An autophagy-related kinase is essential for the symbiotic relationship between phaseolus vulgaris and both rhizobia and arbuscular mycorrhizal fungi

Autores
Estrada Navarrete, Georgina; Cruz Mireles, Neftaly; Lascano, Hernan Ramiro; Alvarado Affantranger, Xóchitl; Hernández Barrera, Alejandra; Barraza, Aarón; Olivares, Juan E.; Arthikala, Manoj Kumar; Cárdenas, Luis; Quinto, Carmen; Sanchez, Federico
Año de publicación
2016
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Eukaryotes contain three types of lipid kinases that belong to the phosphatidylinositol 3-kinase (PI3K) family. In plants and Saccharomyces cerevisiae, only PI3K class III family members have been identified. These enzymes regulate the innate immune response, intracellular trafficking, autophagy, and senescence. Here, we report that RNAi-mediated downregulation of common bean (Phaseolus vulgaris) PI3K severely impaired symbiosis in composite P. vulgaris plants with endosymbionts such as Rhizobium tropici and Rhizophagus irregularis. Downregulation of Pv-PI3K was associated with a marked decrease in root hair growth and curling. Additionally, infection thread growth, root-nodule number, and symbiosome formation in root nodule cells were severely affected. Interestingly, root colonization by AM fungi and the formation of arbuscules were also abolished in PI3K loss-of-function plants. Furthermore, the transcript accumulation of genes encoding proteins known to interact with PI3K to form protein complexes involved in autophagy was drastically reduced in these transgenic roots. RNAimediated downregulation of one of these genes, Beclin1/Atg6, resulted in a similar phenotype as observed for transgenic roots in which Pv-PI3K had been downregulated. Our findings show that an autophagy-related process is crucial for the mutualistic interactions of P. vulgaris with beneficial microorganisms.
Fil: Estrada Navarrete, Georgina. Universidad Nacional Autónoma de México; México
Fil: Cruz Mireles, Neftaly. Universidad Nacional Autónoma de México; México
Fil: Lascano, Hernan Ramiro. Instituto Nacional de Tecnología Agropecuaria. Centro de Investigaciones Agropecuarias. Instituto de Fisiología y Recursos Genéticos Vegetales; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba; Argentina
Fil: Alvarado Affantranger, Xóchitl. Universidad Nacional Autónoma de México; México
Fil: Hernández Barrera, Alejandra. Universidad Nacional Autónoma de México; México
Fil: Barraza, Aarón. Universidad Nacional Autónoma de México; México
Fil: Olivares, Juan E.. Universidad Nacional Autónoma de México; México
Fil: Arthikala, Manoj Kumar. Universidad Nacional Autónoma de México; México
Fil: Cárdenas, Luis. Universidad Nacional Autónoma de México; México
Fil: Quinto, Carmen. Universidad Nacional Autónoma de México; México
Fil: Sanchez, Federico. Universidad Nacional Autónoma de México; México
Materia
Gene silencing - RNA interference/RNAi,
Plant-microbe symbiosis
Autophagy
Root development - root nodules
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/161260
Acceder
id CONICETDig_3a286779b7f88c6c4230be8475636e79
oai_identifier_str oai:ri.conicet.gov.ar:11336/161260
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling An autophagy-related kinase is essential for the symbiotic relationship between phaseolus vulgaris and both rhizobia and arbuscular mycorrhizal fungiEstrada Navarrete, GeorginaCruz Mireles, NeftalyLascano, Hernan RamiroAlvarado Affantranger, XóchitlHernández Barrera, AlejandraBarraza, AarónOlivares, Juan E.Arthikala, Manoj KumarCárdenas, LuisQuinto, CarmenSanchez, FedericoGene silencing - RNA interference/RNAi,Plant-microbe symbiosisAutophagyRoot development - root noduleshttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Eukaryotes contain three types of lipid kinases that belong to the phosphatidylinositol 3-kinase (PI3K) family. In plants and Saccharomyces cerevisiae, only PI3K class III family members have been identified. These enzymes regulate the innate immune response, intracellular trafficking, autophagy, and senescence. Here, we report that RNAi-mediated downregulation of common bean (Phaseolus vulgaris) PI3K severely impaired symbiosis in composite P. vulgaris plants with endosymbionts such as Rhizobium tropici and Rhizophagus irregularis. Downregulation of Pv-PI3K was associated with a marked decrease in root hair growth and curling. Additionally, infection thread growth, root-nodule number, and symbiosome formation in root nodule cells were severely affected. Interestingly, root colonization by AM fungi and the