A nucleoside signal generated by a fungal endophyte regulates host cell death and promotes root colonization

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-Review

Autorschaft

  • Nick Dunken
  • Heidi Widmer
  • Gerd U. Balcke
  • Henryk Straube
  • Gregor Langen
  • Nyasha M. Charura
  • Pia Saake
  • Concetta De Quattro
  • Jonas Schön
  • Hanna Rövenich
  • Stephan Wawra
  • Mamoona Khan
  • Armin Djamei
  • Matias D. Zurbriggen
  • Alain Tissier
  • Claus Peter Witte
  • Alga Zuccaro

Organisationseinheiten

Externe Organisationen

  • Universität zu Köln
  • Exzellenzcluster für Pflanzenwissenschaften CEPLAS
  • Leibniz-Institut für Pflanzenbiochemie, Halle (IPB)
  • Københavns Universitet
  • Universitätsklinikum Düsseldorf
  • Rheinische Friedrich-Wilhelms-Universität Bonn
  • Martin-Luther-Universität Halle-Wittenberg
Forschungs-netzwerk anzeigen

Details

OriginalspracheEnglisch
Seiten (von - bis)2161-2177.e7
Seitenumfang25
FachzeitschriftCell Host and Microbe
Jahrgang32
Ausgabenummer12
Frühes Online-Datum26 Nov. 2024
PublikationsstatusVeröffentlicht - 11 Dez. 2024

Abstract

The intracellular colonization of plant roots by the beneficial fungal endophyte Serendipita indica follows a biphasic strategy, including a host cell death phase that enables successful colonization of Arabidopsis thaliana roots. How host cell death is initiated and controlled is largely unknown. Here, we show that two fungal enzymes, the ecto-5′-nucleotidase SiE5NT and the nuclease SiNucA, act synergistically in the apoplast at the onset of cell death to produce deoxyadenosine (dAdo). The uptake of extracellular dAdo but not the structurally related adenosine activates cell death via the equilibrative nucleoside transporter ENT3. We identified a previously uncharacterized Toll-like interleukin 1 receptor (TIR)-nucleotide-binding leucine-rich repeat receptor (NLR) protein, ISI (induced by S. indica), as an intracellular factor that affects host cell death, fungal colonization, and growth promotion. Our data show that the combined activity of two fungal apoplastic enzymes promotes the production of a metabolite that engages TIR-NLR-modulated pathways to induce plant cell death, providing a link to immunometabolism in plants.

ASJC Scopus Sachgebiete

Zitieren

A nucleoside signal generated by a fungal endophyte regulates host cell death and promotes root colonization. / Dunken, Nick; Widmer, Heidi; Balcke, Gerd U. et al.
in: Cell Host and Microbe, Jahrgang 32, Nr. 12, 11.12.2024, S. 2161-2177.e7.

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-Review

Dunken, N, Widmer, H, Balcke, GU, Straube, H, Langen, G, Charura, NM, Saake, P, De Quattro, C, Schön, J, Rövenich, H, Wawra, S, Khan, M, Djamei, A, Zurbriggen, MD, Tissier, A, Witte, CP & Zuccaro, A 2024, 'A nucleoside signal generated by a fungal endophyte regulates host cell death and promotes root colonization', Cell Host and Microbe, Jg. 32, Nr. 12, S. 2161-2177.e7. https://doi.org/10.1016/j.chom.2024.10.020
Dunken, N., Widmer, H., Balcke, G. U., Straube, H., Langen, G., Charura, N. M., Saake, P., De Quattro, C., Schön, J., Rövenich, H., Wawra, S., Khan, M., Djamei, A., Zurbriggen, M. D., Tissier, A., Witte, C. P., & Zuccaro, A. (2024). A nucleoside signal generated by a fungal endophyte regulates host cell death and promotes root colonization. Cell Host and Microbe, 32(12), 2161-2177.e7. https://doi.org/10.1016/j.chom.2024.10.020
Dunken N, Widmer H, Balcke GU, Straube H, Langen G, Charura NM et al. A nucleoside signal generated by a fungal endophyte regulates host cell death and promotes root colonization. Cell Host and Microbe. 2024 Dez 11;32(12):2161-2177.e7. Epub 2024 Nov 26. doi: 10.1016/j.chom.2024.10.020
Dunken, Nick ; Widmer, Heidi ; Balcke, Gerd U. et al. / A nucleoside signal generated by a fungal endophyte regulates host cell death and promotes root colonization. in: Cell Host and Microbe. 2024 ; Jahrgang 32, Nr. 12. S. 2161-2177.e7.
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abstract = "The intracellular colonization of plant roots by the beneficial fungal endophyte Serendipita indica follows a biphasic strategy, including a host cell death phase that enables successful colonization of Arabidopsis thaliana roots. How host cell death is initiated and controlled is largely unknown. Here, we show that two fungal enzymes, the ecto-5′-nucleotidase SiE5NT and the nuclease SiNucA, act synergistically in the apoplast at the onset of cell death to produce deoxyadenosine (dAdo). The uptake of extracellular dAdo but not the structurally related adenosine activates cell death via the equilibrative nucleoside transporter ENT3. We identified a previously uncharacterized Toll-like interleukin 1 receptor (TIR)-nucleotide-binding leucine-rich repeat receptor (NLR) protein, ISI (induced by S. indica), as an intracellular factor that affects host cell death, fungal colonization, and growth promotion. Our data show that the combined activity of two fungal apoplastic enzymes promotes the production of a metabolite that engages TIR-NLR-modulated pathways to induce plant cell death, providing a link to immunometabolism in plants.",
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T1 - A nucleoside signal generated by a fungal endophyte regulates host cell death and promotes root colonization

