Multi-symbiotic systems: functional implications of the coexistence of grass-endophyte and legume-rhizobia symbioses

Autores
Garcia Parisi, Pablo Adrian; Lattanzi, Fernando Alfredo; Grimoldi, Agustin Alberto; Omacini, Marina
Año de publicación
2014
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The coexistence of symbionts with different functional roles in co-occurring plants is highly probable in terrestrial ecosystems. Analyses of how plants and microbes interact above- and belowground in multi-symbiotic systems are key to understand community structure and ecosystem functioning. We performed an outdoor experiment in mesocosms to investigate the consequences of the interaction of a provider belowground symbiont of legumes (nitrogen-fixing bacteria) and a protector aerial fungal symbiont of grasses (Epichloё endophyte) on nitrogen dynamics and aboveground net primary productivity. Four plants of Trifolium repens (Trifolium, a perennial legume) either inoculated or not with Rhizobium leguminosarum, grew surrounded by 16 plants of Lolium multiflorum (Lolium, an annual grass), with either low or high levels of the endophyte Neotyphodium occultans. After five months, we quantified the number of nodules in Trifolium roots, shoot biomass of both plant species, and the contribution of atmospheric nitrogen fixation vs. soil nitrogen uptake to above ground nitrogen in each plant species. The endophyte increased grass biomass production (+ 16%), and nitrogen uptake from the soil – the main source for the grass. Further, it reduced the nodulation of neighbour Trifolium plants (−50%). Notably, due to a compensatory increase in nitrogen fixation per nodule, this reduced neither its atmospheric nitrogen fixation – the main source of nitrogen for the legume – nor its biomass production, both of which were doubled by rhizobial inoculation. In consequence, the total amount of nitrogen in aboveground biomass and aboveground productivity were greatest in mesocosms with both symbionts (i.e. high rhizobia + high endophyte). These results show that, in spite of the deleterious effect of the endophyte on the establishment of the rhizobia–legume symbiosis, the coexistence of these symbionts, leading to additive effects on nitrogen capture and aboveground productivity, can generate complementarity on the functioning of multi-symbiotic systems.
Fil: Garcia Parisi, Pablo Adrian. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina
Fil: Lattanzi, Fernando Alfredo. Technische Universität. Lehrstuhl für Grünlandlehre; Alemania
Fil: Grimoldi, Agustin Alberto. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina
Fil: Omacini, Marina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina
Materia
Neotyphodium
Rhizobium
Symbiosis
Nitrogen Fixation
Nitrogen Dynamics
Mutualisms
Ecosystem Functioning
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:11336/4209
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/4209
network_acronym_str CONICETDig
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network_name_str CONICET Digital (CONICET)
spelling Multi-symbiotic systems: functional implications of the coexistence of grass-endophyte and legume-rhizobia symbiosesGarcia Parisi, Pablo AdrianLattanzi, Fernando AlfredoGrimoldi, Agustin AlbertoOmacini, MarinaNeotyphodiumRhizobiumSymbiosisNitrogen FixationNitrogen DynamicsMutualismsEcosystem Functioninghttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1The coexistence of symbionts with different functional roles in co-occurring plants is highly probable in terrestrial ecosystems. Analyses of how plants and microbes interact above- and belowground in multi-symbiotic systems are key to understand community structure and ecosystem functioning. We performed an outdoor experiment in mesocosms to investigate the consequences of the interaction of a provider belowground symbiont of legumes (nitrogen-fixing bacteria) and a protector aerial fungal symbiont of grasses (Epichloё endophyte) on nitrogen dynamics and aboveground net primary productivity. Four plants of Trifolium repens (Trifolium, a perennial legume) either inoculated or not with Rhizobium leguminosarum, grew surrounded by 16 plants of Lolium multiflorum (Lolium, an annual grass), with either low or high levels of the endophyte Neotyphodium occultans. After five months, we quantified the number of nodules in Trifolium