Phylogeographic and phylogenomic structure of the quarantine plant pathogen Colletotrichum liriopes, including new reports in the United States

Authors: CHAVERRI, P - Oak Ridge Institute For Science And Education (ORISE); ROMBERG, MEGAN - Animal And Plant Health Inspection Service (APHIS); MONTERRO-VARGAS, MARIPAZ - Costa Rica Institution; MCKEMY, JOHN - Animal And Plant Health Inspection Service (APHIS); RANE, KAREN - University Of Maryland; BALBALIAN, CLARISSA - Mississippi State University; Castlebury, Lisa

Submitted to: Plant Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/16/2023
Publication Date: 9/19/2023
Citation: Chaverri, P., Romberg, M.K., Monterro-Vargas, M., McKemy, J.M., Rane, K.K., Balbalian, C.J., Castlebury, L.A. 2023. Phylogeographic and phylogenomic structure of the quarantine plant pathogen Colletotrichum liriopes, including new reports in the United States. Plant Disease. 107:2816-2824. https://doi.org/10.1094/PDIS-10-22-2324-RE
DOI: https://doi.org/10.1094/PDIS-10-22-2324-RE

Interpretive Summary: Many fungi cause plant diseases and the presence of a fungus not known to occur in the United States can cause shipments of live plants from outside of the U.S. to be destroyed or sent back to their originating country. This causes millions of dollars in losses each year to the nursery industry and importers. Liriope is a common ornamental plant that is often imported for sale in the U.S. Since the fungus Colletotrichum liriopes was not known to occur on this plant in the U.S., shipments of plants infected with this fungus were rejected at the ports and often destroyed. This study surveyed several locations in the eastern half of the U.S. and discovered that C. liriopes is present in multiple locations on liriope and like widespread wherever liriope is grown. DNA sequencing and microscopy were used to identify the pathogen. This information will be used by regulatory officials, extension personnel and plant pathologists to determine if infected plants are a risk and could save millions of dollars in import/export costs.

Technical Abstract: Global agricultural trade has accelerated the emergence and re-emergence of new plant pathogens. In the United States, the fungal pathogen Colletotrichum liriopes is still considered a foreign quarantine pathogen that affects ornamental plants (i.e., Liriope spp.). Even though this species has been reported in East Asia on various asparagaceous hosts, its first and only report in the United States was in 2018. However, that study used only ITS nrDNA for identification, and no available culture or voucher specimen was maintained. The main objective of the present study was to determine the geographic and host distribution of specimens identified as C. liriopes. To accomplish this, new and existing isolates, sequences, and genomes obtained from various hosts and geographic locations (i.e., China, Colombia, Mexico, and the United States) were compared with the ex-type of C. liriopes. Multilocus phylogenetic (ITS, Tub2, GAPDH, CHS-1, and HIS3), phylogenomic, and splits tree analyses revealed that all the studied isolates/sequences form a well-supported clade with little intraspecific variation. Morphological characterizations support these findings. The minimum spanning network, low nucleotide diversity, and negative Tajima’s D from both multilocus and genomic data suggest that there was a recent movement/invasion of a few East Asian genotypes to other countries where the ornamental plants are produced (e.g., South America) and subsequently to the importing countries, such as the United States. The study reveals that the geographic and host distribution of C. liriopes sensu stricto is expanded to the United States (i.e., at least Maryland, Mississippi, and Tennessee) and on various hosts in addition to Asparagaceae and Orchidaceae. The present study produces fundamental knowledge that can be used in efforts to reduce costs or losses from agricultural trade and to expand our understanding of pathogen movement.