How ferns learnt to live in the shadows

We thought we knew how plant evolution worked – genes mutate, or are reshuffled through sex, and natural selection does the rest. In the past few years, however, we’ve learnt of another way – genes can be pilfered from a different species. A spectacular example was reported this April in Proceedings of the National Academy of Sciences. According to a team led by Fay-Wei Li at Duke University, North Carolina, ferns may have gained their ability to thrive in the shade by acquiring a gene from the hornwort, a tiny moss-like plant.

Toward the end of the Cretaceous period, when dinosaurs ruled the Earth, flowering plants took over as the predominant flora and created thick forest canopies that left the ancestors of modern ferns to wither in the shade. They didn’t. They adapted to low-light conditions and researchers believe that was thanks to a light-sensing protein called neochrome.

Light-sensing proteins help plants orient their leaves towards light. Most detect only blue light but neochrome equips plants to sense red light as well. That gives ferns an advantage over fellow shade-dwellers because the leaf pigments in the canopy absorb most of the blue light so that predominantly red light reaches the forest floor. Armed with neochrome, ferns can orient their photosynthetic equipment towards this red light and absorb enough energy to thrive.

What came as a surprise to Li, however, was how ferns got hold of the gene that produces neochrome. The acquisition appears to be the result of horizontal gene transfer (HGT) – the direct DNA transmission from one species to another that is common in microbes but rare in animals and plants.

“It’s interesting to think that maybe we see so many ferns today because of a genetic gift from a bryophyte moss-like plant,” says Li. Li calculated that the moment of exchange came roughly 180 million years ago, around the time that ferns began to diversify and thrive under the canopy. “These results are strong,” says Jeffrey Palmer who studies horizontal gene transfer in plants at Indiana University.

Scientists have reported more and more examples of gene swapping in plants.

When Li set about tracing the evolutionary history of the fern’s neochrome gene a few years ago, he didn’t have much to go on. That changed when an international team of scientists released genome data from hundreds of plants as part of an initiative called the 1,000 Plants Project. Li wrote software to search the databases for genes with similar sequences to neochrome. “Then one night my laptop popped up with the information that ‘oh, you’ve found a neochrome gene in hornworts’,” says Li. “I didn’t sleep well that night. I kept thinking ‘oh wow’.”

Hornworts are distant relatives of ferns, so his discovery demanded an explanation. One possibility was that ferns and hornworts share a common ancestor that had the gene and the rest of the descendants, including all trees and flowering plants, lost it. But while ferns and hornworts diverged from their common ancestor 400 million years ago, Li’s analysis suggested that their respective neochrome genes had been evolving separately for just 180 million years.

All the evidence pointed to a direct transfer from hornworts to ferns.

How would a gene travel from the mossy hornwort to a fern? It’s not hard to imagine that down on the moist forest floor these two species could have gotten up close and personal during the sexual phase of the fern’s life cycle. The familiar fern plant with its large waxy fronds represents the asexual phase. But the spores, visible as neat brown dots under the fronds, give rise to a delicate, fingernail-sized plant. Cradled in its moist leafy tissue, sperm and egg are produced, and mingle. Because this stage of the plant has no protective waxy layer, the moist and intimate mingling process is exposed to other plant species growing in close contact. Hornworts, it seems, joined in with the fun. Li suggests that a virus jumping between the two plants might have acted as a vehicle for the neochrome gene.

Over the past decade scientists have reported more and more examples of this kind of gene swapping in plants, but few transferred genes have played such a fundamental role in the plant’s survival. In this case it’s different. For ferns, “plant-to-plant horizontal gene transfer appears to have had a big evolutionary impact”, says Li.

Palmer is more cautious. It’s hard to prove that one particular gene was critical to fern evolution, he says. But if the evidence continues to stack up, this study would “show that plant-to-plant horizontal gene transfer can be adaptively important.”