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Cyanogenic pseudomonads influence multitrophic interactions in the rhizosphere.

Rudrappa T, Splaine RE, Biedrzycki ML, Bais HP - PLoS ONE (2008)

Bottom Line: Additionally, pseudomonad cyanogenesis also affected other beneficial rhizospheric processes such as Bacillus subtilis colonization by biofilm formation on A. thaliana Col-0 roots.The effect of cyanogenesis on B. subtilis biofilm formation was further established by the down regulation of important B. subtilis biofilm operons epsA and yqxM.Our results show, the functional significance of pseudomonad cyanogenesis in regulating multitrophic rhizospheric interactions.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant and Soil Sciences, University of Delaware, Newark, Delaware, United States of America.

ABSTRACT
In the rhizosphere, plant roots cope with both pathogenic and beneficial bacterial interactions. The exometabolite production in certain bacterial species may regulate root growth and other root-microbe interactions in the rhizosphere. Here, we elucidated the role of cyanide production in pseudomonad virulence affecting plant root growth and other rhizospheric processes. Exposure of Arabidopsis thaliana Col-0 seedlings to both direct (with KCN) and indirect forms of cyanide from different pseudomonad strains caused significant inhibition of primary root growth. Further, we report that this growth inhibition was caused by the suppression of an auxin responsive gene, specifically at the root tip region by pseudomonad cyanogenesis. Additionally, pseudomonad cyanogenesis also affected other beneficial rhizospheric processes such as Bacillus subtilis colonization by biofilm formation on A. thaliana Col-0 roots. The effect of cyanogenesis on B. subtilis biofilm formation was further established by the down regulation of important B. subtilis biofilm operons epsA and yqxM. Our results show, the functional significance of pseudomonad cyanogenesis in regulating multitrophic rhizospheric interactions.

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Suppression of DR5::GUS expression in A. thaliana by the indirect exposure of the pseudomonad strains (A) and cyanide (B) and the effect of exogenous IAA on cyanide mediated down regulation of DR5::GUS expression (C).The images show complete suppression of DR5::GUS expression in the Col-0 DR5::GUS transgenic seedling roots when indirectly exposed to P. aeruginosa strains PAO1 and PA14, CHAO and cyanide. The images were representative of ten independent plants imaged (A) (bar = 100 µm). The figure also shows the effect of different doses (0–700 µM) of cyanide on DR5::GUS expression. The arrows in the panel show the localized DR5 expression.
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pone-0002073-g004: Suppression of DR5::GUS expression in A. thaliana by the indirect exposure of the pseudomonad strains (A) and cyanide (B) and the effect of exogenous IAA on cyanide mediated down regulation of DR5::GUS expression (C).The images show complete suppression of DR5::GUS expression in the Col-0 DR5::GUS transgenic seedling roots when indirectly exposed to P. aeruginosa strains PAO1 and PA14, CHAO and cyanide. The images were representative of ten independent plants imaged (A) (bar = 100 µm). The figure also shows the effect of different doses (0–700 µM) of cyanide on DR5::GUS expression. The arrows in the panel show the localized DR5 expression.

Mentions: Auxin is an important plant hormone which controls primary root growth by regulating cell proliferation and enlargement [32]. Since all of our results with pseudomonad strains and cyanide showed severe inhibition of primary root growth in A. thaliana Col-0, we further speculated that this may affect the auxin biosynthesis/perception at the root tip. To examine this interesting speculation, we conducted compartment plate assays using an A. thaliana Col-0 transgenic line stably expressing a GUS reporter gene fusion to the auxin responsive promoter DR5 (DR5::GUS). The results presented in Figure 4A show a complete suppression of the DR5 expression when co-inoculated with P. aeruginosa strains PAO1/PA14, P. fluorescens strain CHAO and cyanide (KCN) treatment. All of the other bacterial treatments such as cyanide mutants PAO6344 and CHAO77, showed stable expression of DR5::GUS similar to the control untreated plants. The dose response experiments performed using HCN (0–700 µM KCN+0.1 M HCl) showed complete suppression of DR5::GUS expression at ≥100 µM (Figure 4B). Further, the DR5::GUS expression was not affected when exogenous IAA (1 mg l−1) was included in the assay plates and the DR5::GUS expression was restored in the plants pre-treated with cyanide and subsequently exposed to IAA (Figure 4C). These results suggest that the cyanide produced by different strains of P. aeruginosa cause the inhibition of primary root growth of A. thaliana Col-0 through a complete suppression of the auxin biosynthesis/perception at the root tip.


