Vacuolar H+-Pyrophosphatase AVP1 is Involved in Amine Fungicide Tolerance in Arabidopsis thaliana and Provides Tridemorph Resistance in Yeast

Amine fungicides are widely used as crop protectants. Their success is believed to be related to their ability to inhibit postlanosterol sterol biosynthesis in fungi, in particular sterol-Δ8,Δ7-isomerases and sterol-Δ14-reductases, with a concomitant accumulation of toxic abnormal sterols. However,...

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Autores: Hernández, Agustín, Herrera Palau, Rosana, Madroñal, Juan M., Albi Rodríguez, Tomás, López Lluch, Guillermo, Pérez Castiñeira, José Román, Navas Lloret, Plácido, Valverde Albacete, Federico, Serrano Delgado, Aurelio
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2016
País:España
Institución:Universidad de Sevilla (US)
Repositorio:idUS. Depósito de Investigación de la Universidad de Sevilla
OAI Identifier:oai:idus.us.es:11441/57481
Acceso en línea:http://hdl.handle.net/11441/57481
https://doi.org/10.3389/fpls.2016.00085
Access Level:acceso abierto
Palabra clave:pyrophosphate
cell death
abnormal sterols
vacuole
H+-pyrophosphatase
V-ATPase
fungicide
crop protection
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spelling Vacuolar H+-Pyrophosphatase AVP1 is Involved in Amine Fungicide Tolerance in Arabidopsis thaliana and Provides Tridemorph Resistance in YeastHernández, AgustínHerrera Palau, RosanaMadroñal, Juan M.Albi Rodríguez, TomásLópez Lluch, GuillermoPérez Castiñeira, José RománNavas Lloret, PlácidoValverde Albacete, FedericoSerrano Delgado, Aureliopyrophosphatecell deathabnormal sterolsvacuoleH+-pyrophosphataseV-ATPasefungicidecrop protectionAmine fungicides are widely used as crop protectants. Their success is believed to be related to their ability to inhibit postlanosterol sterol biosynthesis in fungi, in particular sterol-Δ8,Δ7-isomerases and sterol-Δ14-reductases, with a concomitant accumulation of toxic abnormal sterols. However, their actual cellular effects and mechanisms of death induction are still poorly understood. Paradoxically, plants exhibit a natural resistance to amine fungicides although they have similar enzymes in postcicloartenol sterol biosynthesis that are also susceptible to fungicide inhibition. A major difference in vacuolar ion homeostasis between plants and fungi is the presence of a dual set of primary proton pumps in the former (V-ATPase and H+-pyrophosphatase), but only the V-ATPase in the latter. Abnormal sterols affect the proton-pumping capacity of V-ATPases in fungi and this has been proposed as a major determinant in fungicide action. Using Saccharomyces cerevisiae as a model fungus, we provide evidence that amine fungicide treatment induced cell death by apoptosis. Cell death was concomitant with impaired H+-pumping capacity in vacuole vesicles and dependent on vacuolar proteases. Also, the heterologous expression of the Arabidopsis thaliana main H+-pyrophosphatase (AVP1) at the fungal vacuolar membrane reduced apoptosis levels in yeast and increased resistance to amine fungicides. Consistently, A. thaliana avp1 mutant seedlings showed increased susceptibility to this amine fungicide, particularly at the level of root development. This is in agreement with AVP1 being nearly the sole H+-pyrophosphatase gene expressed at the root elongation zones. All in all, the present data suggest that H+-pyrophosphatases are major determinants of plant tolerance to amine fungicides.España, Ministerio de Ciencia e innovación BFU2004-00843España, Ministerio de Ciencia e innovación, BFU2007-61887España, Ministerio de Ciencia e innovación BFU2010-15622Frontiers MediaBioquímica Vegetal y Biología Molecular2016info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/11441/57481https://doi.org/10.3389/fpls.2016.00085reponame:idUS. Depósito de Investigación de la Universidad de Sevillainstname:Universidad de Sevilla (US)InglésFrontiers in Plant Science, 7, 85-.BFU2004-00843BFU2007-61887BFU2010-15622http://dx.doi.org/ 10.3389/fpls.2016.00085info:eu-repo/semantics/openAccessoai:idus.us.es:11441/574812026-06-17T12:51:07Z
dc.title.none.fl_str_mv Vacuolar H+-Pyrophosphatase AVP1 is Involved in Amine Fungicide Tolerance in Arabidopsis thaliana and Provides Tridemorph Resistance in Yeast
title Vacuolar H+-Pyrophosphatase AVP1 is Involved in Amine Fungicide Tolerance in Arabidopsis thaliana and Provides Tridemorph Resistance in Yeast
spellingShingle Vacuolar H+-Pyrophosphatase AVP1 is Involved in Amine Fungicide Tolerance in Arabidopsis thaliana and Provides Tridemorph Resistance in Yeast
Hernández, Agustín
pyrophosphate
cell death
abnormal sterols
vacuole
H+-pyrophosphatase
V-ATPase
fungicide
crop protection
title_short Vacuolar H+-Pyrophosphatase AVP1 is Involved in Amine Fungicide Tolerance in Arabidopsis thaliana and Provides Tridemorph Resistance in Yeast
title_full Vacuolar H+-Pyrophosphatase AVP1 is Involved in Amine Fungicide Tolerance in Arabidopsis thaliana and Provides Tridemorph Resistance in Yeast
title_fullStr Vacuolar H+-Pyrophosphatase AVP1 is Involved in Amine Fungicide Tolerance in Arabidopsis thaliana and Provides Tridemorph Resistance in Yeast
title_full_unstemmed Vacuolar H+-Pyrophosphatase AVP1 is Involved in Amine Fungicide Tolerance in Arabidopsis thaliana and Provides Tridemorph Resistance in Yeast
title_sort Vacuolar H+-Pyrophosphatase AVP1 is Involved in Amine Fungicide Tolerance in Arabidopsis thaliana and Provides Tridemorph Resistance in Yeast
dc.creator.none.fl_str_mv Hernández, Agustín
Herrera Palau, Rosana
Madroñal, Juan M.
