Pseudoflowers produced by Fusarium xyrophilum on yellow-eyed grass (Xyris spp.) in Guyana: A novel floral mimicry system?

Authors: LARABA, IMANE - Orise Fellow; McCormick, Susan; Vaughan, Martha; Proctor, Robert; Busman, Mark; Appell, Michael; O Donnell, Kerry; Felker, Frederick; AIME, M - Purdue University; WURDACK, KENNETH - Smithsonian Institute

Submitted to: Fungal Genetics and Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/11/2020
Publication Date: 9/19/2020
Citation: Laraba, I., McCormick, S.P., Vaughan, M.M., Proctor, R.H., Busman, M., Appell, M., O'Donnell, K., Felker, F.C., Aime, M.C., Wurdack, K.J. 2020. Pseudoflowers produced by Fusarium xyrophilum on yellow-eyed grass (Xyris spp.) in Guyana: A novel floral mimicry system? Fungal Genetics and Biology. 144. Article 103466. https://doi.org/10.1016/j.fgb.2020.103466.
DOI: https://doi.org/10.1016/j.fgb.2020.103466

Interpretive Summary: Diseases caused by fusaria and their toxins pose a global threat to agricultural biosecurity and food safety. Reports of plant pathogens that induce pseudoflowers (i.e., flower-like structures) on their hosts are exceedingly rare. Herein we report on the discovery of pseudoflowers on Xyris species (yellow-eyed grass) in the savannas of the Pakaraima Mountains of western Guyana. The pseudoflowers mimic Xyris floral traits, they are composed entirely of Fusarium xyrophilum mycelium, and contained both mating types. Biochemical analyses revealed that cultures of the fungus produced pigments characterized by fluorescence emissions over several wavelengths known to attract insects and volatiles previously reported as pollinators attractants. These data suggest that visual and olfactory cues are potentially involved in this mimicry system to attract pollinators that might vector infective spores to new hosts. This study advances our understanding of the structural diversity of pseudoflowers and provides a foundation for subsequent investigations into the natural history and molecular underpinnings of a novel floral mimicry system. The present study has opened a completely new avenue of research for plant and fungal molecular biologists to elucidate how plant pathogens manipulate their hosts. Such knowledge could inform novel strategies for controlling plant diseases.

Technical Abstract: Pseudoflower formation is arguably the rarest outcome of a plant-fungal interaction. Here we report on a novel floral mimicry system with pseudoflowers made up entirely of fungal tissues in contrast to modified leaves documented in previous systems. Pseudoflowers on two perennial Xyris species (yellow-eyed grass, Xyridaceae) recovered during fieldwork in Guyana were produced by Fusarium xyrophilum. We characterized the visual and olfactory cues that might be involved in this mimicry system, investigated whether the pathogen established a systemic infection in its hosts, and assessed its sexual reproductive mode. We also analyzed the ability of F. xyrophilum to produce phytohormones. These fungal pseudoflowers are ultraviolet reflective, mimic Xyris flowers in gross morphology, and contain both mating type idiomorphs. Cultures of F. xyrophilum produced two pigments, which had fluorescence emission maxima in light ranges that trichromatic insects are sensitive to, volatiles known to attract insect pollinators, and IAA and iPR phytohormones. Fusarium xyrophilum had established a systemic infection in both Xyris species. Field observations revealed that pseudoflowers and Xyris flowers were visited by bees. These data suggest that F. xyrophilum is likely deceiving pollinators into vectoring its conidia via visual and olfactory cues, which might facilitate outcrossing of this putatively heterothallic fungus.