Aphids and their ability to spread viruses are the bane of many farmers’ production forecasts.

Globally, aphids cause billions of dollars in crop damage, and more plant viruses are transmitted by aphids than any other group of insects. But until recently, the complex relationship between the aphid host — a plant virus — and an animal virus was not fully understood. Nor was it understood how those two viruses co-operate to use the aphid to their advantage to expand to new hosts and spread disease.

Researchers at the U.S. Department of Agriculture’s Agricultural Research Service and Boyce Thompson Institute at Cornell University in New York focused their study on the green peach aphid, which feeds on peaches, tomatoes, potatoes, cabbage, and corn while transmitting more than 100 different plant viruses.

One particular virus is the potato leafroll virus (PLRV), which can reduce potato yields by more than 50 percent globally. A series of unexpected discoveries revealed just how destructive the potato virus can be. The PLRV not only uses the aphid for a ride to new hosts but is able to suppress the aphid’s immune system by manipulating a virus protein known to impair plants’ immune systems.

With the aphid’s defences down, the researchers discovered a rapid increase in an insect virus known as Myzus persicae densovirus (MpDNV). And that led to discovering that aphids with more copies of MpDNV were more likely to grow wings.

The significance of this is that green peach aphids rarely grow wings until the fall when the weather is cooler. But with wings earlier in the growing season, the aphid can fly and spread both the potato virus and the insect virus to new hosts, thereby spreading disease.

“We do think this is the result of evolution,” said Dr. Michelle Heck, a USDA scientist. “Both the plant virus and the insect virus have evolved to manipulate the aphid to increase their spread. Viruses that gained this ability by random mutation were more successful and, thus, became more abundant in the population. The insect virus (MpDNV) can cause the aphids to prematurely grow wings in the absence of the plant virus (PLRV), (but) the plant virus may be taking advantage of this by suppressing the aphid’s immune system, since having more winged aphids will also increase (its) spread. This means that an ancestor of PLRV that accidentally suppressed the aphid immune system likely became so successful that it became the most abundant form of PLRV. That is why we can observe this trait in PLRV today.”

While both viruses have a different relationship with the aphid (one is a pathogen, the other a passenger along for the ride) their interests are aligned, which is what encouraged the co-operation.

“We think we have found the first example of co-operation between a plant virus and an insect virus,” said Jennifer Wilson, a PhD candidate in the School of Integrative Plant Science at Cornell University and who is conducting her thesis research with Heck.

Exactly how the potato virus manipulates the P0 protein is still unclear and Heck said it is possible the aphids are exposed to the P0 protein by feeding on plant sap. P0 is a PLRV protein that is expressed inside plant tissue and not inside the aphids themselves.

“We don’t know if the aphids ingest P0 from the plant or not, but we do know that, when P0 is present in the plant, the aphids’ immune systems are suppressed,” said Wilson.

The aphids suck on the leaves rather than chew. Heck said it is possible that the P0 protein is doing something inside the plant that is indirectly affecting the aphids. They do not need to ingest the actual P0 protein for the effect to happen.

“This is one part of the puzzle we are still working on,” she said.

Wing growth on aphids can be triggered by a number of things. The most common is a change in the season when the weather gets cooler. If aphid numbers become too crowded or their food is depleted, they will give birth to young that develop wings. That ability, giving birth to winged or unwinged offspring, is known as polyphenism. The insect virus takes advantage of this phenomenon to trigger the aphid to grow wings and carry it to a new host. But how the virus does this at a time when aphids are not growing wings is still unclear and thought to be by changing how genes in the aphid are expressed during development.

While each virus is capable of spreading infection alone, their work is more successful when co-operating.

“This is something we are testing,” said Heck. “We do think these viruses exist in proximity in nature. Not all the time, but often enough that this co-operation has evolved. PLRV is just one of many plant viruses transmitted by aphids. It would be very interesting to know how those other plant viruses may be manipulating the aphid.”

The researchers are exploring how this new information can be applied to use deadly insect viruses to control pests.

“One new avenue of controlling insect pests, such as aphids, is using deadly insect viruses (unlike MpDNV, which is relatively benign),” said Heck. “Since PLRV suppresses the aphid immune system, it makes the aphids more vulnerable to all insect viruses. Although we haven’t tested it yet, it is possible that PLRV may make aphids susceptible to other insect pathogens like fungi or bacteria. Therefore, a potential long-term application of this research is to use the P0 protein to increase the vulnerability of aphids to insecticidal insect viruses and other pathogens. How exactly to deliver this protein to the aphid to suppress their immune systems remains one of the most challenging aspects of translating our research to the field.”