The identification of a key gene highlights macrocyclic ring’s role in trichothecene toxicity

[EN] Trichothecenes are toxins produced by certain species from several fungal genera, including Aspergillus, Fusarium, Isaria, Paramyrothecium, Stachybotrys, Trichoderma, and Trichothecium. These toxins are of interest because they contribute to the toxigenicity, plant pathogenicity, and/or biologi...

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Autores: McCormick, Susan P., Cardoza, Rosa E., Martínez-Reyes, Natalia, Vermillion, Karl, Busman, Mark, Rodríguez-González, Álvaro, Casquero, Pedro A., Proctor, Robert H., Gutiérrez , Santiago 1965-
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2024
País:España
Recursos:Universidad de León
Repositorio:BULERIA. Repositorio Institucional de la Universidad de León
OAI Identifier:oai:buleria.unileon.es:10612/23118
Acesso em linha:https://link.springer.com/article/10.1007/s00253-024-13297-x
https://hdl.handle.net/10612/23118
Access Level:acceso abierto
Palavra-chave:Biotecnología
Paramyrothecium roridum
Gene deletion
Macrocyclic trichothecenes
Trichothecene toxicity
Trichoverrins
2414 Microbiología
2414.06 Hongos
2415.01 Biología Molecular de Microorganismos
3108.02 Control Biológico de Enfermedades
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spelling The identification of a key gene highlights macrocyclic ring’s role in trichothecene toxicityLa identificación de un gen clave destaca el papel del anillo macrocíclico en la toxicidad del tricotecenoMcCormick, Susan P.Cardoza, Rosa E.Martínez-Reyes, NataliaVermillion, KarlBusman, MarkRodríguez-González, ÁlvaroCasquero, Pedro A.Proctor, Robert H.Gutiérrez , Santiago 1965-BiotecnologíaParamyrothecium roridumGene deletionMacrocyclic trichothecenesTrichothecene toxicityTrichoverrins2414 Microbiología2414.06 Hongos2415.01 Biología Molecular de Microorganismos3108.02 Control Biológico de Enfermedades[EN] Trichothecenes are toxins produced by certain species from several fungal genera, including Aspergillus, Fusarium, Isaria, Paramyrothecium, Stachybotrys, Trichoderma, and Trichothecium. These toxins are of interest because they contribute to the toxigenicity, plant pathogenicity, and/or biological control activities of some fungi. All trichothecenes have the same core (12,13-epoxytrichothec-9-ene or EPT) structure but can differ from one another by the presence or absence of a macrocyclic ring formed from polyketide and isoprenoid substituents esterified to carbon atoms 4 and 15 of EPT, respectively. Genes required for formation and some modifications of EPT have been elucidated, but almost nothing is known about genes specific to the formation of the macrocyclic ring. Therefore, we used genomic, transcriptomic, metabolomic, and gene deletion analyses to identify genes that are required specifically for the formation of the macrocyclic ring. These analyses identified one gene, TRI24, that is predicted to encode an acyltransferase and that is required for macrocyclic ring formation during biosynthesis of macrocyclic trichothecenes by the fungus Paramyrothecium roridum. In addition, a TRI24 deletion mutant of P. roridum caused less severe disease symptoms on common bean and had less antifungal activity than its wild-type progenitor strain. We propose that the reduced aggressiveness and antifungal activity of the mutant resulted from its inability to produce trichothecenes with a macrocyclic ring. To our knowledge, this is the first report of a gene required specifically for the formation of the macrocyclic ring of trichothecenes and that loss of the macrocyclic ring of trichothecenes can alter the biological activities of a fungus. KEY POINTS: • TRI24 gene is found in all known macrocyclic trichothecene-producing fungi. • A tri24-deletion mutant exhibits a reduction in antifungal and plant disease activities. • TRI24 is the first described gene specific to macrocyclic trichothecene biosynthesis.SISpringer LinkMicrobiologiaFacultad de Ciencias Biologicas y Ambientales2024info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttps://link.springer.com/article/10.1007/s00253-024-13297-xhttps://hdl.handle.net/10612/23118reponame:BULERIA. Repositorio Institucional de la Universidad de Leóninstname:Universidad de LeónIngléshttp://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:buleria.unileon.es:10612/231182026-06-24T12:43:27Z
dc.title.none.fl_str_mv The identification of a key gene highlights macrocyclic ring’s role in trichothecene toxicity
La identificación de un gen clave destaca el papel del anillo macrocíclico en la toxicidad del tricoteceno
title The identification of a key gene highlights macrocyclic ring’s role in trichothecene toxicity
spellingShingle The identification of a key gene highlights macrocyclic ring’s role in trichothecene toxicity
McCormick, Susan P.
