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Root exposure to apple replant disease soil triggers local defense response and rhizoplane microbiome dysbiosis

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-Review

Autorschaft

  • Alicia Balbín-Suárez
  • Samuel Jacquiod
  • Annmarie Deetja Rohr
  • Benye Liu
  • Traud Winkelmann

Externe Organisationen

  • Julius Kühn-Institut (JKI) Bundesforschungsinstitut für Kulturpflanzen
  • Institut national de recherche pour l’agriculture, l’alimentation et l’environnement (INRAE)
  • Technische Universität Braunschweig
  • Københavns Universitet
  • Helmholtz Zentrum München - Deutsches Forschungszentrum für Gesundheit und Umwelt
  • Martin-Luther-Universität Halle-Wittenberg
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Details

OriginalspracheEnglisch
Aufsatznummerfiab031
FachzeitschriftFEMS microbiology ecology
Jahrgang97
Ausgabenummer4
PublikationsstatusVeröffentlicht - Apr. 2021

Abstract

A soil column split-root experiment was designed to investigate the ability of apple replant disease (ARD)-causing agents to spread in soil. 'M26' apple rootstocks grew into a top layer of Control soil, followed by a barrier-free split-soil layer (Control soil/ARD soil). We observed a severely reduced root growth, concomitant with enhanced gene expression of phytoalexin biosynthetic genes and phytoalexin content in roots from ARD soil, indicating a pronounced local plant defense response. Amplicon sequencing (bacteria, archaea, fungi) revealed local shifts in diversity and composition of microorganisms in the rhizoplane of roots from ARD soil. An enrichment of operational taxonomic units affiliated to potential ARD fungal pathogens (Ilyonectria and Nectria sp.) and bacteria frequently associated with ARD (Streptomyces, Variovorax) was noted. In conclusion, our integrated study supports the idea of ARD being local and not spreading into surrounding soil, as only the roots in ARD soil were affected in terms of growth, phytoalexin biosynthetic gene expression, phytoalexin production and altered microbiome structure. This study further reinforces the microbiological nature of ARD, being likely triggered by a disturbed soil microbiome enriched with low mobility of the ARD-causing agents that induce a strong plant defense and rhizoplane microbiome dysbiosis, concurring with root damage.

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Root exposure to apple replant disease soil triggers local defense response and rhizoplane microbiome dysbiosis. / Balbín-Suárez, Alicia; Jacquiod, Samuel; Rohr, Annmarie Deetja et al.
in: FEMS microbiology ecology, Jahrgang 97, Nr. 4, fiab031, 04.2021.

