Lifestyle of the biotroph Agrobacterium tumefaciens in the ecological niche constructed on its host plant

New Phytol. 2018 Jul;219(1):350-362. doi: 10.1111/nph.15164. Epub 2018 Apr 27.

Abstract

Agrobacterium tumefaciens constructs an ecological niche in its host plant by transferring the T-DNA from its Ti plasmid into the host genome and by diverting the host metabolism. We combined transcriptomics and genetics for understanding the A. tumefaciens lifestyle when it colonizes Arabidopsis thaliana tumors. Transcriptomics highlighted: a transition from a motile to sessile behavior that mobilizes some master regulators (Hfq, CtrA, DivK and PleD); a remodeling of some cell surface components (O-antigen, succinoglucan, curdlan, att genes, putative fasciclin) and functions associated with plant defense (Ef-Tu and flagellin pathogen-associated molecular pattern-response and glycerol-3-phosphate and nitric oxide signaling); and an exploitation of a wide variety of host resources, including opines, amino acids, sugars, organic acids, phosphate, phosphorylated compounds, and iron. In addition, construction of transgenic A. thaliana lines expressing a lactonase enzyme showed that Ti plasmid transfer could escape host-mediated quorum-quenching. Finally, construction of knock-out mutants in A. tumefaciens showed that expression of some At plasmid genes seemed more costly than the selective advantage they would have conferred in tumor colonization. We provide the first overview of A. tumefaciens lifestyle in a plant tumor and reveal novel signaling and trophic interplays for investigating host-pathogen interactions.

Keywords: Agrobacterium; Arabidopsis; horizontal transfer; niche exploitation; opine; plasmid; quorum-sensing; tumor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Agrobacterium tumefaciens / drug effects
  • Agrobacterium tumefaciens / pathogenicity*
  • Agrobacterium tumefaciens / physiology*
  • Arabidopsis / genetics
  • Arabidopsis / metabolism
  • Arabidopsis / microbiology*
  • Arginine / analogs & derivatives
  • Arginine / pharmacology
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Carbon / metabolism
  • Cell Wall / metabolism
  • Cell Wall / microbiology
  • Chemotaxis
  • Ecosystem
  • Gene Expression Regulation, Bacterial
  • Genome, Bacterial
  • Host-Pathogen Interactions / physiology*
  • Iron / metabolism
  • Mutation
  • Nitrogen / metabolism
  • Plant Tumors / microbiology*
  • Plants, Genetically Modified
  • Sugar Phosphates / pharmacology

Substances

  • Bacterial Proteins
  • Sugar Phosphates
  • nopaline
  • Carbon
  • agrocinopine
  • Arginine
  • Iron
  • Nitrogen