F Rosa Rubicondior: Evolution News - An Extreme Case of Evolved Mimicry

Monday 15 March 2021

Evolution News - An Extreme Case of Evolved Mimicry

Two orange-yellow “blooms” at right are fungal mimics of flowers produced by yellow-eyed grasses, such as the one at left.

Credit: K. Wurdack/Smithsonian Institution
This Flower Is Really a Fungus in Disguise - Scientific American

This fascinating example of fungal parasitism comes from Guyana and was discovered by researchers from the Mycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, Peoria, IL, USA.

It is produced by the novel fungus Fusarium xyrophilum which parasitizes two plant species of the Xyris genus, X. setigera and X. surinamensis, commonly known as yellow-eyed grass. Not only does the parasite mimic the petals of the flowers it mimics but also the scents they use to attract pollinating insects, so tricking bees and other pollinating insects into spreading the fungal spores instead of pollen.

The research team's findings were published last November in the journal, Fungal Genetics and Biology sadly, behind a paywall, however, the summary by the USDA Agricultural Research Service gives the following details:
This is the only example that we know of, anywhere on planet Earth, where the false flower is all fungal.

Kerry O’Donnell, Co-author
Microbiologist U.S. Department of Agriculture’s Agricultural Research Service
U.S. Department of Agriculture

Quoted in Scientific American
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.
I think it’s a case of mimicry that still needs more documentation, but when you look at the shape, the color [of the pseudoflowers], it’s hard not to be incredibly impressed with what nature has done.

Jonathan Gershenzon (not involved in the study)
Max Planck Institute for Chemical Ecology
Jena, Germany

Quoted in Scientific American
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.
Mimicry evolves where there is a clear advantage in resembling another species in the organism's environment. In this case, the organisms the fungus came to resemble were the the related species that it parasitised, where there was a clear and obvious advantage in resembling the flowers it grew in close proximity to. The more closely it resembles its host's flowers the more successful at getting its spores dispersed it would have become. The fact that it was attracting the same pollinating insects explains why it produces colours to which those insects are attracted and scents to which they are also attracted.

But, from an intelligent [sic] design perspective, what a complex and prolifically wasteful method for producing the next generation of F. xyrophilum, of which the fungus only need produce one other offspring over its lifetime for the population to remain stable. Surely, it would not have been beyond the capabilities of a real intelligent, omnipotent, designer to design a simpler way to produce another fungus.

What will be interesting, once the coronavirus pandemic is over and the team can again travel to Guyana, whether there are any signs of an arms race developing between the host species and this parasitic fungus which are both competing for the same insect pollinator resource to achieve the same result - reproduction.

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. 144:103466. DOI: https://doi.org/10.1016/j.fgb.2020.103466

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