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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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Direct and indirect effect of pseudomonad strains on the growth of A. thaliana Col-0 roots (A&B).Severe reduction of primary root length (A&B) followed by the death of the seedlings was observed 5 days post-inoculation in the case of PAO1, PA14 and CHAO cultured at a distance of 1.5 cm from the primary root tip. The data also shows less reduction in primary root length in the case of PAO6344, CHAO77, when compared to PA01, PA14 and CHAO, Different letters indicate a statistically significant difference between treatments (Fisher's LSD, P<0.05). Data is the mean±SD of 12 replicates and the experiment was repeated on two independent occasions.
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pone-0002073-g001: Direct and indirect effect of pseudomonad strains on the growth of A. thaliana Col-0 roots (A&B).Severe reduction of primary root length (A&B) followed by the death of the seedlings was observed 5 days post-inoculation in the case of PAO1, PA14 and CHAO cultured at a distance of 1.5 cm from the primary root tip. The data also shows less reduction in primary root length in the case of PAO6344, CHAO77, when compared to PA01, PA14 and CHAO, Different letters indicate a statistically significant difference between treatments (Fisher's LSD, P<0.05). Data is the mean±SD of 12 replicates and the experiment was repeated on two independent occasions.

Mentions: The direct effect of pseudomonads on primary root growth was studied by inoculating 3–4 day old A. thaliana (Col-0) seedlings with different strains of bacteria at a distance of 1.5 cm from the primary root tip. The results presented in Figure 1A show that five days after inoculation, P. aeruginosa (strains PAO1&PA14) and P. fluorescens (wild type strain CHAO) caused significantly shorter primary root lengths in A. thaliana compared to control treatments (Fig. 1A&B) (P<0.05; n = 12). A less drastic (but not significant) reduction in the primary root length was observed with the cyanide synthase (ΔhcnB) mutant (PAO6344) of P. aeruginosa (Figure 1A&B) and CHAO77 (ΔhcnABC) of P. fluorescens. Apart from the wild type strains and cyanide mutants, we also examined a quorum sensing (QS) mutant PAO210 (ΔrhlI) of P. aeruginosa to evaluate if another known virulence pathway, such as QS played a role in the observed root phenotype. The data showed significant inhibition of primary root growth by the mutant PAO210 compared to the cyanide mutant indicating that the inhibitory effect is more of a result of the cyanide synthase mutation. These results also suggest that an external factor produced by pseudomonad strains is involved in the inhibition of A. thaliana Col-0 seedlings. However, the relatively less inhibition of root length by the cyanide mutant strains of P. aeruginosa (PAO6344) and P. fluorescens (CHAO77) indicated a possible role for cyanide in the inhibition of root growth.


Cyanogenic pseudomonads influence multitrophic interactions in the rhizosphere.

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

Direct and indirect effect of pseudomonad strains on the growth of A. thaliana Col-0 roots (A&B).Severe reduction of primary root length (A&B) followed by the death of the seedlings was observed 5 days post-inoculation in the case of PAO1, PA14 and CHAO cultured at a distance of 1.5 cm from the primary root tip. The data also shows less reduction in primary root length in the case of PAO6344, CHAO77, when compared to PA01, PA14 and CHAO, Different letters indicate a statistically significant difference between treatments (Fisher's LSD, P<0.05). Data is the mean±SD of 12 replicates and the experiment was repeated on two independent occasions.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0002073-g001: Direct and indirect effect of pseudomonad strains on the growth of A. thaliana Col-0 roots (A&B).Severe reduction of primary root length (A&B) followed by the death of the seedlings was observed 5 days post-inoculation in the case of PAO1, PA14 and CHAO cultured at a distance of 1.5 cm from the primary root tip. The data also shows less reduction in primary root length in the case of PAO6344, CHAO77, when compared to PA01, PA14 and CHAO, Different letters indicate a statistically significant difference between treatments (Fisher's LSD, P<0.05). Data is the mean±SD of 12 replicates and the experiment was repeated on two independent occasions.
Mentions: The direct effect of pseudomonads on primary root growth was studied by inoculating 3–4 day old A. thaliana (Col-0) seedlings with different strains of bacteria at a distance of 1.5 cm from the primary root tip. The results presented in Figure 1A show that five days after inoculation, P. aeruginosa (strains PAO1&PA14) and P. fluorescens (wild type strain CHAO) caused significantly shorter primary root lengths in A. thaliana compared to control treatments (Fig. 1A&B) (P<0.05; n = 12). A less drastic (but not significant) reduction in the primary root length was observed with the cyanide synthase (ΔhcnB) mutant (PAO6344) of P. aeruginosa (Figure 1A&B) and CHAO77 (ΔhcnABC) of P. fluorescens. Apart from the wild type strains and cyanide mutants, we also examined a quorum sensing (QS) mutant PAO210 (ΔrhlI) of P. aeruginosa to evaluate if another known virulence pathway, such as QS played a role in the observed root phenotype. The data showed significant inhibition of primary root growth by the mutant PAO210 compared to the cyanide mutant indicating that the inhibitory effect is more of a result of the cyanide synthase mutation. These results also suggest that an external factor produced by pseudomonad strains is involved in the inhibition of A. thaliana Col-0 seedlings. However, the relatively less inhibition of root length by the cyanide mutant strains of P. aeruginosa (PAO6344) and P. fluorescens (CHAO77) indicated a possible role for cyanide in the inhibition of root growth.

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