Aboveground insect infestation attenuates belowground Agrobacterium-mediated genetic transformation

New Phytol. 2015 Jul;207(1):148-158. doi: 10.1111/nph.13324. Epub 2015 Feb 10.

Abstract

Agrobacterium tumefaciens causes crown gall disease. Although Agrobacterium can be popularly used for genetic engineering, the influence of aboveground insect infestation on Agrobacterium induced gall formation has not been investigated. Nicotiana benthamiana leaves were exposed to a sucking insect (whitefly) infestation and benzothiadiazole (BTH) for 7 d, and these exposed plants were inoculated with a tumorigenic Agrobacterium strain. We evaluated, both in planta and in vitro, how whitefly infestation affects crown gall disease. Whitefly-infested plants exhibited at least a two-fold reduction in gall formation on both stem and crown root. Silencing of isochorismate synthase 1 (ICS1), required for salicylic acid (SA) synthesis, compromised gall formation indicating an involvement of SA in whitefly-derived plant defence against Agrobacterium. Endogenous SA content was augmented in whitefly-infested plants upon Agrobacterium inoculation. In addition, SA concentration was three times higher in root exudates from whitefly-infested plants. As a consequence, Agrobacterium-mediated transformation of roots of whitefly-infested plants was clearly inhibited when compared to control plants. These results suggest that aboveground whitefly infestation elicits systemic defence responses throughout the plant. Our findings provide new insights into insect-mediated leaf-root intra-communication and a framework to understand interactions between three organisms: whitefly, N. benthamiana and Agrobacterium.

Keywords: Agrobacterium; crown gall; multitrophic interactions; salicylic acid (SA); transformation efficiency; whitefly infestation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Agrobacterium tumefaciens / physiology*
  • Animals
  • Cyclopentanes / metabolism
  • Gene Expression Regulation, Plant
  • Gene Silencing
  • Genes, Plant
  • Hemiptera / physiology*
  • Models, Biological
  • Molecular Sequence Data
  • Nicotiana / genetics
  • Nicotiana / microbiology*
  • Nicotiana / parasitology*
  • Oxylipins / metabolism
  • Plant Exudates / metabolism
  • Plant Roots / metabolism
  • Plant Stems / microbiology
  • Plant Tumors / microbiology
  • Plant Tumors / parasitology
  • Plant Viruses / physiology
  • Salicylic Acid / metabolism
  • Transformation, Genetic*

Substances

  • Cyclopentanes
  • Oxylipins
  • Plant Exudates
  • jasmonic acid
  • Salicylic Acid

Associated data

  • GENBANK/U60489