Independent Evolution Has Led to Distinct Genomic Signatures in Dutch Elm Disease-Causing Fungi and Other Vascular Wilts-Causing Fungal Pathogens

Vascular wilts are important diseases caused by plant pathogenic fungi that result in the rapid death of their plant hosts. This is due to a systemic defense mechanism whereby the plant induces the compartmentalization of the infected vascular system in order to reduce the propagation of the fungus. The ascomycete class Sordariomycetes contains several species that cause vascular wilts in diverse plant hosts, and they can be classified into four taxonomic orders. The genetic mechanisms of pathogenesis have already been investigated in Fusarium and Verticillium species, but they have not yet been compared with other well-known wilt-causing species, especially fungi causing oak wilt or Dutch elm disease (DED). Here we analyzed 20 whole genome assemblies of wilt-causing fungi together with 56 other species using phylogenetic approaches to trace expansions and contractions of orthologous gene families and gene classes related to pathogenicity. We found that the wilt-causing pathogens evolved seven times, experiencing the largest fold changes in different classes of genes almost every time. However, some similarities exist across groups of wilt pathogens, particularly in Microascales and Ophiostomatales, and these include the common gains and losses of genes that make up secondary metabolite clusters (SMC). DED pathogens do not experience large-scale gene expansions, with most of the gene classes, except for some SMC families, reducing in number. We also found that gene family expansions in the most recent common ancestors of wilt pathogen groups are enriched for carbohydrate metabolic processes. Our study shows that wilt-causing species evolve primarily through distinct changes in their repertoires of pathogenicity-related genes and that there is the potential importance of carbohydrate metabolism genes for regulating osmosis in those pathogens that penetrate the plant vascular system.

Automated summary

Vascular wilts are important diseases caused by plant pathogenic fungi that cause rapid death of plants. Genetic mechanisms of pathogenesis in wilt-causing fungi have been investigated, but not compared to wilt-causing fungi causing oak wilt or Dutch elm disease. In this study, 20 whole genome assemblies of wilt-causing fungi were analyzed, together with 56 other species, to trace expansions and contractions of pathogenicity-related genes. Wilt-causing pathogens evolved seven times, with changes in different classes of genes. Common gains and losses of genes in secondary metabolite clusters were found in groups of wilt pathogens. Carbohydrate metabolic genes were enriched in gene family expansions of wilt pathogen groups. The study highlights the importance of pathogenicity-related genes and carbohydrate metabolism in wilt-causing fungi.