formation of arbuscules were also abolished in PI3K loss-of-function plants. Furthermore, the transcript accumulation of genes encoding proteins known to interact with PI3K to form protein complexes involved in autophagy was drastically reduced in these transgenic roots. RNAimediated downregulation of one of these genes, Beclin1/Atg6, resulted in a similar phenotype as observed for transgenic roots in which Pv-PI3K had been downregulated. Our findings show that an autophagy-related process is crucial for the mutualistic interactions of P. vulgaris with beneficial microorganisms.Fil: Estrada Navarrete, Georgina. Universidad Nacional Autónoma de México; MéxicoFil: Cruz Mireles, Neftaly. Universidad Nacional Autónoma de México; MéxicoFil: Lascano, Hernan Ramiro. Instituto Nacional de Tecnología Agropecuaria. Centro de Investigaciones Agropecuarias. Instituto de Fisiología y Recursos Genéticos Vegetales; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba; ArgentinaFil: Alvarado Affantranger, Xóchitl. Universidad Nacional Autónoma de México; MéxicoFil: Hernández Barrera, Alejandra. Universidad Nacional Autónoma de México; MéxicoFil: Barraza, Aarón. Universidad Nacional Autónoma de México; MéxicoFil: Olivares, Juan E.. Universidad Nacional Autónoma de México; MéxicoFil: Arthikala, Manoj Kumar. Universidad Nacional Autónoma de México; MéxicoFil: Cárdenas, Luis. Universidad Nacional Autónoma de México; MéxicoFil: Quinto, Carmen. Universidad Nacional Autónoma de México; MéxicoFil: Sanchez, Federico. Universidad Nacional Autónoma de México; MéxicoAmerican Society of Plant Biologist2016-09info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/161260Estrada Navarrete, Georgina; Cruz Mireles, Neftaly; Lascano, Hernan Ramiro; Alvarado Affantranger, Xóchitl; Hernández Barrera, Alejandra; et al.; An autophagy-related kinase is essential for the symbiotic relationship between phaseolus vulgaris and both rhizobia and arbuscular mycorrhizal fungi; American Society of Plant Biologist; Plant Cell; 28; 9; 9-2016; 2326-23411040-46511532-298XCONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/plcell/article/28/9/2326/6098387info:eu-repo/semantics/altIdentifier/doi/10.1105/tpc.15.01012info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-10T13:02:06Zoai:ri.conicet.gov.ar:11336/161260instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-10 13:02:07.173CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv An autophagy-related kinase is essential for the symbiotic relationship between phaseolus vulgaris and both rhizobia and arbuscular mycorrhizal fungi
title An autophagy-related kinase is essential for the symbiotic relationship between phaseolus vulgaris and both rhizobia and arbuscular mycorrhizal fungi
spellingShingle An autophagy-related kinase is essential for the symbiotic relationship between phaseolus vulgaris and both rhizobia and arbuscular mycorrhizal fungi
Estrada Navarrete, Georgina
Gene silencing - RNA interference/RNAi,
Plant-microbe symbiosis
Autophagy
Root development - root nodules
title_short An autophagy-related kinase is essential for the symbiotic relationship between phaseolus vulgaris and both rhizobia and arbuscular mycorrhizal fungi
title_full An autophagy-related kinase is essential for the symbiotic relationship between phaseolus vulgaris and both rhizobia and arbuscular mycorrhizal fungi
title_fullStr An autophagy-related kinase is essential for the symbiotic relationship between phaseolus vulgaris and both rhizobia and arbuscular mycorrhizal fungi
title_full_unstemmed An autophagy-related kinase is essential for the symbiotic relationship between phaseolus vulgaris and both rhizobia and arbuscular mycorrhizal fungi
title_sort An autophagy-related kinase is essential for the symbiotic relationship between phaseolus vulgaris and both rhizobia and arbuscular mycorrhizal fungi
dc.creator.none.fl_str_mv Estrada Navarrete, Georgina
Cruz Mireles, Neftaly
Lascano, Hernan Ramiro
Alvarado Affantranger, Xóchitl
Hernández Barrera, Alejandra
Barraza, Aarón
Olivares, Juan E.
Arthikala, Manoj Kumar
Cárdenas, Luis
Quinto, Carmen
Sanchez, Federico
author Estrada Navarrete, Georgina
author_facet Estrada Navarrete, Georgina
Cruz Mireles, Neftaly
Lascano, Hernan Ramiro
Alvarado Affantranger, Xóchitl
Hernández Barrera, Alejandra
Barraza, Aarón
Olivares, Juan E.
Arthikala, Manoj Kumar
Cárdenas, Luis
Quinto, Carmen
Sanchez, Federico
author_role author
author2 Cruz Mireles, Neftaly
Lascano, Hernan Ramiro
Alvarado Affantranger, Xóchitl
Hernández Barrera, Alejandra
Barraza, Aarón
Olivares, Juan E.
