A plant gene may have helped whiteflies become a major pest

At some point between 35 million and 80 million years ago, a whitefly landed on a leaf and started sucking its sweet sap. That fateful meal provided more than sugar. Somehow, a gene from the plant wound its way into the whitefly’s genome, a new study suggests, and may have helped its ancestors become one of the most notorious agricultural pests today.

The gene helps plants neutralize and safely store certain toxic molecules they use to deter herbivores. In whiteflies (Bemisia tabaci), it allows the insects to feed on flora, undeterred by one of the plant world’s best chemical weapons, researchers report March 25 in Cell. This plant-to-insect gene swap is the second ever documented, and the clearest example of an insect effectively commandeering the genetic toolkit of their “prey” to use it against them.

“Ten or 20 years ago no one thought that this kind of gene transfer was possible,” says Roy Kirsch, a chemical ecologist at the Max Planck Institute for Chemical Ecology in Jena, Germany, who wasn’t involved in the study. “There are so many barriers a gene must overcome to move from a plant to an insect, but this study clearly shows that it happened, and that the gene provides a benefit to whiteflies.”

Gene swapping is common among bacteria (SN: 10/31/11), and occasionally happens between gut microbes and their animal hosts. Known as horizontal gene transfer, this process allows organisms to bypass the plodding nature of parent-to-offspring inheritance and instantly acquire genes shaped by generations of natural selection. But a genetic jump from plants to insects, lineages separated by at least a billion years of evolution, has been documented only once before, also in whiteflies.

Whiteflies are aphidlike insects that feed on over 600 different plants around the globe. The pernicious pests’ wide-ranging diet stems in part from their ability to evade many common plant defenses (SN: 4/4/19). While looking for genes that underlie this ability, researchers in China stumbled upon something strange in three closely related whitefly species — a gene, called BtPMaT1, not known to exist outside of plants.

Two scenarios could explain such a pattern. Either the gene arose in the common ancestor of plants and insects and was subsequently snuffed out on all intervening branches of the tree of life, or whiteflies somehow acquired the gene from plants. Because plants and insects are so distantly related, the latter scenario is “much, much more likely,” says Kirsch. These three whitefly species split some 35 million years ago, suggesting they got the gene before then. But close relatives that diverged 80 million years ago lack the gene, suggesting the transfer happened within that window.

The gene allows plants to stow a common class of defensive chemicals called phenolic glycosides by neutralizing the toxins until herbivores start munching. “Phenolic glycosides are very toxic to insects,” says study coauthor Ted Turlings, a chemical ecologist and entomologist at the University of Neuchâtel in Switzerland. The possibility that whiteflies might use a plant detoxification gene to tolerate plant toxins tantalized Turlings’ colleagues in China.

The researchers inserted a bit of RNA into tomato plants in the lab. Once ingested by whiteflies, the RNA was designed to disable their BtPMaT1 gene. Then, the team let whiteflies loose. After a week of feeding on five genetically altered plants, nearly all of the approximately 2,500 whiteflies were dead, compared with only about 20 percent of those that fed on unaltered plants. Such a drastic effect suggests this gene plays an important role in helping whiteflies bypass plant defenses, Turlings says. 

How exactly a plant BtPMaT1 wound up in whiteflies remains a mystery. Viruses can accidentally shuttle bits of DNA between hosts, and Turlings suspects this likely happened here. “This is an extremely rare event, but when you’re talking about billions of insects and plants interacting over millions of years, it becomes more possible,” he says. Horizontal gene transfer might possibly be “an important mechanism for pests to gain abilities to deal with plant defenses.”

The first documented plant-to-insect gene swap, reported September 23 in Scientific Reports, also occurred in whiteflies, though the function of the gene in that swap is less clear. It may not be a coincidence, though, that the two known examples of such an event occurred in the same herbivorous insect.

“The lives of whiteflies and their plant hosts are closely intertwined,” says Shannon Soucy, an evolutionary microbiologist at Dartmouth College who wasn’t involved in the research. That consistent exposure primes the system to be ready for this kind of event, she says, which ultimately allowed whiteflies to use this plant defense gene against its maker.