Whitefly hijacks a plant detoxification gene that neutralizes plant toxins

Cell. 2021 Apr 1;184(7):1693-1705.e17. doi: 10.1016/j.cell.2021.02.014. Epub 2021 Mar 25.

Abstract

Plants protect themselves with a vast array of toxic secondary metabolites, yet most plants serve as food for insects. The evolutionary processes that allow herbivorous insects to resist plant defenses remain largely unknown. The whitefly Bemisia tabaci is a cosmopolitan, highly polyphagous agricultural pest that vectors several serious plant pathogenic viruses and is an excellent model to probe the molecular mechanisms involved in overcoming plant defenses. Here, we show that, through an exceptional horizontal gene transfer event, the whitefly has acquired the plant-derived phenolic glucoside malonyltransferase gene BtPMaT1. This gene enables whiteflies to neutralize phenolic glucosides. This was confirmed by genetically transforming tomato plants to produce small interfering RNAs that silence BtPMaT1, thus impairing the whiteflies' detoxification ability. These findings reveal an evolutionary scenario whereby herbivores harness the genetic toolkit of their host plants to develop resistance to plant defenses and how this can be exploited for crop protection.

Keywords: Bemisia tabaci; co-evolution; detoxification; horizontal gene transfer; insect-plant interaction; pest control; phenolic glucoside malonyltransferase; plant secondary metabolite; tomato.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Gene Transfer, Horizontal
  • Genes, Plant
  • Glucosides / chemistry
  • Glucosides / metabolism
  • Hemiptera / genetics*
  • Hemiptera / physiology
  • Herbivory
  • Insect Proteins / antagonists & inhibitors
  • Insect Proteins / classification
  • Insect Proteins / genetics
  • Insect Proteins / metabolism*
  • Intestinal Mucosa / metabolism
  • Malonyl Coenzyme A / metabolism
  • Phylogeny
  • Plants, Genetically Modified / genetics
  • Plants, Genetically Modified / metabolism
  • RNA Interference
  • RNA, Double-Stranded / metabolism
  • Solanum lycopersicum / genetics*
  • Solanum lycopersicum / metabolism
  • Toxins, Biological / chemistry
  • Toxins, Biological / metabolism*

Substances

  • Glucosides
  • Insect Proteins
  • RNA, Double-Stranded
  • Toxins, Biological
  • Malonyl Coenzyme A