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Dormancy and germination of microsclerotia of Verticillium longisporum are regulated by soil bacteria and soil moisture levels but not by nutrients

The soil-borne pathogen Verticillium longisporum infects roots of its host plant, oilseed rape, and systemically colonizes stems where it finally forms microsclerotia at crop maturity. Once returned to the soil after harvest, microsclerotia undergo a stage of dormancy, in which they may survive for...

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Autores principales: Sarenqimuge, Sarenqimuge, Rahman, Shahinoor, Wang, Yao, von Tiedemann, Andreas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9539216/
https://www.ncbi.nlm.nih.gov/pubmed/36212810
http://dx.doi.org/10.3389/fmicb.2022.979218
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author Sarenqimuge, Sarenqimuge
Rahman, Shahinoor
Wang, Yao
von Tiedemann, Andreas
author_facet Sarenqimuge, Sarenqimuge
Rahman, Shahinoor
Wang, Yao
von Tiedemann, Andreas
author_sort Sarenqimuge, Sarenqimuge
collection PubMed
description The soil-borne pathogen Verticillium longisporum infects roots of its host plant, oilseed rape, and systemically colonizes stems where it finally forms microsclerotia at crop maturity. Once returned to the soil after harvest, microsclerotia undergo a stage of dormancy, in which they may survive for several years. Since there is neither efficient chemical control nor effective resistance in oilseed rape cultivars to control the disease, alternative control strategies may consist in regulating the germination and dormancy of microsclerotia in the soil. Therefore, a series of experiments were conducted to explore the effects of nutrients, soil moisture, and the soil microbiome on germination of dormant microsclerotia. Experiments with microsclerotia exposed in vitro to different nutrients indicated that under sterile conditions the stimulating effect of nutrients on microsclerotia germination was not enhanced as compared to water. Moreover, further assays revealed a strong inhibitory effect of unsterile soil on microsclerotia germination. Accordingly, oilseed rape plants inoculated with microsclerotia of V. longisporum showed severe infection with V. longisporum when grown in autoclaved soil, in contrast to plants grown in unsterile soil. These experiments indicate a crucial role of soil fungistasis and thus the soil microbiome on microsclerotia germination. Further bioassays demonstrated that viable soil bacteria obtained from the rhizosphere of oilseed rape plants and bulk field soil effectively inhibited microsclerotia germination, whereas dead bacteria and bacterial culture filtrates hardly suppressed germination. A putative inhibitory role of volatile organic compounds (VOCs) produced by soil bacteria was confirmed in two-compartment Petri dishes, where microsclerotia germination and colony growth were significantly inhibited. Bacterial VOCs were collected and analyzed by GC–MS. In total, 45 VOCs were identified, among which two acid and two alcohol compounds were emitted by all tested bacteria. A bioassay, conducted with corresponding pure chemicals in two-compartment Petri dishes, indicated that all acidic volatile compounds, including 3-methylbutanoic acid, 2-methylbutanoic acid, hexanoic acid, and 2-methylpropionic acid, induced strong inhibitory effects on microsclerotia. We conclude that bacterial acidic volatiles play a key role in the fungistatic effect on microsclerotia of V. longisporum in the soil and could thus be targeted for development of novel strategies to control this pathogen by artificially regulating dormancy of microsclerotia in soil.
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spelling pubmed-95392162022-10-08 Dormancy and germination of microsclerotia of Verticillium longisporum are regulated by soil bacteria and soil moisture levels but not by nutrients Sarenqimuge, Sarenqimuge Rahman, Shahinoor Wang, Yao von Tiedemann, Andreas Front Microbiol Microbiology The soil-borne pathogen Verticillium longisporum infects roots of its host plant, oilseed rape, and systemically colonizes stems where it finally forms microsclerotia at crop maturity. Once returned to the soil after harvest, microsclerotia undergo a stage of dormancy, in which they may survive for several years. Since there is neither efficient chemical control nor effective resistance in oilseed rape cultivars to control the disease, alternative control strategies may consist in regulating the germination and dormancy of microsclerotia in the soil. Therefore, a series of experiments were conducted to explore the effects of nutrients, soil moisture, and the soil microbiome on germination of dormant microsclerotia. Experiments with microsclerotia exposed in vitro to different nutrients indicated that under sterile conditions the stimulating effect of nutrients on microsclerotia germination was not enhanced as compared to water. Moreover, further assays revealed a strong inhibitory effect of unsterile soil on microsclerotia germination. Accordingly, oilseed rape plants inoculated with microsclerotia of V. longisporum showed severe infection with V. longisporum when grown in autoclaved soil, in contrast to plants grown in unsterile soil. These experiments indicate a crucial role of soil fungistasis and thus the soil microbiome on microsclerotia germination. Further bioassays demonstrated that viable soil bacteria obtained from the rhizosphere of oilseed rape plants and bulk field soil effectively inhibited microsclerotia germination, whereas dead bacteria and bacterial culture filtrates hardly suppressed germination. A putative inhibitory role of volatile organic compounds (VOCs) produced by soil bacteria was confirmed in two-compartment Petri dishes, where microsclerotia germination and colony growth were significantly inhibited. Bacterial VOCs were collected and analyzed by GC–MS. In total, 45 VOCs were identified, among which two acid and two alcohol compounds were emitted by all tested bacteria. A bioassay, conducted with corresponding pure chemicals in two-compartment Petri dishes, indicated that all acidic volatile compounds, including 3-methylbutanoic acid, 2-methylbutanoic acid, hexanoic acid, and 2-methylpropionic acid, induced strong inhibitory effects on microsclerotia. We conclude that bacterial acidic volatiles play a key role in the fungistatic effect on microsclerotia of V. longisporum in the soil and could thus be targeted for development of novel strategies to control this pathogen by artificially regulating dormancy of microsclerotia in soil. Frontiers Media S.A. 2022-09-23 /pmc/articles/PMC9539216/ /pubmed/36212810 http://dx.doi.org/10.3389/fmicb.2022.979218 Text en Copyright © 2022 Sarenqimuge, Rahman, Wang and von Tiedemann. 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
Sarenqimuge, Sarenqimuge
Rahman, Shahinoor
Wang, Yao
von Tiedemann, Andreas
Dormancy and germination of microsclerotia of Verticillium longisporum are regulated by soil bacteria and soil moisture levels but not by nutrients
title Dormancy and germination of microsclerotia of Verticillium longisporum are regulated by soil bacteria and soil moisture levels but not by nutrients
title_full Dormancy and germination of microsclerotia of Verticillium longisporum are regulated by soil bacteria and soil moisture levels but not by nutrients
title_fullStr Dormancy and germination of microsclerotia of Verticillium longisporum are regulated by soil bacteria and soil moisture levels but not by nutrients
title_full_unstemmed Dormancy and germination of microsclerotia of Verticillium longisporum are regulated by soil bacteria and soil moisture levels but not by nutrients
title_short Dormancy and germination of microsclerotia of Verticillium longisporum are regulated by soil bacteria and soil moisture levels but not by nutrients
title_sort dormancy and germination of microsclerotia of verticillium longisporum are regulated by soil bacteria and soil moisture levels but not by nutrients
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9539216/
https://www.ncbi.nlm.nih.gov/pubmed/36212810
http://dx.doi.org/10.3389/fmicb.2022.979218
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