A fungal sRNA silences a host plant transcription factor to promote arbuscular mycorrhizal symbiosis

Cross-kingdom RNA interference (ckRNAi) is a mechanism of interspecies communication where small RNAs (sRNAs) are transported from one organism to another; these sRNAs silence target genes in trans by loading into host AGO proteins. In this work, we investigated the occurrence of ckRNAi in Arbuscula...

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Autores: Silvestri, Alessandro, Ledford, William Conrad, Fiorilli, Valentina, Votta, Cristina, Scerna, Alessia, Tucconi, Jacopo, Mocchetti, Antonio, Grasso, Gianluca, Balestrini, Raffaella, Jin, Hailing, Rubio-Somoza, Ignacio, Lanfranco, Luisa
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2025
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/388629
Acceso en línea:http://hdl.handle.net/10261/388629
https://api.elsevier.com/content/abstract/scopus_id/85209774160
Access Level:acceso abierto
Palabra clave:Medicago truncatula
Rhizophagus irregularis
Arbuscular mycorrhizal symbiosis
Cross‐kingdom RNA interference
Small RNA
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oai_identifier_str oai:digital.csic.es:10261/388629
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv A fungal sRNA silences a host plant transcription factor to promote arbuscular mycorrhizal symbiosis
title A fungal sRNA silences a host plant transcription factor to promote arbuscular mycorrhizal symbiosis
spellingShingle A fungal sRNA silences a host plant transcription factor to promote arbuscular mycorrhizal symbiosis
Silvestri, Alessandro
Medicago truncatula
Rhizophagus irregularis
Arbuscular mycorrhizal symbiosis
Cross‐kingdom RNA interference
Small RNA
title_short A fungal sRNA silences a host plant transcription factor to promote arbuscular mycorrhizal symbiosis
title_full A fungal sRNA silences a host plant transcription factor to promote arbuscular mycorrhizal symbiosis
title_fullStr A fungal sRNA silences a host plant transcription factor to promote arbuscular mycorrhizal symbiosis
title_full_unstemmed A fungal sRNA silences a host plant transcription factor to promote arbuscular mycorrhizal symbiosis
title_sort A fungal sRNA silences a host plant transcription factor to promote arbuscular mycorrhizal symbiosis
dc.creator.none.fl_str_mv Silvestri, Alessandro
Ledford, William Conrad
Fiorilli, Valentina
Votta, Cristina
Scerna, Alessia
Tucconi, Jacopo
Mocchetti, Antonio
Grasso, Gianluca
Balestrini, Raffaella
Jin, Hailing
Rubio-Somoza, Ignacio
Lanfranco, Luisa
author Silvestri, Alessandro
author_facet Silvestri, Alessandro
Ledford, William Conrad
Fiorilli, Valentina
Votta, Cristina
Scerna, Alessia
Tucconi, Jacopo
Mocchetti, Antonio
Grasso, Gianluca
Balestrini, Raffaella
Jin, Hailing
Rubio-Somoza, Ignacio
Lanfranco, Luisa
author_role author
author2 Ledford, William Conrad
Fiorilli, Valentina
Votta, Cristina
Scerna, Alessia
Tucconi, Jacopo
Mocchetti, Antonio
Grasso, Gianluca
Balestrini, Raffaella
Jin, Hailing
Rubio-Somoza, Ignacio
Lanfranco, Luisa
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministero dell'Istruzione, dell'Università e della Ricerca
European Commission
Ministerio de Ciencia e Innovación (España)
Generalitat de Catalunya
Silvestri, Alessandro [0000-0002-1635-7050]
Ledford, William Conrad [0000-0001-7130-2960]
Fiorilli, Valentina [0000-0001-9805-1559]
Votta, Cristina [0000-0001-6685-6547]
Grasso, Gianluca [0000-0001-9865-0017]
Balestrini, Raffaella [0000-0002-5450-1746]
Jin, Hailing [0000-0001-5778-5193]
Rubio-Somoza, Ignacio [0000-0003-0754-816X]
Lanfranco, Luisa [0000-0002-3961-2552]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Medicago truncatula
Rhizophagus irregularis
Arbuscular mycorrhizal symbiosis
Cross‐kingdom RNA interference
Small RNA
topic Medicago truncatula
Rhizophagus irregularis
Arbuscular mycorrhizal symbiosis
Cross‐kingdom RNA interference
Small RNA
description Cross-kingdom RNA interference (ckRNAi) is a mechanism of interspecies communication where small RNAs (sRNAs) are transported from one organism to another; these sRNAs silence target genes in trans by loading into host AGO proteins. In this work, we investigated the occurrence of ckRNAi in Arbuscular Mycorrhizal Symbiosis (AMS). We used an in silico prediction analysis to identify a sRNA (Rir2216) from the AM fungus Rhizophagus irregularis and its putative plant gene target, the Medicago truncatula MtWRKY69 transcription factor. Heterologous co-expression assays in Nicotiana benthamiana, 5' RACE reactions and AGO1-immunoprecipitation assays from mycorrhizal roots were used to characterize the Rir2216-MtWRKY69 interaction. We further analyzed MtWRKY69 expression profile and the contribution of constitutive and conditional MtWRKY69 expression to AMS. We show that Rir2216 is loaded into an AGO1 silencing complex from the host plant M. truncatula, leading to cleavage of a host target transcript encoding for the MtWRKY69 transcription factor. MtWRKY69 is specifically downregulated in arbusculated cells in mycorrhizal roots and increased levels of MtWRKY69 expression led to a reduced AM colonization level. Our results indicate that MtWRKY69 silencing, mediated by a fungal sRNA, is relevant for AMS; we thus present the first experimental evidence of fungus to plant ckRNAi in AMS.