Cyanogenic pseudomonads influence multitrophic interactions in the rhizosphere.

Rudrappa T, Splaine RE, Biedrzycki ML, Bais HP - PLoS ONE (2008)

Suppression of DR5::GUS expression in A. thaliana by the indirect exposure of the pseudomonad strains (A) and cyanide (B) and the effect of exogenous IAA on cyanide mediated down regulation of DR5::GUS expression (C).The images show complete suppression of DR5::GUS expression in the Col-0 DR5::GUS transgenic seedling roots when indirectly exposed to P. aeruginosa strains PAO1 and PA14, CHAO and cyanide. The images were representative of ten independent plants imaged (A) (bar = 100 µm). The figure also shows the effect of different doses (0–700 µM) of cyanide on DR5::GUS expression. The arrows in the panel show the localized DR5 expression.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2315799&req=5

pone-0002073-g004: Suppression of DR5::GUS expression in A. thaliana by the indirect exposure of the pseudomonad strains (A) and cyanide (B) and the effect of exogenous IAA on cyanide mediated down regulation of DR5::GUS expression (C).The images show complete suppression of DR5::GUS expression in the Col-0 DR5::GUS transgenic seedling roots when indirectly exposed to P. aeruginosa strains PAO1 and PA14, CHAO and cyanide. The images were representative of ten independent plants imaged (A) (bar = 100 µm). The figure also shows the effect of different doses (0–700 µM) of cyanide on DR5::GUS expression. The arrows in the panel show the localized DR5 expression.
Mentions: Auxin is an important plant hormone which controls primary root growth by regulating cell proliferation and enlargement [32]. Since all of our results with pseudomonad strains and cyanide showed severe inhibition of primary root growth in A. thaliana Col-0, we further speculated that this may affect the auxin biosynthesis/perception at the root tip. To examine this interesting speculation, we conducted compartment plate assays using an A. thaliana Col-0 transgenic line stably expressing a GUS reporter gene fusion to the auxin responsive promoter DR5 (DR5::GUS). The results presented in Figure 4A show a complete suppression of the DR5 expression when co-inoculated with P. aeruginosa strains PAO1/PA14, P. fluorescens strain CHAO and cyanide (KCN) treatment. All of the other bacterial treatments such as cyanide mutants PAO6344 and CHAO77, showed stable expression of DR5::GUS similar to the control untreated plants. The dose response experiments performed using HCN (0–700 µM KCN+0.1 M HCl) showed complete suppression of DR5::GUS expression at ≥100 µM (Figure 4B). Further, the DR5::GUS expression was not affected when exogenous IAA (1 mg l−1) was included in the assay plates and the DR5::GUS expression was restored in the plants pre-treated with cyanide and subsequently exposed to IAA (Figure 4C). These results suggest that the cyanide produced by different strains of P. aeruginosa cause the inhibition of primary root growth of A. thaliana Col-0 through a complete suppression of the auxin biosynthesis/perception at the root tip.

Bottom Line: Additionally, pseudomonad cyanogenesis also affected other beneficial rhizospheric processes such as Bacillus subtilis colonization by biofilm formation on A. thaliana Col-0 roots.The effect of cyanogenesis on B. subtilis biofilm formation was further established by the down regulation of important B. subtilis biofilm operons epsA and yqxM.Our results show, the functional significance of pseudomonad cyanogenesis in regulating multitrophic rhizospheric interactions.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant and Soil Sciences, University of Delaware, Newark, Delaware, United States of America.

ABSTRACT
In the rhizosphere, plant roots cope with both pathogenic and beneficial bacterial interactions. The exometabolite production in certain bacterial species may regulate root growth and other root-microbe interactions in the rhizosphere. Here, we elucidated the role of cyanide production in pseudomonad virulence affecting plant root growth and other rhizospheric processes. Exposure of Arabidopsis thaliana Col-0 seedlings to both direct (with KCN) and indirect forms of cyanide from different pseudomonad strains caused significant inhibition of primary root growth. Further, we report that this growth inhibition was caused by the suppression of an auxin responsive gene, specifically at the root tip region by pseudomonad cyanogenesis. Additionally, pseudomonad cyanogenesis also affected other beneficial rhizospheric processes such as Bacillus subtilis colonization by biofilm formation on A. thaliana Col-0 roots. The effect of cyanogenesis on B. subtilis biofilm formation was further established by the down regulation of important B. subtilis biofilm operons epsA and yqxM. Our results show, the functional significance of pseudomonad cyanogenesis in regulating multitrophic rhizospheric interactions.

Show MeSH
Related in: MedlinePlus