The upside-down Kingdom

Teaching elementary school children the natural world is certainly a challenging task. Most of the time there was an unspoken rule, implicit in each of the classes taught: dichotomies dominated the narratives. Grays are always difficult to remember, so why not stick to black and white? Biology is, by definition, the science of exceptions, the science of “it depends on the species”, it depends on the environment, their adaptations, and evolution.

Today, we come to break with those dichotomies and why not, we give a 180-degree turn to the concepts that shaped us: Welcome to the upside-down kingdom.

Let’s travel back in time for a moment, let’s go precisely to that first biology class where they taught us the main differences between the animal kingdom and the plant kingdom. Yes, animals are heterotrophs because they feed on other living beings and plants are autotrophs because they are capable of making their food. But where do all the exceptions to the rule fit into this classification? In the natural world, where else?
Some plants do not perform photosynthesis and take advantage of the efforts of others, known as parasitic plants. There are approximately 3900 species of parasitic plants, which corresponds to a little more than 1% of all flowering plant organisms (angiosperms) with a global distribution of very varied climates.

These plants can be classified as hemiparasites if they possess chlorophyll, thus being able to perform photosynthesis, but they will always need some nutrients from their host (although some can live independently of this); on the contrary, they will be called holoparasites when they do not possess chlorophyll and depend completely on their host. And of course, these plants, in turn, can have general or specific hosts (we like to call them “anyone is fine” and “exquisite”, respectively).

And of course, this change in strategy or way of life towards parasitism implies that the plant goes through a series of morphological and molecular variations that leave its famous autotrophism in the background.
Many of these plants, especially the holoparasites, do not even have leaves (or are reduced to scales), which is why they are very difficult to distinguish at a glance, being able to lodge either in the stem (perfectly camouflaged, of course) or in the roots (below the ground) of their host. Consequently, they are only visible during flowering periods, as what escapes from this camouflage are the striking colors of their reproductive structures, the dreaded flowers.

They generally present modified roots called haustoria that penetrate the host plant to locate the conducting tissues and absorb the elaborated sap (with all the nutrients and food that were manufactured by the poor infected plant). Furthermore, haustoria are the only roots that these organisms possess since the root that was in the soil, generally and after a certain time, perishes.

All these processes and all these structures (the ability to camouflage, the modified roots, the absence of leaves) are extremely sophisticated, they have been designed to resemble the physiological processes of the host and deceive its defense mechanisms. However, the plant being parasitized is not left behind, as it is capable of producing more lignified tissue (hard) or producing substances that inhibit the growth of the haustoria to defend itself from the attack, a true silent battle.

At the genetic level, we can observe that one of the most important modifications is the loss of the ability to generate chlorophyll and perform photosynthesis, basically, the characteristics that best describe the plant kingdom, what a twist, right?

Yet there is more. Genes from parasitic plants have been found coming from the host, so it is believed that there was and is a genetic exchange between both species, a phenomenon known as horizontal gene transfer (HGT), which is common in bacteria, but not so much in eukaryotic organisms like plants.

For this particular case, a hypothesis has been proposed that involves the complete mitochondria of the host plant passing through the contact point and entering the cells of the parasite, where they merge to generate true chimeric mitochondria, allowing genetic exchange between them (they not only wanted to steal nutrients from them but now they decide to go for the genes too). Subsequently, thanks to the incredible capacity of plant cells to transform into other types of cells (totipotentiality for friends), they can give rise to a new shoot that already presents the genes of both plants.

Now, it’s time to exemplify and put a face to so many parasitic plants, here is the genus Cuscuta. These little friends are very common holoparasites and are mainly known by scientists and agronomists due to their destructive capacity, since they do not have leaves, they form true networks with their yellowish stems that completely envelop the top of a tree and parasitize it in different parts (don’t even imagine what it does to helpless herbaceous plants, which it can envelop and kill in a matter of days). To facilitate the transport of nutrients, this plant is capable of self-parasitizing to create real shortcuts and, in this way, no cell is left without its portion of rich sap.

These plants have been studied to elucidate how they search for their victim because, at the beginning of development, they are like any ordinary plant, and they can survive alone due to the energy reserves stored both in the seed and in the first leaves (cotyledons). However, once this reserve is depleted, in the hypothetical case of not having chlorophyll, it is necessary to look for a host that provides nutrients, water, and mineral salts to continue its development.

Dr. Consuelo de Moraes, a biologist from Penn State, carried out a series of experiments that yielded surprising results. First, she placed a Cuscuta genus plant between two other pots, one empty and the other with a plastic plant. The most extreme part of the plant did not lean towards either of the two, which suggests that they are not physical factors (entry and change of light). In a second experiment, it was tested with a real tomato plant in different conditions (light off, light on, an obstacle between the parasite and the tomato plant, both plants enclosed in boxes connected by a tube), and in all cases, it approached the tomato plant. To conclude, it was tested with two different plants, the same tomato plant, and wheat. Regardless of the different combinations, the plant always chose the succulent tomato. It is guided by chemicals in the air (similar to our sense of smell) that allow this species to choose its food, I mean, its next victim.

After this tour of the wonders of parasitic plants, capable of “eating others”, it is time to see the other side of the coin or the other side of the exception. This would be, animals capable of photosynthesis.

Introducing: Elysia chlorotica, our prodigious mollusk, which not only is capable of photosynthesizing assimilates, but curiously also has a leaf-like appearance. This gastropod mollusk or sea slug is capable of surviving for months thanks to its sunlight-based diet. And of course, this information surprises us; the surprise is the result of a lifetime associating photosynthesis exclusively with plants or algae — Finding an animal that directly or indirectly benefits from the sun is truly iconic.

Elysia is capable of photosynthesis because it maintains an endosymbiotic relationship with Vaucheria litorea, a green-yellow marine alga that grows in filamentous form and constitutes the sea slug’s diet. Through a phenomenon called kleptoplasty, our photosynthetic animal not only feeds on the alga but also assimilates its chloroplasts (the photosynthetic organelles), to take advantage of its wonderful autotrophic capacity and nourish itself when specimens of other algae that it usually consumes are scarce.

The amazing thing about its way of life lies in how the alga’s chloroplasts, once inside the sea slug’s digestive diverticula, can carry out their photosynthetic functions without the proper replenishment of proteins, which was possible thanks to the information contained within the algal cells. This means that Elysia not only had to be very careful when digesting its favorite algae but surely had a trick up its sleeve that allowed it to keep all machinery running.

And here is when the story of genetic exchange repeats itself; in 2018, researchers from the University of Queensland, Australia, conducted analyses on the RNA sequences of E. chlorotica to test the idea that the sequestration of chloroplasts from Vaucheria leaves a significant mark on gene expression during the development of our host sea slug. These studies culminated in strong acceptance of this hypothesis, and they demonstrate that upon exposure to and ingestion of V. litorea’s plastids, genes related to oxidative stress response (i.e., compounds called free radicals that can be extremely harmful to the animal) are much more regulated. All this to say that indeed, our sea slug has developed a suite of molecular machinery to respond, tolerate, and maintain its symbiosis with the stolen chloroplasts from the marine alga.

When not, evolution and biodiversity demonstrate that no dichotomy encompasses such variation, that kingdoms are neither black nor white. Today, a parasitic plant like Cuscuta and a photosynthetic animal like Elysia come to show that, once again, in biology, there are no exceptions, only an excessive amount of nuances and variety.