How exceptional plants help to reveal carbon transfer between plants

Author Vincent Merckx discusses recently published Journal of Ecology article: Mycoheterotrophic plants living on arbuscular mycorrhizal fungi are generally enriched in 13C, 15N and 2H isotopes by Gomes et al.

Find out more about mycoheterotrophic plants, which have a symbiotic relationship with fungi, and why they are important.  

Plants without photosynthesis

All biology textbooks will teach you that plants are green and perform photosynthesis to fix carbon in energy-rich carbohydrates. As such, competition for light is an important driver of vegetation structure. Yet, rare exceptions exist. Some plants have managed to abandon photosynthesis, perhaps as an adaptation to low-light habitats. Best known of these plants are holoparasitic plants, which are plants that have no functional photosynthesis and instead derive nutrients directly from hosts through parasitism. There are also fully mycoheterotrophic plants, which don’t need light to grow but obtain carbon from root-associated fungi. Most species of fully mycoheterotrophic plants live on soil fungi, which simultaneously form mycorrhizas (symbiotic association) with surrounding plants. Mycorrhizal fungi are associated with green plants and can form dense underground networks, linking plants of different species. In fact, mycoheterotrophs ‘steal’ carbon from surrounding plants through these fungal networks. So, underground networks of mycorrhizal fungi can be used to transfer carbon between plant species.

Pterospora andromedea (Ericaceae) obtains carbon from surrounding trees through shared Rhizopogon ectomycorrhizal fungi. Yosemite National Park, California, USA. Photo: Vincent Merckx  

Living on fungi: more than non-green plants

Mycoheterotrophy has long been considered an exception, or – as a reviewer on one of my rejected grant proposals wrote: “insignificant in terms of ecosystem functioning”. Only c. 530 species of achlorophyllous mycoheterotrophic plants exist, and many are small and rare – or at least difficult to find (Merckx 2013). However, recent discoveries have hinted that the phenomenon might be much more common in the plant kingdom than previously assumed.

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Corallorhiza trifida (Orchidaceae) is a partial mycoheterotroph: while retaining functional photosynthesis it obtains most its carbon from associated ectomycorrhizal fungi. Bavaria, Germany. Photo: Vincent Merckx.

Partial mycoheterotrophy is difficult to detect. How do you prove that some of the carbon in a plant is of fungal origin, rather than obtained through photosynthesis? The discovery that fully mycoheterotrophic orchids and Ericaceae are significantly enriched in the ‘heavy’ isotopes of carbon (13C) and nitrogen (15N) compared to green plants growing at the same site was a real breakthrough for those trying to detect  partial mycoheterotrophy (Gebauer & Meyer 2003). The isotopic enrichments of these plants reflect their dietary supplements, as the ectomycorrhizal fungi are also enriched in heavy carbon and nitrogen. Measuring stable isotope signatures has become a powerful tool to detect partial mycoheterotrophy and led to the discovery of many partially mycoheterotrophic species (Hynson et al. 2013).

Detecting carbon transfer through arbuscular mycorrhizal fungi

The vast majority of plants on earth grow with arbuscular mycorrhizal fungi, and the occurrence of plant-to-plant carbon transfer through these fungi remains much of a mystery. Fully mycoheterotrophic plants growing on arbuscular mycorrhizal fungi exist, but they almost exclusively grow deep in tropical rainforests. Isotope signatures from these plants are essential to better understand whether isotope abundance measurements can be used to detect carbon transfer in arbuscular mycorrhizal systems as well. However, data is scarce; limited to only two studies from a decade ago, both with very limited geographic and taxonomic sampling (Merckx et al. 2010; Courty et al. 2011).

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Voyria spruceana (Gentianaceae), a fully mycoheterotrophic plant growing on arbuscular mycorrhizal fungi pictures in the Atlantic rainforest in Brazil. Photo: Vincent Merckx.

To fill this gap in our knowledge, we sampled specimens from 13 species of mycoheterotrophic plants and surrounding plants at sites in French Guiana, Malaysia, Australia, and New Zealand. These collection trips took us to remote tropical and temperate rainforests, often digging through the leaf litter on our knees, to find some of the most elusive plants on earth. We measured relative C and N isotope natural abundances and used DNA sequencing to characterise the fungal communities in the roots of the mycoheterotrophs. The results show that mycoheterotrophic plants are, a few exceptions aside, enriched in 13C, 15N and deuterium (2H). Thus, we can use these signatures to detect carbon uptake from arbuscular mycorrhizal fungi.

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The tiny flower of an undescribed species of Thismia (Thismiaceae). This species and its relatives mostly flower under the leaf litter and are rarely seen. Morton National Park, NSW, Australia. Photo: Vincent Merckx.

Are green plants also on the receiving end?

The results give us effective tools to face the next challenge: the controversial question of whether green plants can also take up carbon from arbuscular mycorrhizal networks. The isotope signatures generated in our study have already proven their use. In a recent paper, Giesemann et al. (2020) show that arbuscular mycorrhizal understory plants in forest plots in Bavaria have isotope signatures that resemble the mycoheterotrophic plants we studied. This fuels the hypothesis that carbon transfer through arbuscular mycorrhizal networks is potentially common and widespread. If this turns out to be true, the competition for light we see above ground may only tell us half of the story. For the other half, we have to turn our attention to what happens below our feet.

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Competition above, but cheating below ground? How common carbon transfer between plants through shared arbuscular mycorrhizal fungi is remains to be investigated. Rainforest near Buenaventura, Colombia. Photo: Vincent Merckx.

Vincent Merckx Naturalis Biodiversity Center, Leiden, The Netherlands & Department of Evolutionary and Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands.

Read the full research article online: Mycoheterotrophic plants living on arbuscular mycorrhizal fungi are generally enriched in 13C, 15N and 2H isotopes


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