Albi Rodríguez, Tomás
López Lluch, Guillermo
Pérez Castiñeira, José Román
Navas Lloret, Plácido
Valverde Albacete, Federico
Serrano Delgado, Aurelio
author Hernández, Agustín
author_facet Hernández, Agustín
Herrera Palau, Rosana
Madroñal, Juan M.
Albi Rodríguez, Tomás
López Lluch, Guillermo
Pérez Castiñeira, José Román
Navas Lloret, Plácido
Valverde Albacete, Federico
Serrano Delgado, Aurelio
author_role author
author2 Herrera Palau, Rosana
Madroñal, Juan M.
Albi Rodríguez, Tomás
López Lluch, Guillermo
Pérez Castiñeira, José Román
Navas Lloret, Plácido
Valverde Albacete, Federico
Serrano Delgado, Aurelio
author2_role author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Bioquímica Vegetal y Biología Molecular
dc.subject.none.fl_str_mv pyrophosphate
cell death
abnormal sterols
vacuole
H+-pyrophosphatase
V-ATPase
fungicide
crop protection
topic pyrophosphate
cell death
abnormal sterols
vacuole
H+-pyrophosphatase
V-ATPase
fungicide
crop protection
description Amine fungicides are widely used as crop protectants. Their success is believed to be related to their ability to inhibit postlanosterol sterol biosynthesis in fungi, in particular sterol-Δ8,Δ7-isomerases and sterol-Δ14-reductases, with a concomitant accumulation of toxic abnormal sterols. However, their actual cellular effects and mechanisms of death induction are still poorly understood. Paradoxically, plants exhibit a natural resistance to amine fungicides although they have similar enzymes in postcicloartenol sterol biosynthesis that are also susceptible to fungicide inhibition. A major difference in vacuolar ion homeostasis between plants and fungi is the presence of a dual set of primary proton pumps in the former (V-ATPase and H+-pyrophosphatase), but only the V-ATPase in the latter. Abnormal sterols affect the proton-pumping capacity of V-ATPases in fungi and this has been proposed as a major determinant in fungicide action. Using Saccharomyces cerevisiae as a model fungus, we provide evidence that amine fungicide treatment induced cell death by apoptosis. Cell death was concomitant with impaired H+-pumping capacity in vacuole vesicles and dependent on vacuolar proteases. Also, the heterologous expression of the Arabidopsis thaliana main H+-pyrophosphatase (AVP1) at the fungal vacuolar membrane reduced apoptosis levels in yeast and increased resistance to amine fungicides. Consistently, A. thaliana avp1 mutant seedlings showed increased susceptibility to this amine fungicide, particularly at the level of root development. This is in agreement with AVP1 being nearly the sole H+-pyrophosphatase gene expressed at the root elongation zones. All in all, the present data suggest that H+-pyrophosphatases are major determinants of plant tolerance to amine fungicides.
publishDate 2016
dc.date.none.fl_str_mv 2016
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 http://hdl.handle.net/11441/57481
https://doi.org/10.3389/fpls.2016.00085
url http://hdl.handle.net/11441/57481
https://doi.org/10.3389/fpls.2016.00085
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Frontiers in Plant Science, 7, 85-.
BFU2004-00843
BFU2007-61887
BFU2010-15622
http://dx.doi.org/ 10.3389/fpls.2016.00085
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:idUS. Depósito de Investigación de la Universidad de Sevilla
instname:Universidad de Sevilla (US)
instname_str Universidad de Sevilla (US)
reponame_str idUS. Depósito de Investigación de la Universidad de Sevilla
collection idUS. Depósito de Investigación de la Universidad de Sevilla
repository.name.fl_str_mv
repository.mail.fl_str_mv
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