Comparative genomic analysis reveals contraction of gene families with putative roles in pathogenesis in the fungal boxwood pathogens Calonectria henricotiae and C. pseudonaviculata

Authors: ROGERS, LAYNE - North Carolina State University; KOEHLER, ALYSSA - University Of Delaware; Crouch, Jo Anne; CUBETA, MARC - North Carolina State University; Leblanc, Nicholas

Submitted to: BMC Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/8/2022
Publication Date: 6/21/2022
Citation: Rogers, L.W., Koehler, A.M., Crouch, J.A., Cubeta, M.A., LeBlanc, N.R. 2022. Comparative genomic analysis reveals contraction of gene families with putative roles in pathogenesis in the fungal boxwood pathogens Calonectria henricotiae and C. pseudonaviculata. BMC Ecology and Evolution. 22:29. https://doi.org/10.1186/s12862-022-02035-4.
DOI: https://doi.org/10.1186/s12862-022-02035-4

Interpretive Summary: Boxwood blight, caused by the fungal plant pathogens Calonectria henricotiae and C. pseudonaviculata, has significant negative impacts on the U.S. ornamental horticulture industry. Identifying groups of genes that have increased or decreased during the evolution of C. henricotiae and C. pseudonaviculata will improve understanding of how these pathogens cause disease on ornamental boxwood shrubs and other plants in the boxwood family. In this study, we analyzed genomic data from C. henricotiae, C. pseudonaviculata and 22 closely related fungi to identify groups of genes that have uniquely changed in the causal agents of boxwood blight. Compared to other fungi that do not cause boxwood blight, C. henricotiae and C. pseudonaviculata have a reduced number genes that are predicted to play a role in pathogenesis. These results help explain why C. henricotiae and C. pseudonaviculata only cause disease on plants in the boxwood family and will inform future research focused on pathogen genetics and developing new boxwood blight resistant plants.

Technical Abstract: Boxwood blight disease caused by Calonectria henricotiae and C. pseudonaviculata is of ecological and economic significance in cultivated and native ecosystems worldwide. Prior research has focused on understanding the population genetic and genomic diversity of C. henricotiae and C. pseudonaviculata, but gene family evolution in the context of host adaptation, plant pathogenesis, and trophic lifestyle is poorly understood. This study applied bioinformatic and phylogenetic methods to examine gene family evolution in C. henricotiae, C. pseudonaviculata and 22 related fungi in the Nectriaceae that vary in pathogenic and saprobic (apathogenic) lifestyles. A total of 19750 gene families were identified in the 24 genomes, of which 422 were rapidly evolving. Among the six Calonectria species, C. henricotiae and C. pseudonaviculata were the only species to experience high levels of rapid contraction of pathogenesis-related gene families (89% and 78%, respectively). In contrast, saprobic species Calonectria multiphialidica and C. naviculata, two of the closest known relatives of C. henricotiae and C. pseudonaviculata, showed rapid expansion of pathogenesis-related gene families. Our results provide novel insight into gene family evolution within C. henricotiae and C. pseudonaviculata and suggest gene family contraction may have contributed to limited host-range expansion of these pathogens within the plant family Buxaceae.