publishDate 2025
dc.date.none.fl_str_mv 2025
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/388629
https://api.elsevier.com/content/abstract/scopus_id/85209774160
url http://hdl.handle.net/10261/388629
https://api.elsevier.com/content/abstract/scopus_id/85209774160
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
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info:eu-repo/grantAgreement/MINECO/SEV-2015-0533/
info:eu-repo/grantAgreement/AEI/CEX2019-000902-S/
info:eu-repo/grantAgreement/EC/H2020/945043
The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1111/nph.20273
https://doi.org/10.1111/nph.20273
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
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dc.publisher.none.fl_str_mv John Wiley & Sons
publisher.none.fl_str_mv John Wiley & Sons
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
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spelling A fungal sRNA silences a host plant transcription factor to promote arbuscular mycorrhizal symbiosisSilvestri, AlessandroLedford, William ConradFiorilli, ValentinaVotta, CristinaScerna, AlessiaTucconi, JacopoMocchetti, AntonioGrasso, GianlucaBalestrini, RaffaellaJin, HailingRubio-Somoza, IgnacioLanfranco, LuisaMedicago truncatulaRhizophagus irregularisArbuscular mycorrhizal symbiosisCross‐kingdom RNA interferenceSmall RNACross-kingdom RNA interference (ckRNAi) is a mechanism of interspecies communication where small RNAs (sRNAs) are transported from one organism to another; these sRNAs silence target genes in trans by loading into host AGO proteins. In this work, we investigated the occurrence of ckRNAi in Arbuscular Mycorrhizal Symbiosis (AMS). We used an in silico prediction analysis to identify a sRNA (Rir2216) from the AM fungus Rhizophagus irregularis and its putative plant gene target, the Medicago truncatula MtWRKY69 transcription factor. Heterologous co-expression assays in Nicotiana benthamiana, 5' RACE reactions and AGO1-immunoprecipitation assays from mycorrhizal roots were used to characterize the Rir2216-MtWRKY69 interaction. We further analyzed MtWRKY69 expression profile and the contribution of constitutive and conditional MtWRKY69 expression to AMS. We show that Rir2216 is loaded into an AGO1 silencing complex from the host plant M. truncatula, leading to cleavage of a host target transcript encoding for the MtWRKY69 transcription factor. MtWRKY69 is specifically downregulated in arbusculated cells in mycorrhizal roots and increased levels of MtWRKY69 expression led to a reduced AM colonization level. Our results indicate that MtWRKY69 silencing, mediated by a fungal sRNA, is relevant for AMS; we thus present the first experimental evidence of fungus to plant ckRNAi in AMS.This work was supported by the project CN_00000033 funded under the National Recovery and Resilience Plan (NRRP), Mission 4 Component 2 Investment 1.4 – Call for tender No. 3138 of 16 December 2021, rectified by Decree n. 3175 of 18 December 2021 of the Italian Ministry of University and Research funded by the European Union – NextGenerationEU and by University of Turin (Ricerca locale). The work in the MoRE laboratory was funded by RTI2018-097262-B-I00 (funded by MCIN/AEI/10.13039/501100011033 and by ‘ERDF A way of making Europe’) and through the ‘Severo Ochoa Programme for Centres of Excellence in R&D’ 2016-2019 (SEV-2015-0533) and 2020-2023 (CEX2019-000902-S) funded by MCIN/AEI/10.13039/501100011033 and the CERCA program from the Generalitat de Catalunya. Postdoctoral fellowship to A.S. has received funding from the European Union's Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement No 945043.With funding from the Spanish goverment through the "Severo Ochoa Centre of Excellence" accreditation (SEV-2015-0533 and CEX2019-000902-S)Peer reviewedJohn Wiley & SonsMinistero dell'Istruzione, dell'Università e della RicercaEuropean CommissionMinisterio de Ciencia e Innovación (España)Generalitat de CatalunyaSilvestri, Alessandro [0000-0002-1635-7050]Ledford, William Conrad [0000-0001-7130-2960]Fiorilli, Valentina [0000-0001-9805-1559]Votta, Cristina [0000-0001-6685-6547]Grasso, Gianluca [0000-0001-9865-0017]Balestrini, Raffaella [0000-0002-5450-1746]Jin, Hailing [0000-0001-5778-5193]Rubio-Somoza, Ignacio [0000-0003-0754-816X]Lanfranco, Luisa [0000-0002-3961-2552]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202520252025info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/388629https://api.elsevier.com/content/abstract/scopus_id/85209774160reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-097262-B-I00info:eu-repo/grantAgreement/MINECO/SEV-2015-0533/info:eu-repo/grantAgreement/AEI/CEX2019-000902-S/info:eu-repo/grantAgreement/EC/H2020/945043The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1111/nph.20273https://doi.org/10.1111/nph.20273Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3886292026-05-22T06:33:51Z
score 15.81155

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