Aphid endosymbiont facilitates virus transmission by modulating the volatile profile of host plants

BMC Plant Biol. 2021 Jan 29;21(1):67. doi: 10.1186/s12870-021-02838-5.

Abstract

Background: Most plant viruses rely on vectors for their transmission and spread. One of the outstanding biological questions concerning the vector-pathogen-symbiont multi-trophic interactions is the potential involvement of vector symbionts in the virus transmission process. Here, we used a multi-factorial system containing a non-persistent plant virus, cucumber mosaic virus (CMV), its primary vector, green peach aphid, Myzus persicae, and the obligate endosymbiont, Buchnera aphidicola to explore this uncharted territory.

Results: Based on our preliminary research, we hypothesized that aphid endosymbiont B. aphidicola can facilitate CMV transmission by modulating plant volatile profiles. Gene expression analyses demonstrated that CMV infection reduced B. aphidicola abundance in M. persicae, in which lower abundance of B. aphidicola was associated with a preference shift in aphids from infected to healthy plants. Volatile profile analyses confirmed that feeding by aphids with lower B. aphidicola titers reduced the production of attractants, while increased the emission of deterrents. As a result, M. persicae changed their feeding preference from infected to healthy plants.

Conclusions: We conclude that CMV infection reduces the B. aphidicola abundance in M. persicae. When viruliferous aphids feed on host plants, dynamic changes in obligate symbionts lead to a shift in plant volatiles from attraction to avoidance, thereby switching insect vector's feeding preference from infected to healthy plants.

Keywords: Buchnera aphidicola; Cucumber mosaic virus; Multi-trophic interaction; Myzus persicae; Plant volatile.

MeSH terms

  • Animals
  • Aphids / drug effects
  • Aphids / microbiology
  • Aphids / physiology
  • Aphids / virology*
  • Buchnera / physiology*
  • Capsicum / microbiology
  • Capsicum / parasitology
  • Capsicum / virology*
  • Cucumovirus / physiology*
  • Feeding Behavior
  • Host-Parasite Interactions
  • Insect Vectors / physiology
  • Plant Diseases / microbiology
  • Plant Diseases / parasitology
  • Plant Diseases / virology*
  • Rifampin / pharmacology
  • Symbiosis*
  • Volatile Organic Compounds / metabolism

Substances

  • Volatile Organic Compounds
  • Rifampin