Cucumber Mosaic Virus strikes a balance between replication and travel

Viruses are typically made up of genetic material (DNA/RNA) and a protective protein coat. They can’t replicate on their own and must infect into living cells (e.g. in plants or animals) and trick them into producing more virus particles. As such they are not strictly living organisms but I’m bending the definition a bit for this month because I think it is fascinating how Cucumber Mosaic Virus (CMV) can modify both the defences of its host plants and the behaviour of the green peach aphid (Myzus persicae), which transports the virus from plant-to plant.

Aphids are the most prevalent carriers of plant viruses. Virus particles get into the mouthparts of the insects when they feed on sap from virus-infected plants. When these aphids then feed on the sap of another plant, virus particles are “injected” into it. A short feed by an aphid is enough for virus transmission into a plant and evidence suggests that longer feeds by aphids may actually reduce the efficiency of virus transmission (1,2). So, it can be good for the virus if the aphids feed only briefly on the plant. Also, since the aphids are the means of the virus travelling between plants, deterring the aphids from remaining on virus-infected plants is good for spreading the virus.

A recent paper published in PLOS ONE studied the interaction between CMV, the green peach aphid and the plant Arabidopsis thaliana (3). They found that the aphids were less likely to feed from CMV-infected A. thaliana plants and that the aphids on the virus-infected plants had a lower growth rate (Figure 1). When the aphids were transferred to healthy wildtype plants their growth rates recovered to be similar to aphids that had fed on uninfected plants (Figure 1B). The decrease in aphid feeding was due to the production of a chemical aphid feeding-deterrent upon CMV infection (3).

Aphids feed less on CMV-infected A. thaliana plants. Image credit ref 1 distritubed under a CC BY 4.0 licence.

Figure 1: Aphids feed less on CMV-infected A. thaliana plants. (A) Aphid feeding behaviour over 12-hour periods. (B) Aphid growth rates on uninfected (mock) and CMV-infected plants before and after a switch to healthy uninfected plants. Image credit reference (3) distributed under a CC BY 4.0 licence.

How does CMV induce the production of the aphid feeding-deterrent in the plant? Apart from the proteins that are required for virus movement and the protective coat, the CMV genome encodes three proteins: 1a, 2a and 2b. The 1a and 2a proteins are needed for viral RNA replication, but 2a also triggers plant defence responses leading to increased production of the aphid feeding-deterrent (Figure 2) (3).

However, inducing plant defence responses in the plant can backfire on CMV as one of the defence responses is anti-viral RNA silencing, which prevents the production of viral proteins by degrading viral RNAs. To avoid this, the 2b protein inhibits plant defence against the virus by inhibiting antiviral RNA silencing (3).  In this way the protein 2b promotes the accumulation of viral proteins in the cell. However, the 2b protein also inhibits AGO1, a protein that both promotes the production of the aphid feeding-deterrent and inhibits the production of compounds that are toxic to aphids (3). This would decrease the production of the aphid feeding-deterrent and make it more likely that the aphids would be poisoned, which would not help CMV spread to other plants.

Three CMV proteins |(1a, 2a and 2b) modulate plant defences to maximise CMV replication and transport by aphids to other (uninfected) plants. Image modifed by S. Shailes from Figure 10 in reference (3), distributed under CC BY 4.0 licence.

Figure 2: Three CMV proteins |(1a, 2a and 2b) modulate plant defences to maximise CMV replication and transport by aphids to other (uninfected) plants. Image modifed by S. Shailes from Figure 10 in reference (3), distributed under CC BY 4.0 licence.

To be successful at replicating in plants, and be spread to new plants by aphids the CMV virus must balance the downregulation of plant defence responses required for its replication with the need for the production of the aphid feeding-deterrent. This seems to be achieved by the 1a protein inhibiting 2b-mediated inhibition of AGO1 (Figure 2) (3), so that the aphids would be deterred from feeding but not poisoned.

So, using only three proteins CMV can modulate plant defence responses to enable its replication and to encourage aphids to leave the plant in search of a new host for the virus.

References:

(1) Powell, G. (2005) Intracellular salivation is the aphid activity associated with inoculation of non-persistently transmitted viruses. J Gen Virol.

(2) Mauck K. et al (2012) Transmission mechanisms shape pathogen effects on host-vector interactions: evidence from plant viruses. Functional Ecol.

(3) Westwood J.H. et al (2013) A trio of vial proteins tunes aphid-plant interactions in Arabidopsis thaliana. PLOS ONE.

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4 thoughts on “Cucumber Mosaic Virus strikes a balance between replication and travel

  1. Pingback: Morsels For The Mind – 03/01/2014 › Six Incredible Things Before Breakfast

  2. Pingback: Cucumber Mosaic Virus strikes a balance between...

  3. Pingback: One year of blogging at Plant Scientist | Plant Scientist

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