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Gliotoxin, an Immunosuppressive Fungal Metabolite, Primes Plant Immunity: Evidence from BrowZine Journal Cover Trichoderma virens-Tomato Interaction
Year:
2022
Source of publication :
mBio
Authors :
Bar, Maya
;
.
Gupta, Rupali K.
;
.
Leibman-Markus, Meirav
;
.
Volume :
Co-Authors:

Rinat Zaid
Roni Koren
Efrat Kligun
Rupali Gupta 
Meirav Leibman-Markus
Prasun K Mukherjee 
Charles M Kenerley
Maya Bar
Benjamin A Horwitz 

Facilitators :
From page:
0
To page:
0
(
Total pages:
1
)
Abstract:

Beneficial interaction of members of the fungal genus Trichoderma with plant roots primes the plant immune system, promoting systemic resistance to pathogen infection. Some strains of Trichoderma virens produce gliotoxin, a fungal epidithiodioxopiperazine (ETP)-type secondary metabolite that is toxic to animal cells. It induces apoptosis, prevents NF-κB activation via the inhibition of the proteasome, and has immunosuppressive properties. Gliotoxin is known to be involved in the antagonism of rhizosphere microorganisms. To investigate whether this metabolite has a role in the interaction of Trichoderma with plant roots, we compared gliotoxin-producing and nonproducing T. virens strains. Both colonize the root surface and outer layers, but they have differential effects on root growth and architecture. The responses of tomato plants to a pathogen challenge were followed at several levels: lesion development, levels of ethylene, and reactive oxygen species. The transcriptomic signature of the shoot tissue in response to root interaction with producing and nonproducing T. virens strains was monitored. Gliotoxin producers provided stronger protection against foliar pathogens, compared to nonproducing strains. This was reflected in the transcriptomic signature, which showed the induction of defense-related genes. Two markers of plant defense response, PR1 and Pti-5, were differentially induced in response to pure gliotoxin. Gliotoxin thus acts as a microbial signal, which the plant immune system recognizes, directly or indirectly, to promote a defense response. IMPORTANCE A single fungal metabolite induces far-reaching transcriptomic reprogramming in the plant, priming immune responses and defense, in contrast to its immunosuppressive effect on animal cells. While the negative effects of gliotoxin-producing Trichoderma strains on growth may be observed only under a particular set of laboratory conditions, gliotoxin-linked molecular patterns, including the potential for limited cell death, could strongly prime plant defense, even in mature soil-grown plants in which the same Trichoderma strain promotes growth.

Note:
Related Files :
gliotoxin
immunity
plant symbiont
root
tomato
Trichoderma
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More details
DOI :
10.1128/mbio.00389-22
Article number:
0
Affiliations:
Database:
PubMed
Publication Type:
article
;
.
Language:
English
Editors' remarks:
ID:
61677
Last updated date:
30/08/2022 13:34
Creation date:
30/08/2022 13:34
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Scientific Publication
Gliotoxin, an Immunosuppressive Fungal Metabolite, Primes Plant Immunity: Evidence from BrowZine Journal Cover Trichoderma virens-Tomato Interaction

Rinat Zaid
Roni Koren
Efrat Kligun
Rupali Gupta 
Meirav Leibman-Markus
Prasun K Mukherjee 
Charles M Kenerley
Maya Bar
Benjamin A Horwitz 

Gliotoxin, an Immunosuppressive Fungal Metabolite, Primes Plant Immunity: Evidence from BrowZine Journal Cover Trichoderma virens-Tomato Interaction

Beneficial interaction of members of the fungal genus Trichoderma with plant roots primes the plant immune system, promoting systemic resistance to pathogen infection. Some strains of Trichoderma virens produce gliotoxin, a fungal epidithiodioxopiperazine (ETP)-type secondary metabolite that is toxic to animal cells. It induces apoptosis, prevents NF-κB activation via the inhibition of the proteasome, and has immunosuppressive properties. Gliotoxin is known to be involved in the antagonism of rhizosphere microorganisms. To investigate whether this metabolite has a role in the interaction of Trichoderma with plant roots, we compared gliotoxin-producing and nonproducing T. virens strains. Both colonize the root surface and outer layers, but they have differential effects on root growth and architecture. The responses of tomato plants to a pathogen challenge were followed at several levels: lesion development, levels of ethylene, and reactive oxygen species. The transcriptomic signature of the shoot tissue in response to root interaction with producing and nonproducing T. virens strains was monitored. Gliotoxin producers provided stronger protection against foliar pathogens, compared to nonproducing strains. This was reflected in the transcriptomic signature, which showed the induction of defense-related genes. Two markers of plant defense response, PR1 and Pti-5, were differentially induced in response to pure gliotoxin. Gliotoxin thus acts as a microbial signal, which the plant immune system recognizes, directly or indirectly, to promote a defense response. IMPORTANCE A single fungal metabolite induces far-reaching transcriptomic reprogramming in the plant, priming immune responses and defense, in contrast to its immunosuppressive effect on animal cells. While the negative effects of gliotoxin-producing Trichoderma strains on growth may be observed only under a particular set of laboratory conditions, gliotoxin-linked molecular patterns, including the potential for limited cell death, could strongly prime plant defense, even in mature soil-grown plants in which the same Trichoderma strain promotes growth.

Scientific Publication
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