The ammonium channel NOD26 is the evolutionary innovation that drives the emergence, consolidation, and dissemination of nitrogen-fixing symbiosis in angiosperms

Autores
Frare, Romina Alejandra; Ayub, Nicolás Daniel; Alleva, Karina Edith; Soto, Gabriela Cinthia
Año de publicación
2018
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Increasing evidence indicates that N-fixing symbiosis has evolved several times in the N-fixing clade of angiosperms and that this evolution is driven by a single evolutionary innovation. However, the genetics of this ancestral predisposition to N-fixing symbiosis remains unclear. A natural candidate for such molecular innovation is the ammonium channel NOD26, the main protein component of the symbiosome membrane, which facilitates the plant uptake of the nitrogen fixed by symbiotic bacteria. Here, in concordance with the emergence of N-fixing symbiosis in angiosperms but not in ancestral plants, phylogenetic analysis showed that NOD26 belongs to an angiosperm-exclusive subgroup of aquaporins. Integrated genomic, phylogenetic, and gene expression analyses supported NOD26 occurrence in the N-fixing clade, the increase in the NOD26 copy number by block and tandem duplications in legumes, and the low-copy number or even the loss of NOD26 in non-legume species of the N-fixing clade, which correlated with the possibility to lose N-fixing symbiosis in legume and non-legume lineages. Metabolic reconstructions showed that retention of NOD26 in N-fixing precursor could represent an adaptive mechanism to bypass energy crisis during anaerobic stress by ammonium detoxification. Finally, we discuss the potential use of NOD26 to transfer N-fixation to non-N-fixing crops as cereals.
Instituto de Genética
Fil: Frare, Romina Alejandra. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Ayub, Nicolás Daniel. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Alleva, Karina Edith. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Biodiversidad y Biología Experimental; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética "Ewald A. Favret"; Argentina
Fil: Soto, Gabriela Cinthia. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fuente
Journal of Molecular Evolution 86 (8) : 554-565 (Octubre 2018)
Materia
Ammonium
Anaerobic Treatment
Symbiosis
Nitrogen Fixation
Angiosperms
Evolution
Amonio
Tratamiento Anaeróbico
Simbiosis
Fijación del Nitrógeno
Angiospermas
Evolución
Nivel de accesibilidad
acceso restringido
Condiciones de uso
Repositorio
INTA Digital (INTA)
Institución
Instituto Nacional de Tecnología Agropecuaria
OAI Identificador
oai:localhost:20.500.12123/6703
Acceder
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spelling The ammonium channel NOD26 is the evolutionary innovation that drives the emergence, consolidation, and dissemination of nitrogen-fixing symbiosis in angiospermsFrare, Romina AlejandraAyub, Nicolás DanielAlleva, Karina EdithSoto, Gabriela CinthiaAmmoniumAnaerobic TreatmentSymbiosisNitrogen FixationAngiospermsEvolutionAmonioTratamiento AnaeróbicoSimbiosisFijación del NitrógenoAngiospermasEvoluciónIncreasing evidence indicates that N-fixing symbiosis has evolved several times in the N-fixing clade of angiosperms and that this evolution is driven by a single evolutionary innovation. However, the genetics of this ancestral predisposition to N-fixing symbiosis remains unclear. A natural candidate for such molecular innovation is the ammonium channel NOD26, the main protein component of the symbiosome membrane, which facilitates the plant uptake of the nitrogen fixed by symbiotic bacteria. Here, in concordance with the emergence of N-fixing symbiosis in angiosperms but not in ancestral plants, phylogenetic analysis showed that NOD26 belongs to an angiosperm-exclusive subgroup of aquaporins. Integrated genomic, phylogenetic, and gene expression analyses supported NOD26 occurrence in the N-fixing clade, the increase in the NOD26 copy number by block and tandem duplications in legumes, and the low-copy number or even the loss of NOD26 in non-legume species of the N-fixing clade, which correlated with the possibility to lose N-fixing symbiosis in legume and non-legume lineages. Metabolic reconstructions showed that retention of NOD26 in N-fixing precursor could represent an adaptive mechanism to bypass energy crisis during anaerobic stress by ammonium detoxification. Finally, we discuss the potential use of NOD26 to transfer N-fixation to non-N-fixing crops as cereals.Instituto de GenéticaFil: Frare, Romina Alejandra. