Fusarium xyrophilum sp. nov., a remarkable pseudoflower-producing pathogen of yellow-eyed grasses (Xyris spp.) from Guyana

Authors: LARABA, IMANE - Orise Fellow; Kim, Hye-Seon; Proctor, Robert; Busman, Mark; O Donnell, Kerry; Felker, Frederick; AIME, CATHERINE - Purdue University; KOCH, RACHEL - Purdue University; WURDACK, KENNETH - Smithsonian Research Institute

Submitted to: Mycologia
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/13/2019
Publication Date: 12/11/2019
Citation: Laraba, I., Kim, H.-S., Proctor, R.H., Busman, M., O'Donnell, K., Felker, F.C., Aime, M.C., Koch, R.A., Wurdack, K.J. 2019. Fusarium xyrophilum, sp. nov., a member of the Fusarium fujikuroi species complex recovered from pseudoflowers on yellow-eyed grass (Xyris spp.) from Guyana. Mycologia. 112(1):39-51. https://doi.org/10.1080/00275514.2019.1668991.
DOI: https://doi.org/10.1080/00275514.2019.1668991

Interpretive Summary: Fusarial diseases and their toxins are responsible for multibillion-dollar annual losses to the U.S. and world’s agricultural economy. While Fusarium and other plant pathogens can induce significant changes in the flowers that they infect, reports of fungi that induce flower-like structures called pseudoflowers on their hosts are exceedingly rare. Here we report on the discovery and characterization of pseudoflowers on Xyris species (yellow-eyed grass) growing in western Guyana. The pseudoflowers produced on Xyris are fundamentally different from the few previously reported because they are composed entirely of Fusarium. Pseudoflowers appear to serve as visual cues attracting pollinators that might vector infective spores to new hosts. Analyses of the F. xyrophilum genome indicated it has the genetic potential to produce several mycotoxins, pigments, and plant hormones. These research results provide a starting point for investigating the transmission biology and molecular basis of a unique plant pathogen-host interaction.

Technical Abstract: Herein we report on the discovery and characterization of a novel Fusarium species that produced yellow-orange pseudoflowers on Xyris spp. (yellow-eyed grass; Xyridaceae) growing in the savannas of the Pakaraima Mountains of western Guyana. By examining herbarium specimens, we documented a broader occurrence of pseudoflowers on four Xyris species spanning northern South America. The petaloid fungal structures produced on infected plants mimic host flowers in gross morphology. Molecular phylogenetic analyses of full-length RPB1, RPB2, and TEF1 DNA sequences mined from whole genomes resolved the fungus, described herein as F. xyrophilum sp. nov., as sister to F. pseudocircinatum within the African clade of the F. fujikuroi species complex. Results of a PCR assay for mating type idiomorph revealed that single conidial isolates of F. xyrophilum only possessed one of the MAT idiomorphs (MAT1-1 or MAT1-2), which suggests that this fungus might possess a heterothallic sexual reproductive mode. BLASTn searches of whole genome sequence of three strains of F. xyrophilum indicated it has the genetic potential to produce secondary metabolites, including phytohormones, pigments and mycotoxins. However, a polyketide-derived pigment, 8-O-methylbostrycoidin, was the only metabolite detected on cracked maize kernel cultures. Furthermore, F. xyrophilum is phenotypically distinct from all other Fusarium species in that it produces 0-septate microconidia on erect synnemata that are up to 2 mm tall on carnation leaves and it apparently lacks the ability to produce multiseptate macroconidia.