Genomic insights into Ceratobasidium sp. associated with vascular streak dieback of woody ornamentals in the United States using a metagenomic sequencing approach

Abstract

Woody ornamentals are integral to urban landscapes and play important roles in habitat restoration and ecological conservation, yet their national and international trade facilitates the spread of plant diseases with significant ecological and economic consequences. Vascular streak dieback (VSD) recently emerged on woody ornamentals in the United States and was found to be associated with the fungal pathogen Ceratobasidium sp. (Csp), but little is known about its genomic diversity and associated microbial communities. We thus applied metagenomic sequencing to 106 symptomatic samples that had tested positive for Csp and had been collected from 34 woody ornamental species in seven states. Taxonomic profiling identified Csp as the only putative pathogen of which we recovered 17 high-quality draft genomes. Phylogenomic and pangenome analyses revealed that U.S. Csp isolates form a tight genetic cluster, distinct in gene content from C. theobromae, a pathogen of cacao, avocado, and cassava in Southeast Asia. Comparative analyses highlighted gene content differences, including candidate effectors and secondary metabolite clusters, which may underlie host interactions and offer diagnostic targets. These findings provide the first genomic insights into the U.S. Csp population, suggest the recent introduction of a single genetic lineage with a broad host range, and establish a framework for improved detection, monitoring, and management of VSD in woody ornamentals. ImportanceIdentification of the pathogen that causes an emerging disease, be it of humans, animals or plants, is a prerequisite to develop effective treatment and/or management practices and to try to control the disease outbreak to prevent further pathogen spread. Vascular Streak Dieback (VSD) is an emerging disease of ornamental bushes and trees in the U.S. Identification of the pathogen has been hindered by the difficulty in growing the fungal pathogen found to be associated with diseased plants in pure culture. Here we succeeded in sequencing DNA of the likely pathogen directly from plant tissue or from the fungal mass growing out of collected plant tissue. The sequences were assembled into genomes, which allowed us to precisely identify the pathogen, compare it to related pathogens of other plants, and to predict how it causes disease. These results can now be used to inform management and control of VSD.