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Ayub, Nicolás Daniel. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Alleva, Karina Edith. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Biodiversidad y Biología Experimental; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética "Ewald A. Favret"; ArgentinaFil: Soto, Gabriela Cinthia. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaSpringer2020-02-10T13:44:08Z2020-02-10T13:44:08Z2018-10info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfhttp://hdl.handle.net/20.500.12123/6703https://link.springer.com/article/10.1007%2Fs00239-018-9867-31432-1432https://doi.org/10.1007/s00239-018-9867-3Journal of Molecular Evolution 86 (8) : 554-565 (Octubre 2018)reponame:INTA Digital (INTA)instname:Instituto Nacional de Tecnología Agropecuariaenginfo:eu-repo/semantics/restrictedAccess2025-10-23T11:17:11Zoai:localhost:20.500.12123/6703instacron:INTAInstitucionalhttp://repositorio.inta.gob.ar/Organismo científico-tecnológicoNo correspondehttp://repositorio.inta.gob.ar/oai/requesttripaldi.nicolas@inta.gob.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:l2025-10-23 11:17:12.074INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuariafalse
dc.title.none.fl_str_mv The ammonium channel NOD26 is the evolutionary innovation that drives the emergence, consolidation, and dissemination of nitrogen-fixing symbiosis in angiosperms
title The ammonium channel NOD26 is the evolutionary innovation that drives the emergence, consolidation, and dissemination of nitrogen-fixing symbiosis in angiosperms
spellingShingle The ammonium channel NOD26 is the evolutionary innovation that drives the emergence, consolidation, and dissemination of nitrogen-fixing symbiosis in angiosperms
Frare, Romina Alejandra
Ammonium
Anaerobic Treatment
Symbiosis
Nitrogen Fixation
Angiosperms
Evolution
Amonio
Tratamiento Anaeróbico
Simbiosis
Fijación del Nitrógeno
Angiospermas
Evolución
title_short The ammonium channel NOD26 is the evolutionary innovation that drives the emergence, consolidation, and dissemination of nitrogen-fixing symbiosis in angiosperms
title_full The ammonium channel NOD26 is the evolutionary innovation that drives the emergence, consolidation, and dissemination of nitrogen-fixing symbiosis in angiosperms
title_fullStr The ammonium channel NOD26 is the evolutionary innovation that drives the emergence, consolidation, and dissemination of nitrogen-fixing symbiosis in angiosperms
title_full_unstemmed The ammonium channel NOD26 is the evolutionary innovation that drives the emergence, consolidation, and dissemination of nitrogen-fixing symbiosis in angiosperms
title_sort The ammonium channel NOD26 is the evolutionary innovation that drives the emergence, consolidation, and dissemination of nitrogen-fixing symbiosis in angiosperms
dc.creator.none.fl_str_mv Frare, Romina Alejandra
Ayub, Nicolás Daniel
Alleva, Karina Edith
Soto, Gabriela Cinthia
author Frare, Romina Alejandra
author_facet Frare, Romina Alejandra
Ayub, Nicolás Daniel
Alleva, Karina Edith
Soto, Gabriela Cinthia
author_role author
author2 Ayub, Nicolás Daniel
Alleva, Karina Edith
Soto, Gabriela Cinthia
author2_role author
author
author
dc.subject.none.fl_str_mv Ammonium
Anaerobic Treatment
Symbiosis
Nitrogen Fixation
Angiosperms
Evolution
Amonio
Tratamiento Anaeróbico
Simbiosis
Fijación del Nitrógeno
Angiospermas
Evolución
topic Ammonium
Anaerobic Treatment
Symbiosis
Nitrogen Fixation
Angiosperms
Evolution
Amonio
Tratamiento Anaeróbico
Simbiosis
Fijación del Nitrógeno
Angiospermas
Evolución
