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

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 candidat...

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Autores principales: Frare, Romina Alejandra, Ayub, Nicolás Daniel, Alleva, Karina Edith, Soto, Gabriela Cinthia
Formato: Artículo
Lenguaje:Inglés
Publicado: Springer 2020
Materias:
Acceso en línea: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
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author Frare, Romina Alejandra
Ayub, Nicolás Daniel
Alleva, Karina Edith
Soto, Gabriela Cinthia
author_browse Alleva, Karina Edith
Ayub, Nicolás Daniel
Frare, Romina Alejandra
Soto, Gabriela Cinthia
author_facet Frare, Romina Alejandra
Ayub, Nicolás Daniel
Alleva, Karina Edith
Soto, Gabriela Cinthia
author_sort Frare, Romina Alejandra
collection INTA Digital
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.
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spelling INTA67032020-02-10T13:54:01Z The ammonium channel NOD26 is the evolutionary innovation that drives the emergence, consolidation, and dissemination of nitrogen-fixing symbiosis in angiosperms Frare, Romina Alejandra Ayub, Nicolás Daniel Alleva, Karina Edith Soto, Gabriela Cinthia Ammonium Anaerobic Treatment Symbiosis Nitrogen Fixation Angiosperms Evolution Amonio Tratamiento Anaeróbico Simbiosis Fijación del Nitrógeno Angiospermas Evolución 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 2020-02-10T13:44:08Z 2020-02-10T13:44:08Z 2018-10 info:ar-repo/semantics/artículo info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion 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 eng info:eu-repo/semantics/restrictedAccess application/pdf Springer Journal of Molecular Evolution 86 (8) : 554-565 (Octubre 2018)
spellingShingle Ammonium
Anaerobic Treatment
Symbiosis
Nitrogen Fixation
Angiosperms
Evolution
Amonio
Tratamiento Anaeróbico
Simbiosis
Fijación del Nitrógeno
Angiospermas
Evolución
Frare, Romina Alejandra
Ayub, Nicolás Daniel
Alleva, Karina Edith
Soto, Gabriela Cinthia
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
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_short The ammonium channel NOD26 is the evolutionary innovation that drives the emergence, consolidation, and dissemination of nitrogen-fixing symbiosis in angiosperms
title_sort ammonium channel nod26 is the evolutionary innovation that drives the emergence consolidation and dissemination of nitrogen fixing symbiosis in angiosperms
topic Ammonium
Anaerobic Treatment
Symbiosis
Nitrogen Fixation
Angiosperms
Evolution
Amonio
Tratamiento Anaeróbico
Simbiosis
Fijación del Nitrógeno
Angiospermas
Evolución
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
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