Genomic differences between the new Fusarium oxysporum f. sp. apii (Foa) race 4 on celery, the less virulent Foa races 2 and 3, and the avirulent on celery f. sp. coriandrii

Authors: Henry, Peter; KAUR, S - University Of California; PHAM, QUYEN - University Of California; BARAKAT, RADWAN - University Of California; BRINKER, SAMUEL - University Of California; HAENSEL, HANNAH - University Of California; DAUGOVISH, OLEG - University Of California - Cooperative Extension Service; EPSTEIN, LYNN - University Of California

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/9/2020
Publication Date: 10/20/2020
Citation: Henry, P.M., Kaur, S., Pham, Q.A.T., Barakat, R., Brinker, S., Haensel, H., Daugovish, O., Epstein, L. 2020. Genomic differences between the new Fusarium oxysporum f. sp. apii (Foa) race 4 on celery, the less virulent Foa races 2 and 3, and the avirulent on celery f. sp. coriandrii. BMC Genomics. 21. https://doi.org/10.1186/s12864-020-07141-5.
DOI: https://doi.org/10.1186/s12864-020-07141-5

Interpretive Summary: Fungal strains in the Fusarium oxysporum species complex (FOSC) usually only cause disease on one “host” plant species. Less common are FOSC strains that can cause disease on multiple hosts. It is important to determine the range of hosts upon which each strain cause disease and the genomic and evolutionary relationships that underly these differences. This information is prerequisite to developing methods for detecting fungi in soil and evaluating the efficacy of treatments for plant disease management. We evaluated the evolutionary relationships and host ranges for FOSC strains that cause disease on celery and cilantro. Isolates that cause disease on celery also caused disease on cilantro, but some isolates could only cause disease on cilantro. The genomes of celery/cilantro and cilantro-specific isolates are very similar, but differ in specific “accessory” chromosomes that are thought to contain genes required for host-specific pathogenicity. We designed DNA-based methods for detecting celery/cilantro and cilantro-specific FOSC from infected plant tissues.

Technical Abstract: Background: Members of the F. oxysporium species complex (FOSC) in the f. sp. apii (Foa) are pathogenic on celery and those in f. sp. coriandrii (Foci) are pathogenic on coriander (=cilantro). Foci was first reported in California in 2005; a new and highly aggressive race 4 of Foa was reported in 2013 in California. Preliminary evidence indicated that Foa can also cause disease on coriander, albeit are less virulent than Foci. Comparative genomics was used to investigate the evolutionary relationships between Foa race 4, Foa race 3, and the Foci, which are all in FOSC Clade 2, and Foa race 2, which is in FOSC Clade 3. Results: A phylogenetic analysis of 2,718 single-copy conserved genes and mitochondrial DNA sequence indicated that Foa races 3 and 4 and the Foci are monophyletic within FOSC Clade 2; these strains also are in a single somatic compatibility group. However, in the accessory genomes, the Foci versus Foa races 3 and 4 differ in multiple contigs. Based on significantly increased expression of Foa race 4 genes in planta vs. in vitro, we identified 23 putative effectors and 13 possible pathogenicity factors. PCR primers for diagnosis of either Foa race 2 or 4 and the Foci were identified. Finally, mixtures of conidia that were pre-stained with different fluorochromes indicated that Foa race 4 formed conidial anastomosis tubes (CATs) with Foci. Foa race 4 and Foa race 2, which are in different somatic compatibility groups, did not form CATs with each other. Conclusions: There was no evidence that Foa race 2 was involved in the recent evolution of Foa race 4; Foa race 2 and 4 are CAT-incompatible. Although Foa races 3 and 4 and the Foci are closely related, there is no evidence that either Foci contributed to the evolution of Foa race 4, or that Foa race 4 was the recipient of a multi-gene chromosomal segment from another strain. However, horizontal chromosome transfer could account for the major difference in the accessory genomes of Foa race 4 and the Foci and for their differences in host range.