Aphids and plant viruses – friends or foe? Open Access

Up to 50% of plant diseases worldwide are caused by plant viruses, leading to significant yield loss and affecting economically important crop plants. The increase in global population means continuously increasing demand of food. Virus-infected plants often exhibit typical symptoms such as yellowing or mosaic symptoms on the leaves (Figure 1), fruit deformation, and stunted plant growth amongst many others.

A majority of plant viruses are vectored by insects such as aphids. Aphids also cause direct damage to plants from their feeding activities. Aphids can produce a vast number of offspring in a short amount of time. They are present all year round in many places worldwide, which makes them a formidable insect pest. Insecticide remains the main method to control aphid population. However, continuous use of insecticide leads to widespread insecticide resistance. The green peach aphid (Myzus persicae) has developed several mechanisms to overcome at multiple classes of insecticides, posing a real problem to growers. Climate change and warmer winter widen the geographical spread and active period of aphids. Combination of integrated control methods and efficient monitoring is often the most sustainable way to control aphid population in the field.

Studies have shown that plant viruses can alter how plant ‘taste’ and ‘smell’ to insects that vector them. In certain cases, a plant virus can render its host plant more attractive to aphids. Since plants are not mobile, virus transmission is more likely to happen if aphids are attracted to come and feed on virus-infected plants, ensuring virus spread and persistence in the environment.

There are two main ways of how aphids can vector plant viruses. These are determined by whether the virus particles are being circulated or not in the aphids’ body. Non-circulative (non-persistently) transmitted plant viruses are short-lived in the aphids. Virus particles are retained in the aphid’s mouthpart and was not internalised into the aphid gut. Aphids only need to feed on the virus-infected plant for a short period of time to pick up the virus, often within minutes. This is a problem as most insecticides do not act fast enough to kill aphids before virus transmission occurs. In contrast, circulative (persistently) transmitted plant viruses require longer feeding period by the aphids to enable virus transmission. Virus particles are taken up into the aphid’s body, cross multiple membrane barriers, circulated in aphid’s gut and salivary gland, and finally exit the aphid through its saliva during feeding. In most cases, aphids do not pass the plant virus that they carry to their offspring.

Many studies have been done on how plant viruses can influence its vector behaviour and fitness. Tobacco (Nicotiana tabacum) and Arabidopsis (Arabidopsis thaliana) plants are widely used in plant science research, often known as model plants, due to their ease of manipulation and availability of genetic resources. Here, I will outline two examples utilising tobacco and Arabidopsis, which showed how plant viruses alter aphid vector–host plant interaction. Both studies utilised a cucumovirus, Cucumber mosaic virus (CMV) and M. persicae. CMV is a plant virus with an extremely wide host range. CMV is able to infect more than 100 species of plants including many agriculturally important crop plants. M. persicae is a generalist aphid, able to colonise many plant species, and known to vector more than 80 known plant viruses (Figure 2).

For aphid experiments, clip cages are often used to contain aphids on the leaves to enable accurate observation (Figure 3). Aphids feeding on CMV-infected tobacco plants exhibited higher survival rate and produced more offspring. In contrast, aphids on CMV-infected Arabidopsis plants produced fewer offspring, gain less weight, and spend less time feeding compared to those on non-infected plants. The study showed that this is primarily due to an increased production of a plant secondary metabolite known as glucosinolates. CMV infection leads to an increased production of an indole glucosinolate, 4-methoxy-3-indolylmethyl, which is a known aphid-feeding deterrent compound.

From these two examples, the hypothesis was that in tobacco–CMV–aphid case, it is favourable for CMV to allow aphid population to build up. Whilst in the Arabidopsis–CMV–aphid case, reduced aphid fitness on virus-infected plant may promote vector dispersion, and thus, viruses spread to neighbouring plants. This highlighted that the nature of plant–virus–vector interactions is species-specific. Plant virus can also influence plant volatile emission, essentially how the plants smell, making virus-infected plants more or less attractive to aphids. Understanding how plant viruses can alter how plants ‘taste’ and ‘smell’ to its aphid vectors will enable a more accurate way to reduce plant virus spread.

It is not yet well understood what biological factor determines aphid vectoring capacity. Another rising area of research is to study the effect of aphid bacterial endosymbionts on aphid–plant–virus interactions. Aphids harbour bacterial endosymbionts in their body in a symbiotic relationship throughout their lifetime. These bacterial endosymbionts are often vital to enable aphids to withstand environmental stresses and escape predation from parasitoid wasps. The author currently utilises the bird cherry oat aphid (Rhopalosiphum padi) and grain aphid (Sitobion avenae) to study bacterial endosymbionts that affect aphid’s efficiency to vector Barley yellow dwarf virus (BYDV). BYDV is aphid-vectored virus, causing damage to cereal crops in the UK and Europe. The research output will aim to enable the identification of certain aphid species or populations which poses high risk as efficient virus vectors by using their bacterial endosymbionts profile as indicator. This can aid a more efficient monitoring effort in the field and optimise control methods.

A majority of plant viruses and their aphid vectors have a wide host range and can infect both crop and non-crop plants. Plant viruses on wild plants and weeds have been reported, but the role of wild plants and weeds as reservoir hosts still remains understudied. Most agricultural lands are bordered with unmanaged habitats. Plant virus disease outbreaks in crops still occur despite the use of virus-free planting materials. Virus ecology is another emerging area of research to understand the influence of plant viruses outside the agricultural ecosystem.

In regard to plant health, plant breeding to produce crop varieties with increased tolerance to withstand virus infection can aid in minimising crop losses due to viral diseases. In England, the laws are evolving, whereas the Genetic Technology (Precision Breeding) Act 2023 allows for precision breeding, which includes gene editing, to be performed provided that the resulting crop is within the range of what could be achieved through traditional breeding. Plant viruses, however, will continue to evolve as resistant breaking virus strain. In addition, aphids as virus vectors are continuously gaining widespread tolerance to insecticides. Long-term insecticide usage is not economically sustainable and can harm other beneficial insects and the environment. Fundamental research to understand the behaviour of aphids and the plant viruses they vector will enable growers to anticipate incoming risk of virus epidemic and to deploy appropriate control measures.

• Carr, et al. (2019) https://pubmed.ncbi.nlm.nih.gov/30709497/

• Westwood, et al. (2013) https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0083066

• Tungadi, et al. (2017) https://pubmed.ncbi.nlm.nih.gov/28468686/

• Mauck, et al. (2010) https://pubmed.ncbi.nlm.nih.gov/20133719/

Trisna is a plant virologist based at Keele University in Staffordshire, UK. Trisna gained her PhD in 2014 from the University of Cambridge, UK working with John Carr. She then remained at Cambridge as a postdoc from 2014-2019 where she continued working on plant viruses, using both molecular biology and entomology approaches. From 2019-2022, Trisna worked as a postdoc at the National Institute of Agriculture Botany in Kent, UK on spotted wing Drosophila, a major insect pest in the soft fruit industry. In 2022, Trisna joined Keele University to build her own research group, where she focuses on aphids as plant virus vectors. Email: [email protected].