Carbohydrate-active enzymes from a core root mycobiota member enable infection of multiple plant hosts
Abstract
The root microbiome includes fungal pathogens capable of colonizing multiple plant hosts, yet the underlying genetic determinants remain unknown. Here we report that Plectosphaerella cucumerina is a core member of the Arabidopsis thaliana root microbiota, which displays pathogenic potential across multiple hosts. Using a collection of 72 Plectosphaerella isolates and whole-genome sequencing, we observed subtle phenotypic and genotypic variation associated with fungal phylogeny but not host plant identity. Transcriptome profiling of a P. cucumerina isolate in roots of diverse plants revealed core and host-specific fungal responses, including induction of carbohydrate-active enzymes (CAZymes) involved in root cell wall deconstruction. A fungal gene encoding a candidate β-1,3-glucanase (GH64) was identified as a key genetic factor driving multihost infection. This gene is present across plant-colonizing fungi and functions as a disease determinant in both P. cucumerina and a Colletotrichum root pathogen. Our results indicate that host-induced CAZymes can couple fungal virulence with multihost compatibility.
Root mycobiota members can establish beneficial relationships with plants but also conditionally cause diseases or hamper plant performance 1-3 . Several core fungal taxa that reproducibly colonize roots of healthy plants are harmful under laboratory conditions 4-6 , illustrating that the pathogenic lifestyle of several root mycobiota members is often kept at bay in nature. In Arabidopsis thaliana, it has been reported that the protective activity of bacterial root commensals is as important as the innate immune branch involving tryptophan-derived specialized metabolites for controlling fungi in roots 2,6-8 , thereby maintaining microbial interkingdom balance for plant health 9 .
Given that soil and root-associated fungal communities are extensively shaped by the local climatic, edaphic and host conditions 10-12 , high endemism in fungal communities has been repeatedly reported 13 . Widespread fungal root colonizers appear particularly successful due to their ability to efficiently disperse, infect multiple hosts and plastically adapt to various environmental conditions 14 . However, the underlying molecular mechanisms enabling adaptation to a broad range of hosts and environments in root mycobiota members remain unknown.
Plant-associated fungi produce remarkable cocktails of carbohydrate-active enzymes (CAZymes) that facilitate fungal entry
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BibTeX
@article{rajakumar2026carbohydrateactive,
title = {{Carbohydrate-active enzymes from a core root mycobiota member enable infection of multiple plant hosts}},
author = {Ram-Sevak Raja-Kumar and Fantin Mesny and Arpan Kumar Basak and Jacy Newfeld and Guillaume Chesneau and Frederickson Entila and Tak Lee and Linda Rigerte and Stephanie Carvajal Acevedo and Bruno Hüttel and Pedro W Crous and Jose G Maciá-Vicente and Helen Stewart and Matthew Ryan and Ahmad M Fakhoury and Soledad Sacristán and Meriem Aitouguinane and Isabelle Batisson and Stefano Dumontet and Wade H Elmer and Jana Henzelyová and Joanna S Kruszewska and Jessica M Nelson and Cara M Santelli and Markus Pauly and Antonio Molina and Kei Hiruma and Stéphane Hacquard},
journal = {Nature Microbiology},
year = {2026},
month = oct,
doi = {10.1038/s41564-026-02492-3},
url = {https://hal.science/hal-05805653v1},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Carbohydrate-active enzymes from a core root mycobiota member enable infection of multiple plant hosts
AU - Ram-Sevak Raja-Kumar
AU - Fantin Mesny
AU - Arpan Kumar Basak
AU - Jacy Newfeld
AU - Guillaume Chesneau
AU - Frederickson Entila
AU - Tak Lee
AU - Linda Rigerte
AU - Stephanie Carvajal Acevedo
AU - Bruno Hüttel
AU - Pedro W Crous
AU - Jose G Maciá-Vicente
AU - Helen Stewart
AU - Matthew Ryan
AU - Ahmad M Fakhoury
AU - Soledad Sacristán
AU - Meriem Aitouguinane
AU - Isabelle Batisson
AU - Stefano Dumontet
AU - Wade H Elmer
AU - Jana Henzelyová
AU - Joanna S Kruszewska
AU - Jessica M Nelson
AU - Cara M Santelli
AU - Markus Pauly
AU - Antonio Molina
AU - Kei Hiruma
AU - Stéphane Hacquard
PY - 2026
DA - 2026/10/01
JO - Nature Microbiology
DO - 10.1038/s41564-026-02492-3
UR - https://hal.science/hal-05805653v1
AB - The root microbiome includes fungal pathogens capable of colonizing multiple plant hosts, yet the underlying genetic determinants remain unknown. Here we report that Plectosphaerella cucumerina is a core member of the Arabidopsis thaliana root microbiota, which displays pathogenic potential across multiple hosts. Using a collection of 72 Plectosphaerella isolates and whole-genome sequencing, we observed subtle phenotypic and genotypic variation associated with fungal phylogeny but not host plant identity. Transcriptome profiling of a P. cucumerina isolate in roots of diverse plants revealed core and host-specific fungal responses, including induction of carbohydrate-active enzymes (CAZymes) involved in root cell wall deconstruction. A fungal gene encoding a candidate β-1,3-glucanase (GH64) was identified as a key genetic factor driving multihost infection. This gene is present across plant-colonizing fungi and functions as a disease determinant in both P. cucumerina and a Colletotrichum root pathogen. Our results indicate that host-induced CAZymes can couple fungal virulence with multihost compatibility. Root mycobiota members can establish beneficial relationships with plants but also conditionally cause diseases or hamper plant performance 1-3 . Several core fungal taxa that reproducibly colonize roots of healthy plants are harmful under laboratory conditions 4-6 , illustrating that the pathogenic lifestyle of several root mycobiota members is often kept at bay in nature. In Arabidopsis thaliana, it has been reported that the protective activity of bacterial root commensals is as important as the innate immune branch involving tryptophan-derived specialized metabolites for controlling fungi in roots 2,6-8 , thereby maintaining microbial interkingdom balance for plant health 9 . Given that soil and root-associated fungal communities are extensively shaped by the local climatic, edaphic and host conditions 10-12 , high endemism in fungal communities has been repeatedly reported 13 . Widespread fungal root colonizers appear particularly successful due to their ability to efficiently disperse, infect multiple hosts and plastically adapt to various environmental conditions 14 . However, the underlying molecular mechanisms enabling adaptation to a broad range of hosts and environments in root mycobiota members remain unknown. Plant-associated fungi produce remarkable cocktails of carbohydrate-active enzymes (CAZymes) that facilitate fungal entry
SN - 2058-5276
SN - 2058-5276
ER -