Pathotypes of Fusarium oxysporum f. sp. fragariae express discrete repertoires of accessory genes and induce distinct host transcriptional responses during root infection

Authors: JENNER, BRADLEY - University Of California; Henry, Peter

Submitted to: Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/11/2022
Publication Date: 6/15/2022
Citation: Jenner, B.N., Henry, P.M. 2022. Pathotypes of Fusarium oxysporum f. sp. fragariae express discrete repertoires of accessory genes and induce distinct host transcriptional responses during root infection. Environmental Microbiology. 24(10):4570-4586. http://doi.org/10.1111/1462-2920.16101.
DOI: https://doi.org/10.1111/1462-2920.16101

Interpretive Summary: Knowledge of pathogen evolution can be utilized to improve disease management strategies. For example, evolutionary differences among pathogens can correspond to differences in disease resistance in plant varieties or the efficacy of molecular techniques for pathogen detection. Therefore, identifying evolutionary differences, even among closely related pathogens, can have important practical applications. This work aimed to improve our understanding of the evolutionary history of Fusarium oxysporum strains that cause disease on strawberry. There is evidence that pathogenicity of strawberry evolved at least two times in F. oxysporum, but the genes required for pathogenicity have not been fully identified in either type. In this work, we analyzed the expression of genes during strawberry plant infection and symptom formation. We found the two types of the pathogenic strains expressed different infection-specific genes, confirming their ability to cause disease on strawberry evolved independently. Additionally, the plant transcriptional response involved different phytohormone pathways to each of these pathogen types. This suggests that different strains of the same fungal species can hijack multiple plant susceptibility factors to cause disease. These results improve our ability to reduce crop losses by targeting specific evolutionary groups among Fusarium oxysporum strains that cause wilt disease of strawberry.

Technical Abstract: Isolates classified as Fusarium oxysporum f. sp. fragariae are genetically diverse and cause symptoms of chlorosis and wilting (the “yellows-fragariae” pathotype), or only wilting (the “wilt-fragariae” pathotype). Past work differentiated these pathotypes by comparative genomics, but pathotype-specific effects on host transcription and the genomic organization of wilt-fragariae pathogenicity genes remain unexplored. We challenged susceptible strawberry (Fragaria × ananassa) plants to root infection by five fungal isolates: three yellows-fragariae, one wilt-fragariae, and one that is not pathogenic to strawberry. Yellows-fragariae isolates triggered an early induction of strawberry genes related to the jasmonic acid phytohormone pathway and widespread reprogramming of cell wall modifying enzyme expression. The wilt-fragariae isolate induced few transcriptional responses in asymptomatic plants, but strongly induced ethylene production and response factors by the later timepoint when symptoms were apparent. The fungal transcriptomes revealed the pathotypes were not differentiated by conserved gene expression, including effectors on core chromosomes. By contrast, differentially expressed genes (DEGs) on fungal accessory chromosomes were almost entirely distinct between pathotypes. An ~150 kbp ‘pathogenicity island’ on a wilt-fragariae accessory chromosome was enriched with DEGs, many of whose predicted functions were related to plant infection. Sequence conservation suggests this region was horizontally transferred between two wilt-fragariae lineages. There were 15 accessory genes expressed by all yellows-fragariae isolates during root infection, and only one of these genes was also DE by the wilt-fragariae isolate. These results support the conclusion that wilt- and yellows-fragariae cause physiologically distinct syndromes by the expression of discrete repertoires of genes on accessory chromosomes.