dc.description.none.fl_txt_mv Increasing evidence indicates that N-fixing symbiosis has evolved several times in the N-fixing clade of angiosperms and that this evolution is driven by a single evolutionary innovation. However, the genetics of this ancestral predisposition to N-fixing symbiosis remains unclear. A natural candidate for such molecular innovation is the ammonium channel NOD26, the main protein component of the symbiosome membrane, which facilitates the plant uptake of the nitrogen fixed by symbiotic bacteria. Here, in concordance with the emergence of N-fixing symbiosis in angiosperms but not in ancestral plants, phylogenetic analysis showed that NOD26 belongs to an angiosperm-exclusive subgroup of aquaporins. Integrated genomic, phylogenetic, and gene expression analyses supported NOD26 occurrence in the N-fixing clade, the increase in the NOD26 copy number by block and tandem duplications in legumes, and the low-copy number or even the loss of NOD26 in non-legume species of the N-fixing clade, which correlated with the possibility to lose N-fixing symbiosis in legume and non-legume lineages. Metabolic reconstructions showed that retention of NOD26 in N-fixing precursor could represent an adaptive mechanism to bypass energy crisis during anaerobic stress by ammonium detoxification. Finally, we discuss the potential use of NOD26 to transfer N-fixation to non-N-fixing crops as cereals.
Instituto de Genética
Fil: Frare, Romina Alejandra. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Ayub, Nicolás Daniel. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Alleva, Karina Edith. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Biodiversidad y Biología Experimental; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética "Ewald A. Favret"; Argentina
Fil: Soto, Gabriela Cinthia. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
description Increasing evidence indicates that N-fixing symbiosis has evolved several times in the N-fixing clade of angiosperms and that this evolution is driven by a single evolutionary innovation. However, the genetics of this ancestral predisposition to N-fixing symbiosis remains unclear. A natural candidate for such molecular innovation is the ammonium channel NOD26, the main protein component of the symbiosome membrane, which facilitates the plant uptake of the nitrogen fixed by symbiotic bacteria. Here, in concordance with the emergence of N-fixing symbiosis in angiosperms but not in ancestral plants, phylogenetic analysis showed that NOD26 belongs to an angiosperm-exclusive subgroup of aquaporins. Integrated genomic, phylogenetic, and gene expression analyses supported NOD26 occurrence in the N-fixing clade, the increase in the NOD26 copy number by block and tandem duplications in legumes, and the low-copy number or even the loss of NOD26 in non-legume species of the N-fixing clade, which correlated with the possibility to lose N-fixing symbiosis in legume and non-legume lineages. Metabolic reconstructions showed that retention of NOD26 in N-fixing precursor could represent an adaptive mechanism to bypass energy crisis during anaerobic stress by ammonium detoxification. Finally, we discuss the potential use of NOD26 to transfer N-fixation to non-N-fixing crops as cereals.
publishDate 2018
dc.date.none.fl_str_mv 2018-10
2020-02-10T13:44:08Z
2020-02-10T13:44:08Z
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/20.500.12123/6703
https://link.springer.com/article/10.1007%2Fs00239-018-9867-3
1432-1432
https://doi.org/10.1007/s00239-018-9867-3
url http://hdl.handle.net/20.500.12123/6703
https://link.springer.com/article/10.1007%2Fs00239-018-9867-3
https://doi.org/10.1007/s00239-018-9867-3
identifier_str_mv 1432-1432
dc.language.none.fl_str_mv eng
language eng
dc.rights.none.fl_str_mv info:eu-repo/semantics/restrictedAccess
eu_rights_str_mv restrictedAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Springer
publisher.none.fl_str_mv Springer
dc.source.none.fl_str_mv Journal of Molecular Evolution 86 (8) : 554-565 (Octubre 2018)
reponame:INTA Digital (INTA)
instname:Instituto Nacional de Tecnología Agropecuaria
reponame_str INTA Digital (INTA)
collection INTA Digital (INTA)
instname_str Instituto Nacional de Tecnología Agropecuaria
repository.name.fl_str_mv INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuaria
repository.mail.fl_str_mv tripaldi.nicolas@inta.gob.ar
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score 12.982451

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