Details
| Original language | English |
|---|---|
| Pages (from-to) | 2161-2177.e7 |
| Number of pages | 25 |
| Journal | Cell Host and Microbe |
| Volume | 32 |
| Issue number | 12 |
| Early online date | 26 Nov 2024 |
| Publication status | Published - 11 Dec 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.
Keywords
- beneficial fungi, deoxyadenosine, ENT3, equilibrative nucleoside transporter, host-microbe interaction, immunometabolism, NLR, nucleotide-binding leucine-rich repeat protein, roots, symbiotic cell death
ASJC Scopus subject areas
- Immunology and Microbiology(all)
- Parasitology
- Immunology and Microbiology(all)
- Microbiology
- Immunology and Microbiology(all)
- Virology
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In: Cell Host and Microbe, Vol. 32, No. 12, 11.12.2024, p. 2161-2177.e7.
Research output: Contribution to journal › Article › Research › peer review
}
TY - JOUR
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.
KW - beneficial fungi
KW - deoxyadenosine
KW - ENT3
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
UR - http://www.scopus.com/inward/record.url?scp=85211093000&partnerID=8YFLogxK
U2 - 10.1016/j.chom.2024.10.020
DO - 10.1016/j.chom.2024.10.020
M3 - Article
C2 - 39603244
AN - SCOPUS:85211093000
VL - 32
SP - 2161-2177.e7
JO - Cell Host and Microbe
JF - Cell Host and Microbe
SN - 1931-3128
IS - 12
ER -