From Plant Press, Vol. 24, No. 1, January 2021.
Fungi exploit their environment and interact with plants in a myriad of complex and sometimes devastating ways – from symbiotic associations in lichens, endophytes, and mycorrhizae, to wood decayers and parasites causing crop diseases. One of their most remarkable and rare life-history strategies is floral mimicry, where a parasitic fungus induces flower-like structures. These “false flowers” or pseudoflowers usually are infected leaves that mimic the look, smell, and rewards (a sugary fungal exudate) of real flowers to attract insects which then disperse the fungal spores to other plants for new infections and to effect outcrossing. The best-known systems involve rust fungi and diverse hosts, including Puccinea + Boechera (Brassicaceae), Uromyces + Euphorbia (Euphorbiaceae), and Molinilia + Vaccinium (Ericaceae).
In a pair of recent papers (Laraba et al., Mycologia 112: 39–51, 2020; Laraba et al., Fungal Genet. Biol. 144: 103466, 2020), Smithsonian Department of Botany scientist Ken Wurdack and mycological collaborators at the U.S. Department of Agriculture and Purdue University describe a novel neotropical plant-fungus association between yellow-eyed grasses (Xyris spp.; Xyridaceae) and a new pseudoflower-producing species of parasitic fungus. This research was begun during BDG-sponsored (Biological Diversity of the Guiana Shield Program) fieldwork by Wurdack, who in 2006 encountered an odd fungus on inflorescences of Xyris surinamensis in the savannas above Kaieteur Falls in the Pakaraima Mountains of western Guyana. Wurdack’s field studies were expanded during plant collecting expeditions in 2010 and 2012 (see The Plant Press 14(1): 1, 9–11, 2011; 16(1): 8–10, 2013) that explored other savannas in this region of the Guiana Shield known for tepuis (table-top mountains) and high biodiversity. The savannas typically form on thin, sandy soils over sandstone rock outcrops in the uplands (300–900 m) between mountain peaks, and are rich in endemic Xyridaceae. The fungus mimics the flowers of Xyris with yellow-orange petaloid fungal tissue that slowly grows to envelope an inflorescence, and apparently fools visiting small bees which otherwise seek to collect pollen. These fungal pseudoflowers had been sparingly noted in the Xyris systematics literature and incidentally collected with plant specimens. Wurdack surveyed Xyris specimens in the U.S. National Herbarium (US as well as MO and NY) and discovered pseudoflowers on 20 historical collections dating back to 1919, which encompassed only four Xyris species (of 250+ worldwide) in the Guiana Shield region of Colombia, Venezuela, and Guyana.
In the research of Laraba et al., a fungus was cultured from the Xyris pseudoflowers that the authors newly describe as Fusarium xyrophilum I. Laraba, K. Wurdack, Aime & O’Donnell, and use molecular phylogenetic analyses to discover its closest relatives are surprisingly from Africa. The fungus was further characterized using modern methods to determine its genome, sexual reproductive mode, and secondary metabolites. Those results paint a detailed picture of the life history of a parasitic fungus that forms unique pseudoflowers made entirely of fungal tissue, can infect all parts of its Xyris host, can manipulate host growth through the production of phytohormones, can produce mycotoxins for defense, and can produce pigments and volatiles that are known to attract insects. Many evolutionary and ecological questions remain unanswered, such as: How did this complex mimicry evolve and how is it maintained despite affecting host fertility? Why is it so host-specific? How does a disease that affects plant fertility coexist with its host? The studies of Laraba et al. are testament to new surprises coming from basic tropical biodiversity research.
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