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-Review

Balbín-Suárez, A, Jacquiod, S, Rohr, AD, Liu, B, Flachowsky, H, Winkelmann, T, Beerhues, L, Nesme, J, Sørensen, SJ, Vetterlein, D & Smalla, K 2021, 'Root exposure to apple replant disease soil triggers local defense response and rhizoplane microbiome dysbiosis', FEMS microbiology ecology, Jg. 97, Nr. 4, fiab031. https://doi.org/10.1093/femsec/fiab031
Balbín-Suárez, A., Jacquiod, S., Rohr, A. D., Liu, B., Flachowsky, H., Winkelmann, T., Beerhues, L., Nesme, J., Sørensen, S. J., Vetterlein, D., & Smalla, K. (2021). Root exposure to apple replant disease soil triggers local defense response and rhizoplane microbiome dysbiosis. FEMS microbiology ecology, 97(4), Artikel fiab031. https://doi.org/10.1093/femsec/fiab031
Balbín-Suárez A, Jacquiod S, Rohr AD, Liu B, Flachowsky H, Winkelmann T et al. Root exposure to apple replant disease soil triggers local defense response and rhizoplane microbiome dysbiosis. FEMS microbiology ecology. 2021 Apr;97(4):fiab031. doi: 10.1093/femsec/fiab031
Balbín-Suárez, Alicia ; Jacquiod, Samuel ; Rohr, Annmarie Deetja et al. / Root exposure to apple replant disease soil triggers local defense response and rhizoplane microbiome dysbiosis. in: FEMS microbiology ecology. 2021 ; Jahrgang 97, Nr. 4.
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title = "Root exposure to apple replant disease soil triggers local defense response and rhizoplane microbiome dysbiosis",
abstract = "A soil column split-root experiment was designed to investigate the ability of apple replant disease (ARD)-causing agents to spread in soil. 'M26' apple rootstocks grew into a top layer of Control soil, followed by a barrier-free split-soil layer (Control soil/ARD soil). We observed a severely reduced root growth, concomitant with enhanced gene expression of phytoalexin biosynthetic genes and phytoalexin content in roots from ARD soil, indicating a pronounced local plant defense response. Amplicon sequencing (bacteria, archaea, fungi) revealed local shifts in diversity and composition of microorganisms in the rhizoplane of roots from ARD soil. An enrichment of operational taxonomic units affiliated to potential ARD fungal pathogens (Ilyonectria and Nectria sp.) and bacteria frequently associated with ARD (Streptomyces, Variovorax) was noted. In conclusion, our integrated study supports the idea of ARD being local and not spreading into surrounding soil, as only the roots in ARD soil were affected in terms of growth, phytoalexin biosynthetic gene expression, phytoalexin production and altered microbiome structure. This study further reinforces the microbiological nature of ARD, being likely triggered by a disturbed soil microbiome enriched with low mobility of the ARD-causing agents that induce a strong plant defense and rhizoplane microbiome dysbiosis, concurring with root damage.",
keywords = "phytoalexins, root system architecture, soil microbiome, split-root experiment, X-ray computed tomography",
author = "Alicia Balb{\'i}n-Su{\'a}rez and Samuel Jacquiod and Rohr, {Annmarie Deetja} and Benye Liu and Henryk Flachowsky and Traud Winkelmann and Ludger Beerhues and Joseph Nesme and S{\o}rensen, {S{\o}ren J.} and Doris Vetterlein and Kornelia Smalla",
note = "We thank Andreas Wrede and the UFZ Workshop for kindly providing us with the material necessary to conduct the experiment (field site maintenance and split-root columns, respectively). We thank Ina-Maria Zickenrott for conducting the column experiment, X-ray CT scanning and all WinRHIZO analyses. We thank Maik Lucas for time resolved X-ray CT analyses and Eva Lippold for calculation of X-ray CT dose. We thank Jasmin Schmidt for excellent technical assistance, and Doreen Babin and DavidAlain Barbeoc{\textquoteright}h for great scientific and graphic design advice, ´ respectively This work was supported by the BonaRes initiative of the German Federal Ministry of Education and Research (BMBF, Bundesministerium fur Bildung und Forschung) (FZK 031B0025G, ¨ FZK 031B0025A and FZK 031B0025B). Samuel Jacquiod was supported by the Universite de Bourgogne Franche-Comt ´ e via ´ the ISITE-BFC International Junior Fellowship award (AAP3: RA19028.AEC.IS). The work of Annmarie-Deetja Rohr was part of the Research Training Group GRK1798 {\textquoteleft}Signaling at the Plant– Soil Interface{\textquoteright} funded by the German Research Foundation (DFG, Deutsche Forschungsgemeinschaft).",
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doi = "10.1093/femsec/fiab031",
language = "English",
volume = "97",
journal = "FEMS microbiology ecology",
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publisher = "Oxford University Press",
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Download

TY - JOUR

T1 - Root exposure to apple replant disease soil triggers local defense response and rhizoplane microbiome dysbiosis

AU - Balbín-Suárez, Alicia

AU - Jacquiod, Samuel

AU - Rohr, Annmarie Deetja

AU - Liu, Benye

AU - Flachowsky, Henryk

AU - Winkelmann, Traud

AU - Beerhues, Ludger

AU - Nesme, Joseph

AU - Sørensen, Søren J.