AU - Dunken, Nick

AU - Widmer, Heidi

AU - Balcke, Gerd U.

AU - Straube, Henryk

AU - Langen, Gregor

AU - Charura, Nyasha M.

AU - Saake, Pia

AU - De Quattro, Concetta

AU - Schön, Jonas

AU - Rövenich, Hanna

AU - Wawra, Stephan

AU - Khan, Mamoona

AU - Djamei, Armin

AU - Zurbriggen, Matias D.

AU - Tissier, Alain

AU - Witte, Claus Peter

AU - Zuccaro, Alga

N1 - Publisher Copyright: © 2024 The Author(s)

PY - 2024/12/11

Y1 - 2024/12/11

N2 - The intracellular colonization of plant roots by the beneficial fungal endophyte Serendipita indica follows a biphasic strategy, including a host cell death phase that enables successful colonization of Arabidopsis thaliana roots. How host cell death is initiated and controlled is largely unknown. Here, we show that two fungal enzymes, the ecto-5′-nucleotidase SiE5NT and the nuclease SiNucA, act synergistically in the apoplast at the onset of cell death to produce deoxyadenosine (dAdo). The uptake of extracellular dAdo but not the structurally related adenosine activates cell death via the equilibrative nucleoside transporter ENT3. We identified a previously uncharacterized Toll-like interleukin 1 receptor (TIR)-nucleotide-binding leucine-rich repeat receptor (NLR) protein, ISI (induced by S. indica), as an intracellular factor that affects host cell death, fungal colonization, and growth promotion. Our data show that the combined activity of two fungal apoplastic enzymes promotes the production of a metabolite that engages TIR-NLR-modulated pathways to induce plant cell death, providing a link to immunometabolism in plants.

AB - The intracellular colonization of plant roots by the beneficial fungal endophyte Serendipita indica follows a biphasic strategy, including a host cell death phase that enables successful colonization of Arabidopsis thaliana roots. How host cell death is initiated and controlled is largely unknown. Here, we show that two fungal enzymes, the ecto-5′-nucleotidase SiE5NT and the nuclease SiNucA, act synergistically in the apoplast at the onset of cell death to produce deoxyadenosine (dAdo). The uptake of extracellular dAdo but not the structurally related adenosine activates cell death via the equilibrative nucleoside transporter ENT3. We identified a previously uncharacterized Toll-like interleukin 1 receptor (TIR)-nucleotide-binding leucine-rich repeat receptor (NLR) protein, ISI (induced by S. indica), as an intracellular factor that affects host cell death, fungal colonization, and growth promotion. Our data show that the combined activity of two fungal apoplastic enzymes promotes the production of a metabolite that engages TIR-NLR-modulated pathways to induce plant cell death, providing a link to immunometabolism in plants.

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KW - deoxyadenosine

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KW - equilibrative nucleoside transporter

KW - host-microbe interaction

KW - immunometabolism

KW - NLR

KW - nucleotide-binding leucine-rich repeat protein

KW - roots

KW - symbiotic cell death

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VL - 32

SP - 2161-2177.e7

JO - Cell Host and Microbe

JF - Cell Host and Microbe

SN - 1931-3128

IS - 12

ER -

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