Like many plant viruses, cucumber mosaic virus (CMV) requires a transport system (seed, animals, insects, wind, or water) to move between plants. In nature, aphids primarily transmit CMV in a non-persistent manner (i.e., the virus loosely attaches to the insect mouthparts and does not infect the insect). More than 70 different aphids, including Myzus persicae, vector CMV to over 1,000 plant species. Once the virus is introduced into the plant through aphid feeding, CMV causes various changes in the host, including effects on immunity nutrient accumulation and visual or olfactory cues, which influence aphid behaviour. These effects on aphid host preference, settling or flight, feeding and reproduction can contribute to an increase in the rate of CMV transmission by aphids.
Work by the Carr Group has shown that tobacco (Nicotiana tabacum cv. Xanthi) plants infected with some CMV strains (Fny or LS) are more susceptible to aphid infestation by M. persicae. Thus, aphids confined on CMV-infected tobacco plants survived for longer and produced more offspring than on virus-free plants. Interestingly, it was found that tobacco plants infected with Fny-CMVΔ2b (a mutant version of the Fny strain that cannot express the 2b counter-defence protein) were toxic to M. persicae. How Fny-CMVΔ2b induced toxicity to aphids in tobacco remained unknown until 2020, when Tungadi and colleagues published a paper in Molecular Plant Pathology showing that a component of the CMV replication complex, the CMV 1a protein, triggers synthesis of one or more substances toxic to Myzus persicae. It was concluded that aphids are not poisoned on tobacco plants infected with wild-type Fny-CMV because the toxicity-inducing effect of the 1a protein is somehow neutralized by the 2b protein.
Based on the known properties of the CMV 2b protein, there were three possible hypotheses to explain how the 2b protein could counteract CMV 1a protein activity: binding to the 1a protein; interfering with small RNA pathways controlling 1a-induced aphid resistance; or inhibiting the action of jasmonic acid, a phytohormone that controls anti-insect defences. In a recent study by Arinaitwe et al., the jasmonic acid hypothesis was tested using plants insensitive to Jasmonic acid by engineering Xanthi tobacco plants to accumulate decreased levels of the mRNA encoding the factor CORONATINE-INSENSITIVE 1 (COI1). COI1 is core to the perception of jasmonic acid. Arinaitwe and colleagues assessed Myzus persicae performance on engineered plants infected with Fny-CMV or CMVΔ2b. They showed that aphid survival and reproduction on transgenic plants, with decreased COI1 expression, were not decreased when these plants were infected with CMVΔ2b. Though the aphid-killing compound produced by CMVΔ2b-infected plants remains unidentified, these findings present a route to identifying potential pesticide-free strategies to combat aphid infestation and insect transmission of plant viruses.
Blog by Warren Arinaitwe.
Warren Arinaitwe, Trisna D. Tungadi, Adrienne E. Pate, Joshua Joyce, Eseul Baek, Alex M. Murphy and John P. Carr published this review in Molecular Plant Pathology:
TITLE IMAGE: 2 transgenic lines of Tobacco are displayed alongside a control plant, demonstrating how aphids were confined onto leaves using clips. All images used with permission of the author.
