Horizontal chromosome transfer and independent evolution drive diversification in Fusarium oxysporum f. sp. fragariae

Authors: Henry, Peter; PINCOT, DOMINIQUE - University Of California; JENNER, BRADLEY - University Of California; BORRERO, CELIA - University Of Sevilla; AVILES, MANUEL - University Of Sevilla; NAM, MYEONG-HYEON - Nonsan Strawberry Agricultural Research & Extension Services; EPSTEIN, LYNN - University Of California; KNAPP, STEVEN - University Of California; GORDON, THOMAS - University Of California

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/9/2020
Publication Date: 3/3/2021
Citation: Henry, P.M., Pincot, D.D.A, Jenner, B.N., Borrero, C., Aviles, M., Nam, M., Epstein, L., Knapp, S.J., Gordon, T.R. 2021. Horizontal chromosome transfer and independent evolution drive diversification in Fusarium oxysporum f. sp. fragariae. New Phytologist. 230(1):327-340. https://doi.org/10.1111/nph.17141.
DOI: https://doi.org/10.1111/nph.17141

Interpretive Summary: Newly emerged fungal pathogens threaten agriculture and human health globally. The evolutionary processes leading to pathogen emergence are often unknown but can inform efficient responses to these threats. We characterized the evolutionary history of Fusarium oxysporum f. sp. fragariae, the cause of Fusarium wilt of strawberry, from four continents. We showed that horizontal chromosome transfer occurred at least four times, driving diversification of this pathogen group. Pathogenic lineages also emerged without the pathogenicity chromosome we identified, and these independently evolved strains caused distinct symptoms. We discovered Fusarium wilt isolates that overcome resistance in strawberry conferred by the gene FW1, which is a critical disease management tool. To address this problem, we identified strawberry accessions resistant tyo a broad array of Fusarium wilt isolates by screening a diverse collection of strawberry germplasm.

Technical Abstract: The genes required for host specific pathogenicity in Fusarium oxysporum can be acquired through horizontal chromosome transfer (HCT). However, the frequency of HCT in nature is unknown, and it is unknown if HCT can explain the abundance of polyphyletic host-specific forms (i.e., formae speciales) in F. oxysporum. We explored the role of HCT in the evolution of F. oxysporum f. sp. fragariae, the cause of Fusarium wilt of strawberry. With isolates from four continents, we observed two distinct syndromes; one syndrome included chlorosis (“yellows-fragariae”) and the other did not (“wilt-fragariae”). We identified a predicted pathogenicity chromosome, “chrY-frag”, that is present in all yellows-fragariae isolates and was horizontally transferred at least four times. ChrY-frag encodes predicted effectors that are highly up-regulated in planta, is associated with virulence on specific cultivars, and has the characteristics of previously identified pathogenicity chromosomes. Sequence diversity suggests that chrY-frag existed in multiple phylogenetic groups before the first report of plants affected by yellows-fragariae. All strains that cause wilt-fragariae evolved without chrY-frag in Spain and eastern Australia. We uncovered no evidence that these strains spread to other countries. In contrast, strains with chrY-frag from Japan and South Korea were transported to California and western Australia. We discovered isolates that overcame resistance to Fusarium wilt conferred by FW1, but also identified broadly resistant heirloom cultivars. Our data support the conclusion that HCT is widespread in F. oxysporum, but pathogenicity can also emerge independently, through convergent evolution. Distinguishing these evolutionary relationships can accelerate the identification of host resistance.