roots, shoot biomass of both plant species, and the contribution of atmospheric nitrogen fixation vs. soil nitrogen uptake to above ground nitrogen in each plant species. The endophyte increased grass biomass production (+ 16%), and nitrogen uptake from the soil – the main source for the grass. Further, it reduced the nodulation of neighbour Trifolium plants (−50%). Notably, due to a compensatory increase in nitrogen fixation per nodule, this reduced neither its atmospheric nitrogen fixation – the main source of nitrogen for the legume – nor its biomass production, both of which were doubled by rhizobial inoculation. In consequence, the total amount of nitrogen in aboveground biomass and aboveground productivity were greatest in mesocosms with both symbionts (i.e. high rhizobia + high endophyte). These results show that, in spite of the deleterious effect of the endophyte on the establishment of the rhizobia–legume symbiosis, the coexistence of these symbionts, leading to additive effects on nitrogen capture and aboveground productivity, can generate complementarity on the functioning of multi-symbiotic systems.Fil: Garcia Parisi, Pablo Adrian. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Lattanzi, Fernando Alfredo. Technische Universität. Lehrstuhl für Grünlandlehre; AlemaniaFil: Grimoldi, Agustin Alberto. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Omacini, Marina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaWiley2014-10info: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/11336/4209Garcia Parisi, Pablo Adrian; Lattanzi, Fernando Alfredo; Grimoldi, Agustin Alberto; Omacini, Marina; Multi-symbiotic systems: functional implications of the coexistence of grass-endophyte and legume-rhizobia symbioses; Wiley; Oikos; 124; 5; 10-2014; 553-5600030-1299enginfo:eu-repo/semantics/altIdentifier/url/http://onlinelibrary.wiley.com/doi/10.1111/oik.01540/abstractinfo:eu-repo/semantics/altIdentifier/issn/0030-1299info:eu-repo/semantics/altIdentifier/doi/DOI:10.1111/oik.01540info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:33:26Zoai:ri.conicet.gov.ar:11336/4209instacron: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:34982025-09-29 10:33:26.612CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Multi-symbiotic systems: functional implications of the coexistence of grass-endophyte and legume-rhizobia symbioses
title Multi-symbiotic systems: functional implications of the coexistence of grass-endophyte and legume-rhizobia symbioses
spellingShingle Multi-symbiotic systems: functional implications of the coexistence of grass-endophyte and legume-rhizobia symbioses
Garcia Parisi, Pablo Adrian
Neotyphodium
Rhizobium
Symbiosis
Nitrogen Fixation
Nitrogen Dynamics
Mutualisms
Ecosystem Functioning
title_short Multi-symbiotic systems: functional implications of the coexistence of grass-endophyte and legume-rhizobia symbioses
title_full Multi-symbiotic systems: functional implications of the coexistence of grass-endophyte and legume-rhizobia symbioses
title_fullStr Multi-symbiotic systems: functional implications of the coexistence of grass-endophyte and legume-rhizobia symbioses
title_full_unstemmed Multi-symbiotic systems: functional implications of the coexistence of grass-endophyte and legume-rhizobia symbioses
title_sort Multi-symbiotic systems: functional implications of the coexistence of grass-endophyte and legume-rhizobia symbioses
dc.creator.none.fl_str_mv Garcia Parisi, Pablo Adrian
Lattanzi, Fernando Alfredo
Grimoldi, Agustin Alberto
Omacini, Marina
author Garcia Parisi, Pablo Adrian
author_facet Garcia Parisi, Pablo Adrian
Lattanzi, Fernando Alfredo
Grimoldi, Agustin Alberto
Omacini, Marina
author_role author
author2 Lattanzi, Fernando Alfredo
Grimoldi, Agustin Alberto
Omacini, Marina
author2_role author
author
author
dc.subject.none.fl_str_mv Neotyphodium
Rhizobium
Symbiosis
Nitrogen Fixation
Nitrogen Dynamics
Mutualisms
Ecosystem Functioning
topic Neotyphodium
Rhizobium
Symbiosis
Nitrogen Fixation
Nitrogen Dynamics
Mutualisms
Ecosystem Functioning
