Pyocyanin, a Virulence Factor Produced by Pseudomonas aeruginosa, Alters Root Development Through Reactive Oxygen Species and Ethylene Signaling in Arabidopsis

Abstract

Pyocyanin acts as a virulence factor in Pseudomonas aeruginosa, a plant and animal pathogen. In this study, we evaluated the effect of pyocyanin on growth and development of Arabidopsis seedlings. Root inoculation with P. aeruginosa PAO1 strain inhibited primary root growth in wild-type (WT) Arabidopsis seedlings. In contrast, single lasI– and double rhlI–/lasI– mutants of P. aeruginosa defective in pyocyanin production showed decreased root growth inhibition concomitant with an increased phytostimulation. Treatment with pyocyanin modulates root system architecture, inhibiting primary root growth and promoting lateral root and root hair formation without affecting meristem viability or causing cell death. These effects correlated with altered proportions of hydrogen peroxide and superoxide in root tips and with an inhibition of cell division and elongation. Mutant analyses showed that pyocyanin modulation of root growth was likely independent of auxin, cytokinin, and abscisic acid but required ethylene signaling because the Arabidopsis etr1-1, ein2-1, and ein3-1 ethylene-related mutants were less sensitive to pyocyanin-induced root stoppage and reactive oxygen species (ROS) distribution. Our findings suggest that pyocyanin is an important factor modulating the interplay between ROS production and root system architecture by an ethylene-dependent signaling.

Beneficial Microbes Affect Endogenous Mechanisms Controlling Root Development

“…A plant-derived compound, rosmarinic acid, was found that affects quorum sensing in soil bacteria [33], suggesting that plants may excrete certain compounds to alter bacteria in the rhizosphere. Microbes within the rhizosphere can in turn modify root exudate composition [40–45], enhance shoot growth [46–48] and induce systemic resistance to subsequent pathogen attack (reviewed in [49]). These examples reveal a rich language of chemical communication between plants and rhizosphere-inhabiting microbes resulting in altered microbial community structure.…”

“…Although growth promotion phenotypes have been well-described [3], few molecular mechanisms underlying these effects are known. Recently, several PGPR have been shown to induce root developmental changes in terms of cell division and differentiation at both the root meristem and at sites of lateral root formation [46–48,51,52]. These cellular level changes alter the root system architecture of the plants [46–48,51,52].…”

Protozoa stimulate the plant beneficial activity of rhizospheric pseudomonads

“…In addition, siderophore production in vitro correlated with plant growth promotion by the different bacteria, but only when protozoa were co-inoculated. Siderophores are a typical plant-growth promoting agent, helping plants to better access soil iron (Sharma et al 2003). Protozoa can enhance siderophore production in bacteria (Levrat et al 1989) and we propose that this enhanced trait expression may have contributed to plant growth.…”

“…In addition, metabolites involved in pathogen suppression, e.g. 2, 4 -DAPG and phenazines, can interfere with plant growth (Brazelton et al 2008;Ortiz-Castro et al 2013), suggesting that it may be difficult to merge plant growth promoting and/or disease suppressive capacities in one bacterial isolate. The fact that bacterial isolates bearing plant growth promoting and disease suppressive traits demonstrated no or even negative plant growth effects in this study when inoculated alone (in absence of amoebae and P. ultimum), strengthens the necessity of investigating further interactions of the bacteria with other organisms in the rhizosphere.…”

Database on the taxonomical characterisation and potential toxigenic capacities of microorganisms used for the industrial production of food enzymes and feed additives, which do not have a recommendation for Qualified Presumption of Safety

“…lipotoxin [241] metallo-β-Lactamase antimicrobial resistance factor [242] PcrV (type III secretion system) virulence factor [243] phenazine and derivates virulence factor [244][245][246] Pseudomonas aeruginosa pseudoverdine virulence factor [247] pyochelin (siderophore) virulence factor [248] pyocyanin (phenazide) virulence factor [223,[249][250][251][252][253][254][255][256][257][258][259][260][261][262] pyoluteorin [263] pyoverdine virulence factor [227,[264][265][266] rhamnolipids bacterial surfactants [227,267] Tse2 virulence factor [268] TypA virulence factor [269] Type II secretion system virulence factor [270] Type III secretion system virulence factor [271- …”