They’re not mushrooms. A bizarre parasitic plant violates all the rules of biology

They're not mushrooms. A bizarre parasitic plant violates all the rules of biology

Filip Husnik / OIST / New Phytologist

They're not mushrooms. A bizarre parasitic plant violates all the rules of biology

Balanophora is exempt

A new study explores the evolutionary mysteries of a rare parasitic plant, with some of the world’s smallest flowers and seeds, that has lost much of what defines it as a plant — but retained enough to function as a parasite.

At the base of moss-covered trees, deep in the mountains of Taiwan and Japan, or hidden in the subtropical forests of Okinawa, grows something that many could mistake for a mushroom. It is, in fact, a very unique plant, with some of the smallest flowers and seeds in the world.

Without chlorophyll to carry out photosynthesis and without a root system to supply water from the soil, the Balanophora evolved a set of extreme characteristics to survive entirely as a parasite in the roots of specific local trees.

Some species and populations produce seeds without any fertilization — a extremely rare phenomenon in the plant kingdom.

The enigmatic genre Balanophoranamed for its resemblance to acorns (from the Greek balanos, acorn; phoros, bearer), has long intrigued biologists and, given its rarity and preference for very specific environments, today threatened by human interference, it has been difficult to study it beyond isolated populations.

But now, researchers from the Okinawa Institute of Science and Technology (OIST), Kobe University and Taipei University have joined forces to survey the Balanophora throughout their scarce and difficult-to-access habitats.

recently published in New Phytologisttraces the evolutionary history of the plant, shows how its organelles work in unexpected ways to accommodate a parasitic way of life, and paves the way for future research into this “strange” ancestor.

“A Balanophora lost much of what defines it as a plantbut retained enough to function as a parasite. It is a fascinating example of how something so strange can evolve from an ancestor that looked like a normal plant, with leaves and a normal root system”, summarizes Petra Svetlikova, researcher at OIST and first author of the study, at the institute.

Plastids, genomes and shrinking island habitats

A common characteristic in parasitic plants is that, as dependence on the host increases, their plastidosan umbrella term for plant organelles, including chloroplasts in photosynthetic plants, tend to lose genes, or even to disappear completely.

But despite being completely dependent on host trees for all of its nutritional needs, the Balanophora kept the plastidsalbeit in a drastically reduced form.

In non-parasitic plants, up to 200 different genes they can encode the structure of plastids; in Balanophora, only 20 left.

At the same time, researchers discovered that more than 700 proteinss are imported into the plastids from the cytoplasm, suggesting that, even in this reduced version, the plastids continue to play a vital role.

“It was surprising to see that Balanophora plastids continue to be involved in the biosynthesis of many compounds unrelated to photosynthesis”, explains the professor Filip Husnikresponsible for the Evolution, Cell Biology and Symbiosis Unit at OIST, and lead author of the study.

“This suggests that the order and timing of plastid reduction in non-photosynthetic plants is similar to what happens in other eukaryotessuch as the parasite that causes malaria, Plasmodium, which originated from a photosynthetic ancestor”, adds Husnik.

By collecting samples from various populations of Balanophorathe team managed build the “tree of life” of the genre and understand how it diversified throughout the subtropical islands of East Asia.

A Balanophoraceaethe family to which the genus belongs Balanophorais one of the oldest fully parasitic plant familieshaving diversified in the mid-Cretaceous, around 100 million years ago — and, therefore, it is also one of the first groups of land plants to have lost photosynthesis.

Another intriguing question that these plants leave open is the reproductionwhich varies markedly from population to population.

Some species require fertilization to produce seeds; others still have the additional capacity to produce seeds without fertilizationthe call facultative agamospermy; and there are also species that are obligately agamospermic, that is, they never reproduce sexually.

“Obligatory agamospermy It is extremely rare in the plant kingdombecause it tends to have many negative effects — lack of genetic diversity, accumulation of harmful mutations, dependence on specific conditions, greater risk of extinction, and so on,” explains Svetlikova.

“Interestingly, we discovered that species of Balanophora obligatorily agamospermic they were all island species — and we speculate that more species of Balanophora they may be facultative, or even obligatory, agamosperms, adds the researcher.

One of the advantages of this reproductive strategy is to allow a single female plant to propagate to new islands, quickly colonizing the very specific niche where it thrives: the dark, damp undergrowth, where few other plants can survive.

Despite the ability to clone itself, Balanophora is extremely selective in choice of host: each population parasitizes only a few tree species. This, unfortunately, also makes these rare and unique flowers more vulnerable.

“Most known habitats of Balanophora is protected on Okinawa, but populations face extinction due to tree felling and unauthorized collection”, highlights Svetlikova.

“We hope to learn as much as possible about this fantastic and ancient plant before it’s too late. It’s a reminder of how evolution continues to surprise us”, concludes the researcher.

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