Barley virus and aphids gang up on wheat

The virus, which is brought into crops on aphid salivia, modifies plant leaves to make them more nutritious for aphids

New research from Pennsylvania State University is uncovering an extraordinary relationship between two aphid species and the barley yellow dwarf virus to the detriment of wheat crops.

The virus, which is brought into wheat fields in the saliva of aphids, modifies the crop leaves by increasing nutrients for the benefit of the aphids. This results in greater reproduction of the insect and therefore greater opportunities for the virus to spread.

“The virus modifies the habitat in ways that benefit its vectors, and, in turn, the aphid vector disperses the virus,” said Mitzy Porras, a recent doctoral graduate in entomology at Penn State University. “Both species (the vector and the virus) benefit from the interaction.”

The aphid species that Porras’s team studied were the bird cherry-oat aphid Rhopalosiphum padi and the corn leaf aphid Rhopalosiphum maidis. Both pests have worldwide distribution.

Normally, when species share the same food source there is some level of competition. But the researchers found that the order of arrival of the aphid species to the wheat affects the outcome for both species.

That outcome is driven by the presence of two strains of the barley yellow dwarf virus (BYDV). R. padi transmits BYDV-PAV and R. maidis transmits BYDV-RMV. The viruses are transported in the salivary glands of the aphids and they invade the plants when the aphids are feeding.

In the absence of viruses, the order for the aphids is that R. padi arrives first and R. maidis arrives later. The foraging of R. padi may affect the food supply of the later arriving aphid. But if R. maidis shows up first, its foraging has a negative impact on both the foraging behaviour and reproduction of latecomer R. padi.

All that changes if the aphids arrive infected with virus strains. The influence of the virus results in R. padi having no problem colonizing the wheat and reproducing. And if R. padi arrives at the wheat first, as it normally does, the virus it carries significantly increases the foraging capacity and reproduction rates of the usually latecoming R. maidis aphids.

The virus stimulates changes in the leaf anatomy by shortening the distance between the vascular bundles and the surface of the leaf and increasing the nutritional content of the wheat leaves, making them easier for the aphids to find and access the sap. The influence of the virus boosts levels of carbohydrates, sterols, and amino acids. Plants with the virus from R. padi saliva have a three-fold increase in fructose and glucose, while the virus from R. maidis influences those concentrations two-fold.

Porras and her team conducted field and laboratory experiments. They grew 360 wheat plants in four lab trays and then randomly selected eight plants from each tray for the experiments. Each plant was caged and exposed to 10 adult aphids/viruses for 10 days according to species. They recorded when each species arrived at the wheat plants, when they started feeding, for how long, their reproductive health, and how their foraging affected the nutritional quality of the plants. The insects were fitted with micro-sensors, which recorded the time it took for the aphids to reach the plant sap (phloem) and the duration of ingestion.

“The virus may modify the anatomical structure of the tissues of the host plant,” said Porras. “This is a result of several changes on different physiological pathways in the plant. If (changes occur in) the area where the aphids have a higher nutrient concentration, (then) the aphids get a better food quality, increasing their fecundity. These strategies between vectors and viruses have evolved for millions of years.”

The virus not only increases the nutrients in the plant but also changes the anatomy of the plants’ leaves, making them easier for aphids to find and access the nutritious sap. This way, they can feed for longer periods, boost their health and have greater reproductive success. And this is what the virus wants. New generations of aphids mean the virus can increase its spread to other aphids and ensure its survival.

“More aphids mean more chances for the virus to be dispersed,” said Porras.

This insect-virus relationship is clearly at the expense of the wheat crop and the primary goal of the research was to better understand the relationship between the aphid and the virus to help develop better controls.

“We should understand how the system virus-vector works to know where the control strategists should focus their efforts,” said Porras.

She said there is mounting evidence that viruses and other pathogens can modify the behaviour of host insects and expand a niche ecosystem all for the fitness and reproductive gains of the pathogen. Further research will uncover more implications of the complex three-way relationships between plants, pests and pathogens.

The research paper “A plant virus (BYDV) promotes trophic facilitation in aphids on wheat” appeared online in August in Scientific Reports.

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