell wall remodelling, chitin degradation and mycoparasitism lifestyle. To improve our knowledge of the chitinase molecular evolution of Ascomycota, the gene family of 72 representatives of this phylum was identified and subjected to phylogenetic, evolution trajectory and selective pressure analyses. Phylogenetic analysis showed that the chitinase gene family size and enzyme types varied significantly, along with species evolution, especially for groups B and C. In addition, two new subgroups, C3 and C4, are recognized in group C chitinases. Random birth and death testing indicated that gene expansion and contraction occurred in most of the taxa, particularly for species in the order Hypocreales (class Sordariomycetes). From an enzyme function point of view, we speculate that group A chitinases are mainly involved in species growth and development, while the expansion of genes in group B chitinases is related to fungal mycoparasitic and entomopathogenic abilities, and, to a certain extent, the expansion of genes in group C chitinases seems to be correlated with the host range broadening of some plant-pathogenic fungi in Sordariomycetes. Further selection pressure testing revealed that chitinases and the related amino acid sites were under positive selection in the evolutionary history, especially at the nodes sharing common ancestors and the terminal branches of Hypocreales. These results give a reasonable explanation for the size and function differences of chitinase genes among ascomycetes, and provide a scientific basis for understanding the evolutionary trajectories of chitinases, particularly that towards a mycoparasitic lifestyle.

Keywords: ascomycota chitinases; episodic selection; mycoparasitism; phylogeny.

Fig. 1.

Maximum-likelihood tree showing the phylogenetic relationships of the chitinase family among 72 ascomycete species. For clarity, an expanded Newick tree is provided in Text S8.

Fig. 2.

Number of fungal chitinases in different groups. The value in each square indicates the number of chitinases; the deeper the square’s colour, the higher the chitinase number.

Fig. 3.

Gene expansion and contraction of chitinases in different species of Ascomycota. Numbers with a circle show the total number of GH18 genes in extant species or estimated for ancestral species and branches in red and blue indicate where significant expansion and contraction of GH18 gene family occurred, respectively.

Fig. 4.

Phylogram showing chitinase gene chi18-7 under positive selection during evolution of Ascomycota. Branches in red indicate a significant episodic positive selection.