Arthikala, Manoj Kumar
Cárdenas, Luis
Quinto, Carmen
Sanchez, Federico
author2_role author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Gene silencing - RNA interference/RNAi,
Plant-microbe symbiosis
Autophagy
Root development - root nodules
topic Gene silencing - RNA interference/RNAi,
Plant-microbe symbiosis
Autophagy
Root development - root nodules
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Eukaryotes contain three types of lipid kinases that belong to the phosphatidylinositol 3-kinase (PI3K) family. In plants and Saccharomyces cerevisiae, only PI3K class III family members have been identified. These enzymes regulate the innate immune response, intracellular trafficking, autophagy, and senescence. Here, we report that RNAi-mediated downregulation of common bean (Phaseolus vulgaris) PI3K severely impaired symbiosis in composite P. vulgaris plants with endosymbionts such as Rhizobium tropici and Rhizophagus irregularis. Downregulation of Pv-PI3K was associated with a marked decrease in root hair growth and curling. Additionally, infection thread growth, root-nodule number, and symbiosome formation in root nodule cells were severely affected. Interestingly, root colonization by AM fungi and the formation of arbuscules were also abolished in PI3K loss-of-function plants. Furthermore, the transcript accumulation of genes encoding proteins known to interact with PI3K to form protein complexes involved in autophagy was drastically reduced in these transgenic roots. RNAimediated downregulation of one of these genes, Beclin1/Atg6, resulted in a similar phenotype as observed for transgenic roots in which Pv-PI3K had been downregulated. Our findings show that an autophagy-related process is crucial for the mutualistic interactions of P. vulgaris with beneficial microorganisms.
Fil: Estrada Navarrete, Georgina. Universidad Nacional Autónoma de México; México
Fil: Cruz Mireles, Neftaly. Universidad Nacional Autónoma de México; México
Fil: Lascano, Hernan Ramiro. Instituto Nacional de Tecnología Agropecuaria. Centro de Investigaciones Agropecuarias. Instituto de Fisiología y Recursos Genéticos Vegetales; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba; Argentina
Fil: Alvarado Affantranger, Xóchitl. Universidad Nacional Autónoma de México; México
Fil: Hernández Barrera, Alejandra. Universidad Nacional Autónoma de México; México
Fil: Barraza, Aarón. Universidad Nacional Autónoma de México; México
Fil: Olivares, Juan E.. Universidad Nacional Autónoma de México; México
Fil: Arthikala, Manoj Kumar. Universidad Nacional Autónoma de México; México
Fil: Cárdenas, Luis. Universidad Nacional Autónoma de México; México
Fil: Quinto, Carmen. Universidad Nacional Autónoma de México; México
Fil: Sanchez, Federico. Universidad Nacional Autónoma de México; México
description Eukaryotes contain three types of lipid kinases that belong to the phosphatidylinositol 3-kinase (PI3K) family. In plants and Saccharomyces cerevisiae, only PI3K class III family members have been identified. These enzymes regulate the innate immune response, intracellular trafficking, autophagy, and senescence. Here, we report that RNAi-mediated downregulation of common bean (Phaseolus vulgaris) PI3K severely impaired symbiosis in composite P. vulgaris plants with endosymbionts such as Rhizobium tropici and Rhizophagus irregularis. Downregulation of Pv-PI3K was associated with a marked decrease in root hair growth and curling. Additionally, infection thread growth, root-nodule number, and symbiosome formation in root nodule cells were severely affected. Interestingly, root colonization by AM fungi and the formation of arbuscules were also abolished in PI3K loss-of-function plants. Furthermore, the transcript accumulation of genes encoding proteins known to interact with PI3K to form protein complexes involved in autophagy was drastically reduced in these transgenic roots. RNAimediated downregulation of one of these genes, Beclin1/Atg6, resulted in a similar phenotype as observed for transgenic roots in which Pv-PI3K had been downregulated. Our findings show that an autophagy-related process is crucial for the mutualistic interactions of P. vulgaris with beneficial microorganisms.
publishDate 2016
dc.date.none.fl_str_mv 2016-09
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/161260
Estrada Navarrete, Georgina; Cruz Mireles, Neftaly; Lascano, Hernan Ramiro; Alvarado Affantranger, Xóchitl; Hernández Barrera, Alejandra; et al.; An autophagy-related kinase is essential for the symbiotic relationship between phaseolus vulgaris and both rhizobia and arbuscular mycorrhizal fungi; American Society of Plant Biologist; Plant Cell; 28; 9; 9-2016; 2326-2341
1040-4651
1532-298X
CONICET Digital
CONICET
url http://hdl.handle.net/11336/161260
identifier_str_mv Estrada Navarrete, Georgina; Cruz Mireles, Neftaly; Lascano, Hernan Ramiro; Alvarado Affantranger, Xóchitl; Hernández Barrera, Alejandra; et al.; An autophagy-related kinase is essential for the symbiotic relationship between phaseolus vulgaris and both rhizobia and arbuscular mycorrhizal fungi; American Society of Plant Biologist; Plant Cell; 28; 9; 9-2016; 2326-2341
1040-4651
1532-298X
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/plcell/article/28/9/2326/6098387
info:eu-repo/semantics/altIdentifier/doi/10.1105/tpc.15.01012
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv American Society of Plant Biologist
publisher.none.fl_str_mv American Society of Plant Biologist
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
_version_ 1842979994986348544
score 12.993085

Publicaciones similares