Hordeum vulgare differentiates its response to beneficial bacteria

Abstract Background In nature, beneficial bacteria triggering induced systemic resistance (ISR) may protect plants from potential diseases, reducing yield losses caused by diverse pathogens. However, little is known about how the host plant initially responds to different beneficial bacteria. To rev...

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Main Authors: Yongming Duan, Min Han, Maja Grimm, Jasper Schierstaedt, Jafargholi Imani, Massimiliano Cardinale, Marie Le Jean, Joseph Nesme, Søren J. Sørensen, Adam Schikora
Format: Article
Language:English
Published: BMC 2023-10-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-023-04484-5
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author Yongming Duan
Min Han
Maja Grimm
Jasper Schierstaedt
Jafargholi Imani
Massimiliano Cardinale
Marie Le Jean
Joseph Nesme
Søren J. Sørensen
Adam Schikora
author_facet Yongming Duan
Min Han
Maja Grimm
Jasper Schierstaedt
Jafargholi Imani
Massimiliano Cardinale
Marie Le Jean
Joseph Nesme
Søren J. Sørensen
Adam Schikora
author_sort Yongming Duan
collection DOAJ
description Abstract Background In nature, beneficial bacteria triggering induced systemic resistance (ISR) may protect plants from potential diseases, reducing yield losses caused by diverse pathogens. However, little is known about how the host plant initially responds to different beneficial bacteria. To reveal the impact of different bacteria on barley (Hordeum vulgare), bacterial colonization patterns, gene expression, and composition of seed endophytes were explored. Results This study used the soil-borne Ensifer meliloti, as well as Pantoea sp. and Pseudomonas sp. isolated from barley seeds, individually. The results demonstrated that those bacteria persisted in the rhizosphere but with different colonization patterns. Although root-leaf translocation was not observed, all three bacteria induced systemic resistance (ISR) against foliar fungal pathogens. Transcriptome analysis revealed that ion- and stress-related genes were regulated in plants that first encountered bacteria. Iron homeostasis and heat stress responses were involved in the response to E. meliloti and Pantoea sp., even if the iron content was not altered. Heat shock protein-encoding genes responded to inoculation with Pantoea sp. and Pseudomonas sp. Furthermore, bacterial inoculation affected the composition of seed endophytes. Investigation of the following generation indicated that the enhanced resistance was not heritable. Conclusions Here, using barley as a model, we highlighted different responses to three different beneficial bacteria as well as the influence of soil-borne Ensifer meliloti on the seed microbiome. In total, these results can help to understand the interaction between ISR-triggering bacteria and a crop plant, which is essential for the application of biological agents in sustainable agriculture.
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spelling doaj.art-b80767d00ed748f48215f5038d082fa82023-11-19T12:52:42ZengBMCBMC Plant Biology1471-22292023-10-0123111610.1186/s12870-023-04484-5Hordeum vulgare differentiates its response to beneficial bacteriaYongming Duan0Min Han1Maja Grimm2Jasper Schierstaedt3Jafargholi Imani4Massimiliano Cardinale5Marie Le Jean6Joseph Nesme7Søren J. Sørensen8Adam Schikora9Julius Kühn Institute (JKI), Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen DiagnosticsJulius Kühn Institute (JKI), Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen DiagnosticsJulius Kühn Institute (JKI), Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen DiagnosticsJulius Kühn Institute (JKI), Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen DiagnosticsInstitute of Phytopathology, Research Centre for BioSystems, Land Use and Nutrition, Justus Liebig University GiessenDepartment of Biological and Environmental Sciences and Technologies, University of Salento, SP6 Lecce- MonteroniLaboratoire Interdisciplinaire des Environnements Continentaux (LIEC), UMR 7360 CNRS, Université de LorraineDepartment of Biology, Section of Microbiology, Copenhagen UniversityDepartment of Biology, Section of Microbiology, Copenhagen UniversityJulius Kühn Institute (JKI), Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen DiagnosticsAbstract Background In nature, beneficial bacteria triggering induced systemic resistance (ISR) may protect plants from potential diseases, reducing yield losses caused by diverse pathogens. However, little is known about how the host plant initially responds to different beneficial bacteria. To reveal the impact of different bacteria on barley (Hordeum vulgare), bacterial colonization patterns, gene expression, and composition of seed endophytes were explored. Results This study used the soil-borne Ensifer meliloti, as well as Pantoea sp. and Pseudomonas sp. isolated from barley seeds, individually. The results demonstrated that those bacteria persisted in the rhizosphere but with different colonization patterns. Although root-leaf translocation was not observed, all three bacteria induced systemic resistance (ISR) against foliar fungal pathogens. Transcriptome analysis revealed that ion- and stress-related genes were regulated in plants that first encountered bacteria. Iron homeostasis and heat stress responses were involved in the response to E. meliloti and Pantoea sp., even if the iron content was not altered. Heat shock protein-encoding genes responded to inoculation with Pantoea sp. and Pseudomonas sp. Furthermore, bacterial inoculation affected the composition of seed endophytes. Investigation of the following generation indicated that the enhanced resistance was not heritable. Conclusions Here, using barley as a model, we highlighted different responses to three different beneficial bacteria as well as the influence of soil-borne Ensifer meliloti on the seed microbiome. In total, these results can help to understand the interaction between ISR-triggering bacteria and a crop plant, which is essential for the application of biological agents in sustainable agriculture.https://doi.org/10.1186/s12870-023-04484-5Induced systemic resistanceBacterial colonizationIron homeostasisSeed endophytesBarleyRhizosphere
spellingShingle Yongming Duan
Min Han
Maja Grimm
Jasper Schierstaedt
Jafargholi Imani
Massimiliano Cardinale
Marie Le Jean
Joseph Nesme
Søren J. Sørensen
Adam Schikora
Hordeum vulgare differentiates its response to beneficial bacteria
BMC Plant Biology
Induced systemic resistance
Bacterial colonization
Iron homeostasis
Seed endophytes
Barley
Rhizosphere
title Hordeum vulgare differentiates its response to beneficial bacteria
title_full Hordeum vulgare differentiates its response to beneficial bacteria
title_fullStr Hordeum vulgare differentiates its response to beneficial bacteria
title_full_unstemmed Hordeum vulgare differentiates its response to beneficial bacteria
title_short Hordeum vulgare differentiates its response to beneficial bacteria
title_sort hordeum vulgare differentiates its response to beneficial bacteria
topic Induced systemic resistance
Bacterial colonization
Iron homeostasis
Seed endophytes
Barley
Rhizosphere
url https://doi.org/10.1186/s12870-023-04484-5
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