Promise for plant pest control: root-associated pseudomonads with insecticidal activities

Abstract

Insects are an important and probably the most challenging pest to control in agriculture, in particular when they feed on belowground parts of plants. The application of synthetic pesticides is problematic owing to side effects on the environment, concerns for public health and the rapid development of resistance. Entomopathogenic bacteria, notably Bacillus thuringiensis and Photorhabdus/Xenorhabdus species, are promising alternatives to chemical insecticides, for they are able to efficiently kill insects and are considered to be environmentally sound and harmless to mammals. However, they have the handicap of showing limited environmental persistence or of depending on a nematode vector for insect infection. Intriguingly, certain strains of plant root-colonizing Pseudomonas bacteria display insect pathogenicity and thus could be formulated to extend the present range of bioinsecticides for protection of plants against root-feeding insects. These entomopathogenic pseudomonads belong to a group of plant-beneficial rhizobacteria that have the remarkable ability to suppress soil-borne plant pathogens, promote plant growth, and induce systemic plant defenses. Here we review for the first time the current knowledge about the occurrence and the molecular basis of insecticidal activity in pseudomonads with an emphasis on plant-beneficial and prominent pathogenic species. We discuss how this fascinating Pseudomonas trait may be exploited for novel root-based approaches to insect control in an integrated pest management framework.

Keywords: Bacillus; Pseudomonas; biocontrol; entomopathogens; insecticidal; plant-associated; rhizosphere; toxins.

FIGURE 1

Certain plant root-associated Pseudomonas bacteria exhibit insect pathogenicity as an additional trait to the well-studied biocontrol activity against phytopathogens (see text for more details).(A) The most important interactions of these plant-beneficial pseudomonads (in green) include cooperation with the plant host (growth promotion and induction of systemic resistance) and competition with and antagonism of soil-borne phytopathogens. In addition, they show insecticidal activity and can use insects as vectors for dispersal. (B) Certain strains of Pseudomonas protegens and Pseudomonas chlororaphis are capable of infecting and efficiently killing insect larvae after oral uptake. P. protegens strain CHA0 (here tagged with GFP for microscopical visualization) typically forms microcolonies on roots (1) of various plant species (here tomato). Following ingestion by herbivorous insects, the entomopathogenic P. protegens strain is able to colonize the midgut (2) of pest insect larvae (here the large cabbage white Pieris brassicae), possibly by competing with the intestinal microbiota. By a so far unknown mechanism CHA0 cells then cross the intestinal epithelial barrier and invade the hemocoel within less than 1 day after oral infection (3). Once in this body compartment, the bacteria proliferate, resist uptake and elimination by hemocytes and cause disease (4). Bars represent 10 μm.