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Pseudomonas Strains Induce Transcriptional and Morphological Changes and Reduce Root Colonization of Verticillium spp.

Phytopathogenic Verticillia cause Verticillium wilt on numerous economically important crops. Plant infection begins at the roots, where the fungus is confronted with rhizosphere inhabiting bacteria. The effects of different fluorescent pseudomonads, including some known biocontrol agents of other p...

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Autores principales: Harting, Rebekka, Nagel, Alexandra, Nesemann, Kai, Höfer, Annalena M., Bastakis, Emmanouil, Kusch, Harald, Stanley, Claire E., Stöckli, Martina, Kaever, Alexander, Hoff, Katharina J., Stanke, Mario, deMello, Andrew J., Künzler, Markus, Haney, Cara H., Braus-Stromeyer, Susanna A., Braus, Gerhard H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8180853/
https://www.ncbi.nlm.nih.gov/pubmed/34108946
http://dx.doi.org/10.3389/fmicb.2021.652468
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author Harting, Rebekka
Nagel, Alexandra
Nesemann, Kai
Höfer, Annalena M.
Bastakis, Emmanouil
Kusch, Harald
Stanley, Claire E.
Stöckli, Martina
Kaever, Alexander
Hoff, Katharina J.
Stanke, Mario
deMello, Andrew J.
Künzler, Markus
Haney, Cara H.
Braus-Stromeyer, Susanna A.
Braus, Gerhard H.
author_facet Harting, Rebekka
Nagel, Alexandra
Nesemann, Kai
Höfer, Annalena M.
Bastakis, Emmanouil
Kusch, Harald
Stanley, Claire E.
Stöckli, Martina
Kaever, Alexander
Hoff, Katharina J.
Stanke, Mario
deMello, Andrew J.
Künzler, Markus
Haney, Cara H.
Braus-Stromeyer, Susanna A.
Braus, Gerhard H.
author_sort Harting, Rebekka
collection PubMed
description Phytopathogenic Verticillia cause Verticillium wilt on numerous economically important crops. Plant infection begins at the roots, where the fungus is confronted with rhizosphere inhabiting bacteria. The effects of different fluorescent pseudomonads, including some known biocontrol agents of other plant pathogens, on fungal growth of the haploid Verticillium dahliae and/or the amphidiploid Verticillium longisporum were compared on pectin-rich medium, in microfluidic interaction channels, allowing visualization of single hyphae, or on Arabidopsis thaliana roots. We found that the potential for formation of bacterial lipopeptide syringomycin resulted in stronger growth reduction effects on saprophytic Aspergillus nidulans compared to Verticillium spp. A more detailed analyses on bacterial-fungal co-cultivation in narrow interaction channels of microfluidic devices revealed that the strongest inhibitory potential was found for Pseudomonas protegens CHA0, with its inhibitory potential depending on the presence of the GacS/GacA system controlling several bacterial metabolites. Hyphal tip polarity was altered when V. longisporum was confronted with pseudomonads in narrow interaction channels, resulting in a curly morphology instead of straight hyphal tip growth. These results support the hypothesis that the fungus attempts to evade the bacterial confrontation. Alterations due to co-cultivation with bacteria could not only be observed in fungal morphology but also in fungal transcriptome. P. protegens CHA0 alters transcriptional profiles of V. longisporum during 2 h liquid media co-cultivation in pectin-rich medium. Genes required for degradation of and growth on the carbon source pectin were down-regulated, whereas transcripts involved in redox processes were up-regulated. Thus, the secondary metabolite mediated effect of Pseudomonas isolates on Verticillium species results in a complex transcriptional response, leading to decreased growth with precautions for self-protection combined with the initiation of a change in fungal growth direction. This interplay of bacterial effects on the pathogen can be beneficial to protect plants from infection, as shown with A. thaliana root experiments. Treatment of the roots with bacteria prior to infection with V. dahliae resulted in a significant reduction of fungal root colonization. Taken together we demonstrate how pseudomonads interfere with the growth of Verticillium spp. and show that these bacteria could serve in plant protection.