AU - Vetterlein, Doris

AU - Smalla, Kornelia

N1 - We thank Andreas Wrede and the UFZ Workshop for kindly providing us with the material necessary to conduct the experiment (field site maintenance and split-root columns, respectively). We thank Ina-Maria Zickenrott for conducting the column experiment, X-ray CT scanning and all WinRHIZO analyses. We thank Maik Lucas for time resolved X-ray CT analyses and Eva Lippold for calculation of X-ray CT dose. We thank Jasmin Schmidt for excellent technical assistance, and Doreen Babin and DavidAlain Barbeoc’h for great scientific and graphic design advice, ´ respectively This work was supported by the BonaRes initiative of the German Federal Ministry of Education and Research (BMBF, Bundesministerium fur Bildung und Forschung) (FZK 031B0025G, ¨ FZK 031B0025A and FZK 031B0025B). Samuel Jacquiod was supported by the Universite de Bourgogne Franche-Comt ´ e via ´ the ISITE-BFC International Junior Fellowship award (AAP3: RA19028.AEC.IS). The work of Annmarie-Deetja Rohr was part of the Research Training Group GRK1798 ‘Signaling at the Plant– Soil Interface’ funded by the German Research Foundation (DFG, Deutsche Forschungsgemeinschaft).

PY - 2021/4

Y1 - 2021/4

N2 - A soil column split-root experiment was designed to investigate the ability of apple replant disease (ARD)-causing agents to spread in soil. 'M26' apple rootstocks grew into a top layer of Control soil, followed by a barrier-free split-soil layer (Control soil/ARD soil). We observed a severely reduced root growth, concomitant with enhanced gene expression of phytoalexin biosynthetic genes and phytoalexin content in roots from ARD soil, indicating a pronounced local plant defense response. Amplicon sequencing (bacteria, archaea, fungi) revealed local shifts in diversity and composition of microorganisms in the rhizoplane of roots from ARD soil. An enrichment of operational taxonomic units affiliated to potential ARD fungal pathogens (Ilyonectria and Nectria sp.) and bacteria frequently associated with ARD (Streptomyces, Variovorax) was noted. In conclusion, our integrated study supports the idea of ARD being local and not spreading into surrounding soil, as only the roots in ARD soil were affected in terms of growth, phytoalexin biosynthetic gene expression, phytoalexin production and altered microbiome structure. This study further reinforces the microbiological nature of ARD, being likely triggered by a disturbed soil microbiome enriched with low mobility of the ARD-causing agents that induce a strong plant defense and rhizoplane microbiome dysbiosis, concurring with root damage.

AB - A soil column split-root experiment was designed to investigate the ability of apple replant disease (ARD)-causing agents to spread in soil. 'M26' apple rootstocks grew into a top layer of Control soil, followed by a barrier-free split-soil layer (Control soil/ARD soil). We observed a severely reduced root growth, concomitant with enhanced gene expression of phytoalexin biosynthetic genes and phytoalexin content in roots from ARD soil, indicating a pronounced local plant defense response. Amplicon sequencing (bacteria, archaea, fungi) revealed local shifts in diversity and composition of microorganisms in the rhizoplane of roots from ARD soil. An enrichment of operational taxonomic units affiliated to potential ARD fungal pathogens (Ilyonectria and Nectria sp.) and bacteria frequently associated with ARD (Streptomyces, Variovorax) was noted. In conclusion, our integrated study supports the idea of ARD being local and not spreading into surrounding soil, as only the roots in ARD soil were affected in terms of growth, phytoalexin biosynthetic gene expression, phytoalexin production and altered microbiome structure. This study further reinforces the microbiological nature of ARD, being likely triggered by a disturbed soil microbiome enriched with low mobility of the ARD-causing agents that induce a strong plant defense and rhizoplane microbiome dysbiosis, concurring with root damage.

KW - phytoalexins

KW - root system architecture

KW - soil microbiome

KW - split-root experiment

KW - X-ray computed tomography

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U2 - 10.1093/femsec/fiab031

DO - 10.1093/femsec/fiab031

M3 - Article

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VL - 97

JO - FEMS microbiology ecology

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SN - 0168-6496

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M1 - fiab031

ER -

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