Pretty Sly for a Whitefly

One of the world’s worst agricultural pests corrupts the alarm signals of plants, disarming those that otherwise might prepare for an assault.

Three whiteflies sitting on a leaf.
The whitefly, one of the world’s worst invasive pests, will chow down on all sorts of crop plants. (Runzhi Zhang)

When plants are bitten by insects, they release a chemical scream—a cocktail of compounds that travel through the air. Some deter pests directly by confusing or repelling them; others indirectly protect plants by summoning predatory ants or parasitic wasps. Still others raise the alarm in parts of the plant that aren’t yet under attack, telling them to ramp up their defenses in preparation. These same alarms can spread over entire fields, warning other plants to prep their defenses. We can’t perceive these signals, but to plants, they’re as foreboding as wailing sirens.

But Peng-Jun Zhang and Xiao-Ping Yu from China Jiliang University have shown that one of the world’s worst agricultural pests—the silverleaf whitefly—can hack this communication system. When the whiteflies bite, they somehow change a plant’s airborne warnings so that they convey information about the wrong threat. Deceived, the neighboring plants invest in the wrong defenses and become more susceptible to the whiteflies. These pests, by seeding entire fields with faulty intelligence, can prime the plants ahead of them for their arrival.

This might help explain why the silverleaf whitefly is so devastatingly invasive. It causes billions of dollars’ worth of damage every year and feeds from some 500 types of plants—squash, cucumber, cotton, melons, eggplant, cabbage, and more. Wherever it goes, it drains nutrients from its hosts, covers their leaves in sticky liquids that promote the growth of molds, and infects them with devastating viruses. Originating somewhere in Africa, it has spread across the entire world over the past two centuries.

In very rough terms, plants have two main defense systems: one for insects and other plant-eating animals, and another for infectious microbes. The former centers on jasmonic acid, a hormone that triggers the production of insecticidal toxins. The latter centers on salicylic acid, a different hormone that triggers the production of antimicrobials, or tough molecules that barricade a plant’s cells against besieging microbes. In 2007, Sonia Zárate and Louisa Kempema from the University of California at Riverside showed that whiteflies induce the wrong defense—the antimicrobial salicylic-acid one, instead of the anti-insect jasmonic-acid one.

Now Zhang and Yu have expanded on that finding by showing that these inappropriate defenses can cascade through an entire field. The team placed pairs of tomato plants in separate glass chambers, connected by tubes that allowed air to pass between them. If the first plant was infested with caterpillars, the second ramped up its anti-insect defenses. When caterpillars attacked that second plant, they had a tougher time and grew more slowly.

But if the first tomato was infested with whiteflies, everything went topsy-turvy. The plant released a very different airborne cocktail, which compelled its neighbor to turn down its anti-insect defenses and turn up the antimicrobial pathway. If whitefly larvae ended up on that misinformed tomato, they actually grew faster than they would have on plants that had received no warnings at all.

It’s not clear how the whiteflies hack the plants’ messages, but the consequences are evident. By simply biting a plant, whiteflies can make surrounding plants into more suitable hosts for the next generation of whiteflies. “It’s a really interesting finding,” says Petra Bleeker from the University of Amsterdam. Although the whitefly larvae gain only a small edge on the neighboring plants, Bleeker says, that small effect could add up across time and space. It would be interesting to do a larger-scale experiment to see how these corrupted messages play out over an entire field or greenhouse.

“It is super interesting to step into this invisible world,” says UC Riverside’s Zárate. “It appears that the whitefly is ahead in the arms race … but the plant may be preparing itself and neighboring plants to do battle with the viruses that the whitefly is known to harbor.” If these are the true threat, it might make sense for infested plants—and their neighbors—to steel themselves against imminent infections instead of approaching insects. “The problem for the plants is that this also benefits the whiteflies,” says Ted Turlings from the University of Neuchâtel, who was involved in the new study.

Turlings suggests that it might be possible to change these responses to our advantage, perhaps by breeding or modifying plants to launch the anti-insect defenses in response to whitefly attacks.

He is also leading a five-year project called Agriscents to create machines that can eavesdrop on the chemical alarms of plants, warning farmers of infestations in real time, before they’re evident to the naked eye. “The ultimate goal is to have robots sniff plants and inform farmers about the presence of pests,” says Turlings. “The farmer—or the robot—can then apply a pesticide at the right time and in the right place, long before the insects do too much damage.”

Such a system might be years in the making, but for now, there already is an animal that does something similar. Encarsia formosa is a parasitic wasp that exclusively targets whiteflies, and as Zhang and Turlings discovered six years ago, it homes in on one of the airborne chemicals released by infested plants. The whiteflies can fool their hosts, and the neighbors of their hosts, but they can’t fool the wasp.