Dataset Information

Confocal microscopy reveals in planta dynamic interactions between pathogenic, avirulent and non-pathogenic Pseudomonas syringae strains.

ABSTRACT: Recent advances in genomics and single-cell analysis have demonstrated the extraordinary complexity reached by microbial populations within their hosts. Communities range from complex multispecies groups to homogeneous populations differentiating into lineages through genetic or non-genetic mechanisms. Diversity within bacterial populations is recognized as a key driver of the evolution of animal pathogens. In plants, however, little is known about how interactions between different pathogenic and non-pathogenic variants within the host impact on defence responses, or how the presence within a mixture may affect the development or the fate of each variant. Using confocal fluorescence microscopy, we analysed the colonization of the plant apoplast by individual virulence variants of Pseudomonas syringae within mixed populations. We found that non-pathogenic variants can proliferate and even spread beyond the inoculated area to neighbouring tissues when in close proximity to pathogenic bacteria. The high bacterial concentrations reached at natural entry points promote such interactions during the infection process. We also found that a diversity of interactions take place at a cellular level between virulent and avirulent variants, ranging from dominant negative effects on proliferation of virulent bacteria to in trans suppression of defences triggered by avirulent bacteria. Our results illustrate the spatial dynamics and complexity of the interactions found within mixed infections, and their potential impact on pathogen evolution.

SUBMITTER: Rufian JS

PROVIDER: S-EPMC6638015 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Confocal microscopy reveals in planta dynamic interactions between pathogenic, avirulent and non-pathogenic Pseudomonas syringae strains.

Rufián José S JS Macho Alberto P AP Corry David S DS Mansfield John W JW Ruiz-Albert Javier J Arnold Dawn L DL Beuzón Carmen R CR

Molecular plant pathology 20170411 3

Recent advances in genomics and single-cell analysis have demonstrated the extraordinary complexity reached by microbial populations within their hosts. Communities range from complex multispecies groups to homogeneous populations differentiating into lineages through genetic or non-genetic mechanisms. Diversity within bacterial populations is recognized as a key driver of the evolution of animal pathogens. In plants, however, little is known about how interactions between different pathogenic a ...[more]

PMID: 28120374

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Project description:Background and aimsSelected beneficial Pseudomonas spp. strains have the ability to influence root architecture in Arabidopsis thaliana by inhibiting primary root elongation and promoting lateral root and root hair formation. A crucial role for auxin in this long-term (1week), long-distance plant-microbe interaction has been demonstrated.MethodsArabidopsis seedlings were cultivated in vitro on vertical plates and inoculated with pathogenic strains Pseudomonas syringae pv. maculicola (Psm) and P. syringae pv. tomato DC3000 (Pst), as well as Agrobacterium tumefaciens (Atu) and Escherichia coli (Eco). Root hair lengths were measured after 24 and 48h of direct exposure to each bacterial strain. Several Arabidopsis mutants with impaired responses to pathogens, impaired ethylene perception and defects in the exocyst vesicle tethering complex that is involved in secretion were also analysed.Key resultsArabidopsis seedling roots infected with Psm or Pst responded similarly to when infected with plant growth-promoting rhizobacteria; root hair growth was stimulated and primary root growth was inhibited. Other plant- and soil-adapted bacteria induced similar root hair responses. The most compromised root hair growth stimulation response was found for the knockout mutants exo70A1 and ein2. The single immune pathways dependent on salicylic acid, jasmonic acid and PAD4 are not directly involved in root hair growth stimulation; however, in the mutual cross-talk with ethylene, they indirectly modify the extent of the stimulation of root hair growth. The Flg22 peptide does not initiate root hair stimulation as intact bacteria do, but pretreatment with Flg22 prior to Psm inoculation abolished root hair growth stimulation in an FLS2 receptor kinase-dependent manner. These early response phenomena are not associated with changes in auxin levels, as monitored with the pDR5::GUS auxin reporter.ConclusionsEarly stimulation of root hair growth is an effect of an unidentified component of living plant pathogenic bacteria. The root hair growth response is triggered in the range of hours after bacterial contact with roots and can be modulated by FLS2 signalling. Bacterial stimulation of root hair growth requires functional ethylene signalling and an efficient exocyst-dependent secretory machinery.

Project description:Interactions between epiphytic bacteria and herbivorous insects are ubiquitous on plants, but little is known about their ecological implications. Aphids are devastating crop pests worldwide, so understanding how epiphytic bacteria impact aphid populations is critically important. Recent evidence demonstrates that plant-associated bacteria, such as Pseudomonas syringae, can be highly virulent to one species of aphid, the pea aphid (Acyrthosiphon pisum). Currently, we have no knowledge on how broad this phenomenon is across diverse aphid species that are of high agricultural concern. In controlled experiments using oral exposure in an artificial diet, we challenged five aphid species of agricultural importance with three strains of P. syringae that vary in virulence to the pea aphid. These strains also vary in epiphytic ability and comprise two phytopathogens and one non-plant-pathogenic strain. In general, differences in virulence to aphids remained relatively constant across strains regardless of the aphid species, except for the bird cherry-oat aphid (Rhopalosiphum padi), which is significantly less susceptible to two P. syringae strains. We demonstrate that lower infection incidence likely plays a role in the reduced susceptibility. Importantly, these data support previous results showing that interactions with epiphytic bacteria are important for aphids and may play a large, but underappreciated, role in insect population dynamics. Our study illustrates a potential role of epiphytic bacteria in the biological control of aphid pests broadly but suggests the need for more research encompassing a greater diversity of pest species.IMPORTANCE Sap-sucking aphids are insects of huge agricultural concern, not only because of direct damage caused by feeding but also because of their ability to transmit various plant pathogens. Some bacteria that grow on leaf surfaces, such as Pseudomonas syringae, can infect and kill aphids, making them potentially useful in the biological control of pest aphids. However, only one aphid species, the pea aphid (Acyrthosiphon pisum), has been tested for infection by P. syringae Here, we challenged five aphid species of agricultural importance with three strains of P. syringae that vary in virulence to the pea aphid. We found that four of these aphid species were susceptible to infection and death, suggesting that these bacteria are broadly useful for biological control. However, one aphid species was much more resistant to infection, indicating that more testing on diverse aphid species is needed.

Dataset Information

Confocal microscopy reveals in planta dynamic interactions between pathogenic, avirulent and non-pathogenic Pseudomonas syringae strains.

Publications

Confocal microscopy reveals in planta dynamic interactions between pathogenic, avirulent and non-pathogenic Pseudomonas syringae strains.

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