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spelling pubmed-81808532021-06-08 Pseudomonas Strains Induce Transcriptional and Morphological Changes and Reduce Root Colonization of Verticillium spp. Harting, Rebekka Nagel, Alexandra Nesemann, Kai Höfer, Annalena M. Bastakis, Emmanouil Kusch, Harald Stanley, Claire E. Stöckli, Martina Kaever, Alexander Hoff, Katharina J. Stanke, Mario deMello, Andrew J. Künzler, Markus Haney, Cara H. Braus-Stromeyer, Susanna A. Braus, Gerhard H. Front Microbiol Microbiology Phytopathogenic Verticillia cause Verticillium wilt on numerous economically important crops. Plant infection begins at the roots, where the fungus is confronted with rhizosphere inhabiting bacteria. The effects of different fluorescent pseudomonads, including some known biocontrol agents of other plant pathogens, on fungal growth of the haploid Verticillium dahliae and/or the amphidiploid Verticillium longisporum were compared on pectin-rich medium, in microfluidic interaction channels, allowing visualization of single hyphae, or on Arabidopsis thaliana roots. We found that the potential for formation of bacterial lipopeptide syringomycin resulted in stronger growth reduction effects on saprophytic Aspergillus nidulans compared to Verticillium spp. A more detailed analyses on bacterial-fungal co-cultivation in narrow interaction channels of microfluidic devices revealed that the strongest inhibitory potential was found for Pseudomonas protegens CHA0, with its inhibitory potential depending on the presence of the GacS/GacA system controlling several bacterial metabolites. Hyphal tip polarity was altered when V. longisporum was confronted with pseudomonads in narrow interaction channels, resulting in a curly morphology instead of straight hyphal tip growth. These results support the hypothesis that the fungus attempts to evade the bacterial confrontation. Alterations due to co-cultivation with bacteria could not only be observed in fungal morphology but also in fungal transcriptome. P. protegens CHA0 alters transcriptional profiles of V. longisporum during 2 h liquid media co-cultivation in pectin-rich medium. Genes required for degradation of and growth on the carbon source pectin were down-regulated, whereas transcripts involved in redox processes were up-regulated. Thus, the secondary metabolite mediated effect of Pseudomonas isolates on Verticillium species results in a complex transcriptional response, leading to decreased growth with precautions for self-protection combined with the initiation of a change in fungal growth direction. This interplay of bacterial effects on the pathogen can be beneficial to protect plants from infection, as shown with A. thaliana root experiments. Treatment of the roots with bacteria prior to infection with V. dahliae resulted in a significant reduction of fungal root colonization. Taken together we demonstrate how pseudomonads interfere with the growth of Verticillium spp. and show that these bacteria could serve in plant protection. Frontiers Media S.A. 2021-05-24 /pmc/articles/PMC8180853/ /pubmed/34108946 http://dx.doi.org/10.3389/fmicb.2021.652468 Text en Copyright © 2021 Harting, Nagel, Nesemann, Höfer, Bastakis, Kusch, Stanley, Stöckli, Kaever, Hoff, Stanke, deMello, Künzler, Haney, Braus-Stromeyer and Braus. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Harting, Rebekka
Nagel, Alexandra
Nesemann, Kai
Höfer, Annalena M.
Bastakis, Emmanouil
Kusch, Harald
Stanley, Claire E.
Stöckli, Martina
Kaever, Alexander
Hoff, Katharina J.
Stanke, Mario
deMello, Andrew J.
Künzler, Markus
Haney, Cara H.
Braus-Stromeyer, Susanna A.
Braus, Gerhard H.
Pseudomonas Strains Induce Transcriptional and Morphological Changes and Reduce Root Colonization of Verticillium spp.
title Pseudomonas Strains Induce Transcriptional and Morphological Changes and Reduce Root Colonization of Verticillium spp.
title_full Pseudomonas Strains Induce Transcriptional and Morphological Changes and Reduce Root Colonization of Verticillium spp.
title_fullStr Pseudomonas Strains Induce Transcriptional and Morphological Changes and Reduce Root Colonization of Verticillium spp.
title_full_unstemmed Pseudomonas Strains Induce Transcriptional and Morphological Changes and Reduce Root Colonization of Verticillium spp.
title_short Pseudomonas Strains Induce Transcriptional and Morphological Changes and Reduce Root Colonization of Verticillium spp.
title_sort pseudomonas strains induce transcriptional and morphological changes and reduce root colonization of verticillium spp.
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8180853/
https://www.ncbi.nlm.nih.gov/pubmed/34108946
http://dx.doi.org/10.3389/fmicb.2021.652468
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