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

Peter Henry,Oleg Daugovish,Sukhwinder Kaur,Radwan Barakat,Hannah Haensel,Lynn Epstein,Samuel Brinker,Quyen Anh Tran Pham

doi:10.1186/s12864-020-07141-5

Abstract

BackgroundMembers 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 observed 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.ResultsA phylogenetic analysis of 2718 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.ConclusionsThere 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 recent 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.

Highlights

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)
We show evidence i) that Fusarium oxysporum f. sp. apii (Foa) races 3 and 4 and the Fusarium oxysporum f. sp. coriandrii (Foci) are in a single somatic compatibility group and form a subclade with the FOSC Clade 2 based on 2718 aligned, conserved nuclear genes within the FOSC and the complete mitochondrial sequence; ii) that while the accessory genomes of Foa races 3 versus 4 are very similar, the Foci and the Foa in FOSC Clade 2 differ in approximately 37% of the accessory genome; and iii) that Foa race 4 apparently arose from a Foa race 3-like progenitor, and that neither the Foci nor Foa race 2 provided new DNA
Foa races 3 and 4 and the Foci are in the same somatic compatibility group; both celery and coriander are in the plant family Apiaceae

Summary

Introduction

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). Preliminary evidence indicated that Foa can cause disease on coriander, albeit are less virulent than Foci. Foa race 2 is virulent on both Tall Utah 52–70 R Improved and Golden Self Blanching, and isolates appear to be monomorphic [3]. In 1984, Puhalla [10] noted that in addition to Foa race 2, there was a Foa race 3 in California that was virulent on Tall Utah 52–70 R Improved but reportedly avirulent on Golden Self Blanching; importantly, Foa race 3 was in a different somatic compatibility group than Foa race 2. In a study that included pathogenicity tests and two-locus sequencing of isolates collected between 1993 and 2013 from symptomatic celery plants that were primarily from California, none of the 174 isolates were classified as Foa race 3 [3]. One isolate from a culture collection that was deposited as the Foa “T” strain by California researcher Shirley Nash Smith in 1981 was classified as a “Foa race 3-type” [3]

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