Fungal imposters

I’ve long been fascinated by the many, complex ways in which plants interact with fungi – mycorrhizal fungi associated with the earliest plant roots are now thought to be have been key in the successful colonisation of land by plants.  However a recent study on fungi which produce pseudoflowers, by Imane Laraba and colleagues, has caught my eye.  These fungi deceive insects into spreading their spores instead of pollen from the plant’s true flowers – a new idea to me.

The story starts in 2006 when, on a plant-collecting trip to Guyana, Kenneth Wurdack of the Smithsonian Institution found some odd looking flowers on two species of Yellow-eyed grass (Xyris sp.). They were more orange in colour than usual, had tightly clustered ‘petals’ and an odd, spongey texture.  It turned out they were not flowers at all but fungal mycelium masquerading as flowers.  When a soil fungus called Fusarium xyrophilum infects Xyris setigera and X. surinamensi it blocks the pathways leading to normal formation and diverts the plant’s energy into producing pseudoflowers made of fungal tissue. The pseudoflowers emerge first at the tip of the infloresence as a disc-shaped mass but then differentiate into petal-like structures.  Whilst uninfected Xyris plants produce one or two new, ephemeral flowers each day, the fungal pseudoflowers persist for several days.

Fig. 1 from Laraba et al. A and B: young and mature Fusarium xyrophilum pseudoflowers at the tip of a spike of Xyris surinamensis C: longitudinal section thorough pseudoflower D: healthy Xyris surinamensis flower. Scale bar = 5 mm.

Why would the fungus go to all this trouble?  To trick insect pollinators into dispersing its spores, allowing them to be transmitted over longer distances than would otherwise be possible and also facilitating outcrossing between the two different fungal mating types, generating all-important genetic diversity. Many Fusarium fungi are pathogens of crop plants, producing wilt diseases in the Solanaceae family (potatoes, tomatoes, aubergines etc) and mycotoxins which accumulate and contaminate cereal crops.   The fungi reproduce by both asexual conidia and sexual ascospores, the latter produced when mycelia of two different mating types fuse.  Dispersing both types of spore widely is the name of the game for the fungus and, as both real flowers and pseudoflowers are visited by small bees, the bees are thought to carry fungal conidia as well as pollen.

Wurdack and his colleagues had many questions, including how pseudoflowers attract pollinators in the absence of a pollen reward. One suggestion was that they produce pigments which emit light at the UV end of the visible spectrum to attract insects such as bees; many yellow flowers, such as those of Xyris, do this. The researchers were able to extract two pigments (8-O-methylfusarubin and 8-O-methylbostrycoidin) from both the pseudoflowers and Fusarium cultures and found that, sure enough, these emitted light strongly at wavelengths of 486 and 495 nm respectively – the region of the light spectrum to which bees are most strongly attracted. 

A second suggestion was that the Fusarium can produce volatile organic compounds (VOCs) similar to those produced by Xyris flowers, to attract insects. The researchers found that F. xyrophilum cultures do emit a mixture of up to ten VOCs one of which, 2-ethylhexanol, is also produced by Xyris laxifolia var. iridifolia flowers.  Plants from many families release this alcohol, which is a strong attractant for bees.  Covid travel restrictions have meant that the researchers had to make do with looking at the floral scent profile of a species of Xyris they were able to find in the US rather than the known pseudoflower-producing species but they hope to be able to confirm that finding once they can visit Guyana again.

The research raises many questions: How does the fungus alter the plant’s growth in these ways? Does it produce a systemic infection in the plant? What controls the production of the pseudoflowers and are they derived from modified leaves, as happens with some other fungal genera such as Puccinia, Uromyces and Monilina?

Unsurprisingly, perhaps, the researchers found by using a PCR assay to check for fungal DNA that Fusarium does infect host plants systemically, with hyphae in both roots and shoots and with the pseudoflowers themselves composed entirely of interwoven and densely packed hyphae – this is unique among known floral mimicry systems.  They were also able to determine that the genes responsible for two important plant growth hormones, auxin and cytokinin, are expressed in Fusarium and that auxin, in particular, is produced at high levels. It is these that induce the production of pseudoflowers.

Interestingly, this seems to be a very specific relationship – F. xyrophilum is the only known pseudoflower-producing Fusarium species and, despite the diversity of the genus, is known to infect only three of the many Xyris species found worldwide.  A few other fungal genera do have species capable of altering host plants to serve their own ends in a less dramatic way, modifying host plant leaves to bear fungal spores, but none go as far as Fusarium in producing pseudoflowers entirely of fungal tissue.  Their combination of producing pigments to match insects’ spectral sensitivity and attractive volatile organic compounds is also unique.

A study like this raises as many question as it answers. Is this an entirely parasitic relationship or do the ephemeral real flowers benefit from increased pollinator traffic to the longer-lived pseudoflowers?  That will partly depend on whether the pseudoflowers and real Xyris flowers share the same insect visitors – it seems likely but, once again, more field research is needed to work this out.  I’d go!

Laraba, I. et al. (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

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