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, 8 (5), 1374-87

Divergent and Convergent Evolution of Fungal Pathogenicity

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Divergent and Convergent Evolution of Fungal Pathogenicity

Yanfang Shang et al. Genome Biol Evol.

Abstract

Fungal pathogens of plants and animals have multifarious effects; they cause devastating damages to agricultures, lead to life-threatening diseases in humans, or induce beneficial effects by reducing insect pest populations. Many virulence factors have been determined in different fungal pathogens; however, the molecular determinants contributing to fungal host selection and adaptation are largely unknown. In this study, we sequenced the genomes of seven ascomycete insect pathogens and performed the genome-wide analyses of 33 species of filamentous ascomycete pathogenic fungi that infect insects (12 species), plants (12), and humans (9). Our results revealed that the genomes of plant pathogens encode more proteins and protein families than the insect and human pathogens. Unexpectedly, more common orthologous protein groups are shared between the insect and plant pathogens than between the two animal group pathogens. We also found that the pathogenicity of host-adapted fungi evolved multiple times, and that both divergent and convergent evolutions occurred during pathogen-host cospeciation thus resulting in protein families with similar features in each fungal group. However, the role of phylogenetic relatedness on the evolution of protein families and therefore pathotype formation could not be ruled out due to the effect of common ancestry. The evolutionary correlation analyses led to the identification of different protein families that correlated with alternate pathotypes. Particularly, the effector-like proteins identified in plant and animal pathogens were strongly linked to fungal host adaptation, suggesting the existence of similar gene-for-gene relationships in fungus-animal interactions that has not been established before. These results well advance our understanding of the evolution of fungal pathogenicity and the factors that contribute to fungal pathotype formation.

Keywords: comparative genomics; convergent evolution; effector; fungal pathogen; host adaptation; pathotype.

Figures

F<sc>ig</sc>. 1.—
Fig. 1.—
Phylogenetic analysis of insect, plant, and mammalian pathogenic fungi. The maximum-likelihood tree was generated using the concatenated sequences of 47 universal proteins with the program TREE-PUZZLE using a Dayhoff substitution model, a partial deletion for gaps or missing data, and 100 bootstrap replicates. The tree is rooted by the basidiomycete plant pathogen Ustilago maydis (UM). Green (MAT 1-1) and red (MAT 1-2) arrows indicate the mating-type of each sequenced strain. Species with both arrows are homothallic fungi. Insect fungi are labeled in red, plant fungi in green, and mammalian fungi in black.
F<sc>ig</sc>. 2.—
Fig. 2.—
Analyses of relationships between three groups of fungi. (A) Venn diagram of IF, PF, and MF pathogenic fungi based on the orthologous protein groups identified by OrthoMCL analysis. (B) Genetic similarity among three groups of fungi. MDS analysis was performed based on the extracted conserved blocks of individual orthologous protein sequence (n = 2,754) alignments, and the K-means clustering (K = 3) was used to group each fungal species into three clusters for IF (blue), MF (red), and PF (green). Pairwise genetic distance was calculated, and the length of each colored segment in each species represents the proportion of its orthologous proteins that represent the minimum average genetic distance to the corresponding fungal group.
F<sc>ig</sc>. 3.—
Fig. 3.—
PCA of fungal species. PCA of examined fungal species based on (A) the orthologous protein groups identified in OrthoMCL analysis, (B) the number of proteins putatively involved in PHI, (C) the number of SSCP effectors, and (D) the number of GHs. Species I1–I12 are simplified for 12 insect pathogenic fungi, P1–P12 for 12 plant pathogenic fungi, and M1–M9 for nine mammalian pathogenic fungi that are detailed in supplementary table S2, Supplementary Material online.
F<sc>ig</sc>. 4.—
Fig. 4.—
Characterization of secreted proteins and putative effectors of SSCPs. (A) Kinetic profiles of the secreted proteins and SSCPs encoded by each fungal species. Species I1–I12 are simplified for 12 insect pathogenic fungi (IF), P1–P12 for 12 plant pathogenic fungi (PF), and M1–M9 for nine mammalian pathogenic fungi (MF) that are detailed in supplementary table S2, Supplementary Material online. (B) Average number of secreted proteins encoded by IF, PF, and MF, respectively. (C) Average number of SSCPs encoded by IF, PF, and MF, respectively.
F<sc>ig</sc>. 5.—
Fig. 5.—
Conserved and lineage-specific evolution of SMs in different fungi. (A) Phylogeny of a highly conserved NRPS putatively involved in siderophore biosynthesis in 25 fungal species. The adenylation domain in the NRPS protein of each species was retrieved and used to generate the maximum-likelihood tree, which revealed a relatively congruent relationship with the fungal speciation tree. The proteins from IF are labeled in red, from PF in green, and from MF in black. (B) A highly conserved NRPS gene cluster is present in the bee pathogen, A. apis and seven mammalian pathogens. Orthologous genes are indicated by the same color. Genes with blank labels are hypothetical.

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