When a plant loses photosynthesis, what else does it lose?

One of the common features of plants they make their own food. But what happens inside a plant when they stop making their food and eat something else?

Plants are, mostly, green at least somewhere on their bodies. The reason they’re green is down to chloroplasts, the organelles that manage photosynthesis. Sometimes though a plant can give up photosynthesis and become a heterotroph, an organism that gets its food from elsewhere. For example, some plants are parasites. They grab the nutrients they need to grow by tapping into another plant. Others steal food from fungi.

Plants in the genus Epirixanthes (Polygalaceae) are an example of a plant that taps into fungi, a mycoheterotroph. The plants are in the Milkwort family, and a dicot, so not typically the kind of plant you’d find as a heterotroph. Dr Gitte Petersen explained how odd Epirixanthes are. “All the species of the genus Epirixanthes are extremely different from their closest relatives, which are normal, green photosynthetic plants. In contrast Epirixanthes species are small, and pale – really inconspicuous. For some unknown reason, mycoheterotrophy is much more common among monocots and particularly well-known from orchids. However, mycoheterotrophy has also developed in three families of eudicots: Ericaceae, Gentianaceae and Polygalaceae, the latter including Epirixanthes. From an evolutionary point of view, it is relevant to compare all independently evolving groups whether they are monocots or not. By comparing independently evolving lineages, we can understand common evolutionary patterns rather than merely describe unique traits.”

Epirixanthes
Epirixanthes. Photo H. Æ. Pedersen

Being able to ditch photosynthesis means there’s no need for green on the flower stalk. It does make the plant look pallid and unhealthy. You might think that the plant has altered its genes to reduce the presence of green, and you’d be half right. Gitte Petersen and colleagues looked at the effect of heterotrophy not on the genes of the plant, but instead on the genes of the plastids.

Plant cells are complex. Most of the DNA sits in the nucleus, as you’d expect, but not all of it. Some DNA is found in the mitochondria. These organelles are the power plants of the cell and operate like a cell within a cell. They have their own DNA and reproduce separately to the plant cell as a whole. Another organelle with its own DNA is the chloroplast.

The chloroplast is the organelle that helps convert sunlight, gases and water to food. When a plant gets its food from elsewhere, the chloroplast is surplus to requirements. So what happens to its DNA? Why should the character of genome change alter dramatically when a plant becomes a heterotroph? Dr Petersen says that the loss of green is down to the lack of use. “When plants become heterotrophs, they do not need to do photosynthesis themselves. They just steal what they need from their host! Since the chloroplast genome houses a large number of genes involved in photosynthesis, these are no longer needed, and gradually they degrade. Although the chloroplast genomes that we have seen in Epirixanthes are indeed reduced, they are still quite a lot bigger and more intact compared to a monocot mycoheterotroph, Sciaphila thaidanica, that we sequenced a while ago. This species had one of the smallest chloroplast genomes yet discovered.”

While the Epirixanthes the authors looked at had become mycoheterotrophs, the plants hadn’t reacted the same way. In their paper, Petersen and colleagues conclude: “The plastomes of Epirixanthes degrade largely according to the pattern described from other lineages of nonphotosynthetic mycoheterotrophic and parasitic plants. However, it is remarkable that degradation occurs at widely different speeds in the sister lineages in this genus.” Petersen said that the plant was surprising, paradoxically, in how divergent and also how normal the plastid genomes were. “Every time we sequence a new heterotroph plant, we have a very open mind and very few expectations. They keep surprising. So in Epirixanthes, the surprise was the unusual structure of the chloroplast genome. We had no idea that the two species would be so different, but now having discovered that it would be fascinating to see what the remaining species are like.”

“When it comes to the mitochondrial genome, we were most surprised to see how normal it is. Plants have extraordinary diverse mitochondrial genomes, mistletoes – another type of heterotroph – being some of the strangest. But, Epirixanthes has simply no special traits at all.”

With so few mycoheterotrophic dicots, it might seem that the study of Epirixanthes could be a niche. However, instead, it promises to be another perspective on similar problems faced by other plants. Petersen sees Epirixanthes as a useful contrast well beyond other mycoheterotrophs. “Comparisons can equally well be made to monocot mycoheterotrophs or even to the other type of heterotrophic plants: the parasitic plants, which parasitize directly on a plant host. Parasitic plants that lose photosynthesis show almost completely similar patterns of chloroplast evolution. Thus, I think we will see more studies joining results from studies of parasitic and mycoheterotrophic plants. But the major scientific advances may come from studies of complete genomes. Given the advances in sequencing techniques, we will see more and more studies tackling complete nuclear genomes, asking the question: What is the evolutionary consequences of heterotrophy at the genomic level?”

Further reading

Petersen, G., Cuenca, A., Møller, I. M., & Seberg, O. (2015). Massive gene loss in mistletoe (Viscum, Viscaceae) mitochondria. Scientific Reports, 5(1). https://doi.org/10.1038/srep17588

Petersen, G., Zervas, A., Pedersen, H. Æ., & Seberg, O. (2018). Genome Reports: Contracted Genes and Dwarfed Plastome in Mycoheterotrophic Sciaphila thaidanica (Triuridaceae, Pandanales). Genome Biology and Evolution, 10(3), 976–981. https://doi.org/10.1093/gbe/evy064

Petersen, G., Darby, H., Lam, V.K.Y., Pedersen, H. Æ., Merckx, V.S.F.T., Zervas, A. Seberg, O. (2019). Mycoheterotrophic Epirixanthes (Polygalaceae) has a typical angiosperm mitogenome but unorthodox plastid genomes Annals Of Botany. https://doi.org/10.1093/aob/mcz114