The genome of Sapria himalayana is rife with gene loss and theft

For most of their lives, plants in the Sapria genus are barely anything — thin ribbons of parasitic cells winding inside vines in Southeast Asian rainforests. They become visible only when they reproduce, bursting from their host as a dinner plate–sized flower that smells like rotting flesh.

Now, new research on the genetic instruction book of this rare plant reveals the lengths to which it has gone to become a specialized parasite. The findings, published January 22 in Current Biology, suggest that at least one species of Sapria has lost nearly half of the genes commonly found in other flowering plants and stolen many others directly from its hosts.

The plant’s rewired genetics echo its bizarre biology. Sapria and its relatives in the family Rafflesiaceae have discarded their stems, roots and any photosynthetic tissue.

“If you’re out in the forest in Borneo and these [plants] aren’t producing flowers, you’re never even going to know they’re there,” says Charles Davis, an evolutionary biologist at Harvard University.

For years, Davis has been studying the evolution of this group of otherworldly parasites, which includes the largest flower in the world, Rafflesia arnoldii (SN: 1/10/07). When some genetic data showed a close relationship between these parasites and their vine hosts, Davis suspected horizontal gene transfer. That’s where genes move directly from one species to another — in this case, from host to parasite. But no one had yet deciphered the genome — the full genetic instruction book — for these plants.

So Davis and his team sequenced many millions of pieces of Sapria himalayana’s genome, assembling them into a cohesive picture. When the team analyzed the genome, they found an abundance of oddities.

About 44 percent of the genes found in most flowering plants were missing in S. himalayana. Yet, at the same time, the genome is about 55,000 genes long, more than that of some other nonparasitic plants. The count is inflated by many repeating segments of DNA, the team found.

Loss of the chlorophyll pigments responsible for photosynthesis is common in parasitic plants that rely on their hosts for sustenance. But S. himalayana appears to have even scrapped all genetic remnants of its chloroplasts, the cellular structures where photosynthesis occurs.

Chloroplasts have their own genome, distinct from the nuclear genome that runs a plant’s cells and the mitochondria that produce energy for the cells. S. himalayana seems to have lost this genome altogether, suggesting that the plant has purged the last remnants of its ancestral life that allowed it to make its own food.

“There is no other case” of an abandoned chloroplast genome among plants, says Davis. Earlier work by other researchers had suggested that the genome may be missing. “Our work clearly verifies that indeed it’s totally gone,” he says, noting that even genes in S. himalayana’s nuclear genome that would regulate components of the chloroplast genome have vanished.

It may be too early to declare the chloroplast genome completely missing in action, cautions Alex Twyford, an evolutionary biologist at the University of Edinburgh who was not involved with this research. It may be difficult to definitively prove the genome is gone, he says, especially if the chloroplast is “unusual in its structure or abundance” and therefore difficult to identify.

Among the remaining parts of the nuclear genome, the team also found that more than 1 percent of S. himalayana’s genome comes from genes stolen from other plants, likely its current and ancestral hosts.

The potential scale of the vanished genome and the volume of repeating bits of DNA are “insane,” says Arjan Banerjee, a biologist at the University of Toronto Mississauga also not involved with this study. The “industrial scale” of the plant’s gene theft is also impressive, he says.

There are still plenty of weird elements left in S. himalayana’s genome to explore, says study coauthor Tim Sackton, an evolutionary biologist also at Harvard. For example, the plant has bloated its genome with extraneous DNA, while most parasites streamline their genomes. “There’s something weird and different going on in this species,” he says, adding that many of the DNA fragments the parasitic plant is stealing from its host don’t appear to encode any genes, and likely don’t do anything important.

The new discovery illustrates the level of commitment S. himalayana and its relatives have given to evolving a parasitic lifestyle, and provide a comparison to other extreme plant parasites (SN: 7/31/20). And for Davis, plants like S. himalayana can help researchers determine some of biology’s limits. These plants have lost half their genes, yet they still survive, he notes. “Maybe these organisms that stretch the boundaries of existence tell us something about how far the rules can be bent before they can be broken.”