Biotecnología
Paramyrothecium roridum
Gene deletion
Macrocyclic trichothecenes
Trichothecene toxicity
Trichoverrins
2414 Microbiología
2414.06 Hongos
2415.01 Biología Molecular de Microorganismos
3108.02 Control Biológico de Enfermedades
title_short The identification of a key gene highlights macrocyclic ring’s role in trichothecene toxicity
title_full The identification of a key gene highlights macrocyclic ring’s role in trichothecene toxicity
title_fullStr The identification of a key gene highlights macrocyclic ring’s role in trichothecene toxicity
title_full_unstemmed The identification of a key gene highlights macrocyclic ring’s role in trichothecene toxicity
title_sort The identification of a key gene highlights macrocyclic ring’s role in trichothecene toxicity
dc.creator.none.fl_str_mv McCormick, Susan P.
Cardoza, Rosa E.
Martínez-Reyes, Natalia
Vermillion, Karl
Busman, Mark
Rodríguez-González, Álvaro
Casquero, Pedro A.
Proctor, Robert H.
Gutiérrez , Santiago 1965-
author McCormick, Susan P.
author_facet McCormick, Susan P.
Cardoza, Rosa E.
Martínez-Reyes, Natalia
Vermillion, Karl
Busman, Mark
Rodríguez-González, Álvaro
Casquero, Pedro A.
Proctor, Robert H.
Gutiérrez , Santiago 1965-
author_role author
author2 Cardoza, Rosa E.
Martínez-Reyes, Natalia
Vermillion, Karl
Busman, Mark
Rodríguez-González, Álvaro
Casquero, Pedro A.
Proctor, Robert H.
Gutiérrez , Santiago 1965-
author2_role author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Microbiologia
Facultad de Ciencias Biologicas y Ambientales
dc.subject.none.fl_str_mv Biotecnología
Paramyrothecium roridum
Gene deletion
Macrocyclic trichothecenes
Trichothecene toxicity
Trichoverrins
2414 Microbiología
2414.06 Hongos
2415.01 Biología Molecular de Microorganismos
3108.02 Control Biológico de Enfermedades
topic Biotecnología
Paramyrothecium roridum
Gene deletion
Macrocyclic trichothecenes
Trichothecene toxicity
Trichoverrins
2414 Microbiología
2414.06 Hongos
2415.01 Biología Molecular de Microorganismos
3108.02 Control Biológico de Enfermedades
description [EN] Trichothecenes are toxins produced by certain species from several fungal genera, including Aspergillus, Fusarium, Isaria, Paramyrothecium, Stachybotrys, Trichoderma, and Trichothecium. These toxins are of interest because they contribute to the toxigenicity, plant pathogenicity, and/or biological control activities of some fungi. All trichothecenes have the same core (12,13-epoxytrichothec-9-ene or EPT) structure but can differ from one another by the presence or absence of a macrocyclic ring formed from polyketide and isoprenoid substituents esterified to carbon atoms 4 and 15 of EPT, respectively. Genes required for formation and some modifications of EPT have been elucidated, but almost nothing is known about genes specific to the formation of the macrocyclic ring. Therefore, we used genomic, transcriptomic, metabolomic, and gene deletion analyses to identify genes that are required specifically for the formation of the macrocyclic ring. These analyses identified one gene, TRI24, that is predicted to encode an acyltransferase and that is required for macrocyclic ring formation during biosynthesis of macrocyclic trichothecenes by the fungus Paramyrothecium roridum. In addition, a TRI24 deletion mutant of P. roridum caused less severe disease symptoms on common bean and had less antifungal activity than its wild-type progenitor strain. We propose that the reduced aggressiveness and antifungal activity of the mutant resulted from its inability to produce trichothecenes with a macrocyclic ring. To our knowledge, this is the first report of a gene required specifically for the formation of the macrocyclic ring of trichothecenes and that loss of the macrocyclic ring of trichothecenes can alter the biological activities of a fungus. KEY POINTS: • TRI24 gene is found in all known macrocyclic trichothecene-producing fungi. • A tri24-deletion mutant exhibits a reduction in antifungal and plant disease activities. • TRI24 is the first described gene specific to macrocyclic trichothecene biosynthesis.
publishDate 2024
dc.date.none.fl_str_mv 2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://link.springer.com/article/10.1007/s00253-024-13297-x
https://hdl.handle.net/10612/23118
url https://link.springer.com/article/10.1007/s00253-024-13297-x
https://hdl.handle.net/10612/23118
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Springer Link
publisher.none.fl_str_mv Springer Link
dc.source.none.fl_str_mv reponame:BULERIA. Repositorio Institucional de la Universidad de León
instname:Universidad de León
instname_str Universidad de León
reponame_str BULERIA. Repositorio Institucional de la Universidad de León
collection BULERIA. Repositorio Institucional de la Universidad de León
repository.name.fl_str_mv
repository.mail.fl_str_mv
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