Virus-induced plant volatiles mediate the olfactory behaviour of its insect vectors

Plant Cell Environ. 2021 Aug;44(8):2700-2715. doi: 10.1111/pce.14069. Epub 2021 May 5.

Abstract

Plant viruses can manipulate their hosts to release odours that are attractive or repellent to their insect vectors. However, the volatile organic compounds (VOCs), either individually or as mixtures, which play a key role in the olfactory behaviour of insect vectors remains largely unknown. Our study focused on green rice leafhoppers (GRLHs) vectoring rice dwarf virus (RDV) revealed that RDV infection significantly induced the emission of (E)-β-caryophyllene and 2-heptanol by rice plants, which influenced the olfactory behaviour of both non-viruliferous and viruliferous GRLHs. (E)-β-caryophyllene attracted non-viruliferous GRLHs to settle on RDV-infected plants, but neither attracted nor repelled viruliferous GRLHs. In contrast, 2-heptanol repelled viruliferous GRLHs to settle on RDV-infected plants, but neither repelled nor attracted non-viruliferous GRLHs. Suppression of (E)-β-caryophyllene synthase OsCAS via CRISPR-Cas9 to generate oscas-1 plants enabled us to confirm the important role played by (E)-β-caryophyllene in modulating the virus-vector-host plant interaction. These novel results reveal the role of these virus-induced VOCs in modulating the behaviour of its GRLH insect vector and may facilitate the design of new strategies for disease control through manipulation of plant volatile emissions.

Keywords: (E)-β-caryophyllene; 2-heptanol; green rice leafhoppers; olfactory behaviour; plant volatiles; rice dwarf virus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Behavior, Animal / drug effects
  • Behavior, Animal / physiology
  • Enzymes / genetics
  • Enzymes / metabolism
  • Gene Expression Regulation, Plant
  • Hemiptera / drug effects*
  • Hemiptera / physiology
  • Heptanol / metabolism
  • Heptanol / pharmacology
  • Host-Pathogen Interactions / physiology*
  • Insect Repellents / metabolism
  • Insect Repellents / pharmacology
  • Odorants
  • Oryza / genetics
  • Oryza / metabolism
  • Oryza / virology*
  • Plant Diseases / virology
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Plant Viruses / pathogenicity
  • Plants, Genetically Modified
  • Polycyclic Sesquiterpenes / metabolism
  • Reoviridae / pathogenicity*
  • Volatile Organic Compounds / metabolism*
  • Volatile Organic Compounds / pharmacology

Substances

  • Enzymes
  • Insect Repellents
  • Plant Proteins
  • Polycyclic Sesquiterpenes
  • Volatile Organic Compounds
  • Heptanol
  • caryophyllene

Supplementary concepts

  • Rice dwarf virus