Thismia and its unusual number of specialist relationships.

Plants sometimes specialise. Catering for a specific partner can ensure a reliable source of food or pollination. At the same time, relying on that partner limits your adaptability. A new study by Guo and colleagues, A symbiotic balancing act: arbuscular mycorrhizal specificity and specialist fungus gnat pollination in the mycoheterotrophic genus Thismia (Thismiaceae), looks at a plant that doesn’t have just one partner, but two.

A gnat inside a Thismia flower
Photo: Guo et al. 2019.

Thismia tentaculata is a plant that uses fungus gnats to pollinate its flowers. The flowers are built for them, and wouldn’t be accessible by other insects. Below the ground, however, things get odder.

Most plants are autotrophs. -troph refers to what they eat, and auto means they make it themselves. So an autotroph makes its own food, usually through photosynthesis. Thismia is a heterotroph, a mycoheterotroph to be precise. -hetero means it gets its food from elsewhere, and Myco tells us it’s from fungus.

Professor Richard Saunders, of The University of Hong Kong, and an author on the paper, said: “Mycoheterotrophy, in which plants abandon photosynthesis in favour of indirectly obtaining their carbon supply from autotrophic plants via a mycorrhizal intermediary, is an inherently interesting biological phenomenon. Although it is comparatively rare among flowering plants, it has evolved independently in multiple different lineages.”

As we know of unrelated mycoheterotrophs, we can compare and contrast plants. If different plants adopt similar solutions to problems, this tells something about how mycoheterotrophy works. Saunders said: “We specifically address whether it is possible for a plant species (in this case, the mycoheterotrophic Thismia tentaculata) to rely on two highly specialised symbionts simultaneously: it has previously been hypothesised that mycoheterotrophs, which are dependent on a very narrow range of arbuscular mycorrhizal symbionts, are likely to adopt a very stable reproductive system that assures seedset. Thismia flowers are structurally highly complex, suggesting that they cross-pollinate rather than achieving seedset by selfing.”

It was these elaborate flowers that provided the clue that Thismia was juggling two partners. Saunders said: “Thismia species have highly complex flowers that are not consistent with self-fertilisation. Many pollination ecologists have speculated on the likely pollination mechanism in the genus, but no empirical studies have ever been conducted before (probably because of the ephemeral nature of the plants and their rarity).”

It seems Thismia can balance the demands of the two partners because while the relationship is specialist, numbers are on Thismia‘s side. Saunders said: “Although we demonstrate the existence of a dual specialisation above and below ground, it appears that both the arbuscular mycorrhizal symbionts and the fungus gnat pollinators are widespread. Multiple-partner symbioses are possible if redundant selective pressures are not exerted to further restrict an already constrained suite of life history traits.”

Given the rarity of Thismia and its transient lifestyle, it might seem it’s an odd plant to base a study on. There must be easier mycoheterotrophs to find. In this case, Saunders said that location was important. “Thismia species are rare and are often transient and inaccessible. My research group is based in Hong Kong, where we are fortunate to have two indigenous Thismia species, one of which is endemic to the territory. The relative ease of access to the sites enabled us to undertake time-consuming observations of reproductive ecology that other researchers have not been able to achieve.”

Saunders said that while Hong Kong has Thismia it still poses difficulties in comparison to the two other partners. “The most significant problem was the relative rarity of Thismia tentaculata, which imposed considerable constraints on sample sizes and replication. The mycorrhizal fungi were identified by extracting the DNA, sequencing it commercially and then comparing the sequence data against available databases. Fungus gnats are ubiquitous to the forest floor and are often seen flying close to the leaf litter (although they are very small, c. 1 mm, and hence are easily overlooked).”

While Thismia have this dual partnership, it’s quite possible that they’re not the only plants to do this. “Fungus gnat pollination is phylogenetically quite widespread amongst species with flowers located close to the leaf litter. The mycorrhizal interactions with mycoheterotrophs are better studied than the pollination ecology, however. Since mycoheterotrophs have often been shown to interact with a single fungal species and often also have structurally complex flowers, it is likely that other species have developed a dual partnership.”

Given the sheer variety of orchids, it might be interesting to search through the more mixtrophic or heterotrophic species.

The research not only overturns an assumption made about mycoheterotrophs but also opens new opportunities. Saunders said: “I think our work is interesting because it demonstrates the pollination system in Thismia for the first time. Species in this genus have an extraordinarily complex and variable floral morphology, and there is considerable scope for understanding the broader diversity of pollination systems in the genus and their associated evolutionary transitions: clearly, reconstructing a robust and well-sampled molecular phylogeny of the genus would greatly assist this, as would clarification of the chemical cues attracting the fungus gnat pollinators. Fungus gnats are known to be attracted to fungi and are likely to be stimulated by fungus-like floral scents; unfortunately, our attempts to characterise the floral scent of Thismia tentaculata was unsuccessful.”

Drops inside a Thismia flower
Photo: Guo et al. 2019.

“Another area worthy of further investigation is the function of the exudate drop that forms on the appendage hair (arrowed above). We are unclear whether it functions as a pollinator reward: if not, then the plant presumably has a deceptive pollination system, and hence is a ‘double cheater’.”

Thismia may be adept at attracting partners, but it seems that it gets the most out of the partners it has.