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv The coexistence of symbionts with different functional roles in co-occurring plants is highly probable in terrestrial ecosystems. Analyses of how plants and microbes interact above- and belowground in multi-symbiotic systems are key to understand community structure and ecosystem functioning. We performed an outdoor experiment in mesocosms to investigate the consequences of the interaction of a provider belowground symbiont of legumes (nitrogen-fixing bacteria) and a protector aerial fungal symbiont of grasses (Epichloё endophyte) on nitrogen dynamics and aboveground net primary productivity. Four plants of Trifolium repens (Trifolium, a perennial legume) either inoculated or not with Rhizobium leguminosarum, grew surrounded by 16 plants of Lolium multiflorum (Lolium, an annual grass), with either low or high levels of the endophyte Neotyphodium occultans. After five months, we quantified the number of nodules in Trifolium roots, shoot biomass of both plant species, and the contribution of atmospheric nitrogen fixation vs. soil nitrogen uptake to above ground nitrogen in each plant species. The endophyte increased grass biomass production (+ 16%), and nitrogen uptake from the soil – the main source for the grass. Further, it reduced the nodulation of neighbour Trifolium plants (−50%). Notably, due to a compensatory increase in nitrogen fixation per nodule, this reduced neither its atmospheric nitrogen fixation – the main source of nitrogen for the legume – nor its biomass production, both of which were doubled by rhizobial inoculation. In consequence, the total amount of nitrogen in aboveground biomass and aboveground productivity were greatest in mesocosms with both symbionts (i.e. high rhizobia + high endophyte). These results show that, in spite of the deleterious effect of the endophyte on the establishment of the rhizobia–legume symbiosis, the coexistence of these symbionts, leading to additive effects on nitrogen capture and aboveground productivity, can generate complementarity on the functioning of multi-symbiotic systems.
Fil: Garcia Parisi, Pablo Adrian. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina
Fil: Lattanzi, Fernando Alfredo. Technische Universität. Lehrstuhl für Grünlandlehre; Alemania
Fil: Grimoldi, Agustin Alberto. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina
Fil: Omacini, Marina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina
description The coexistence of symbionts with different functional roles in co-occurring plants is highly probable in terrestrial ecosystems. Analyses of how plants and microbes interact above- and belowground in multi-symbiotic systems are key to understand community structure and ecosystem functioning. We performed an outdoor experiment in mesocosms to investigate the consequences of the interaction of a provider belowground symbiont of legumes (nitrogen-fixing bacteria) and a protector aerial fungal symbiont of grasses (Epichloё endophyte) on nitrogen dynamics and aboveground net primary productivity. Four plants of Trifolium repens (Trifolium, a perennial legume) either inoculated or not with Rhizobium leguminosarum, grew surrounded by 16 plants of Lolium multiflorum (Lolium, an annual grass), with either low or high levels of the endophyte Neotyphodium occultans. After five months, we quantified the number of nodules in Trifolium roots, shoot biomass of both plant species, and the contribution of atmospheric nitrogen fixation vs. soil nitrogen uptake to above ground nitrogen in each plant species. The endophyte increased grass biomass production (+ 16%), and nitrogen uptake from the soil – the main source for the grass. Further, it reduced the nodulation of neighbour Trifolium plants (−50%). Notably, due to a compensatory increase in nitrogen fixation per nodule, this reduced neither its atmospheric nitrogen fixation – the main source of nitrogen for the legume – nor its biomass production, both of which were doubled by rhizobial inoculation. In consequence, the total amount of nitrogen in aboveground biomass and aboveground productivity were greatest in mesocosms with both symbionts (i.e. high rhizobia + high endophyte). These results show that, in spite of the deleterious effect of the endophyte on the establishment of the rhizobia–legume symbiosis, the coexistence of these symbionts, leading to additive effects on nitrogen capture and aboveground productivity, can generate complementarity on the functioning of multi-symbiotic systems.
publishDate 2014
dc.date.none.fl_str_mv 2014-10
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/11336/4209
Garcia Parisi, Pablo Adrian; Lattanzi, Fernando Alfredo; Grimoldi, Agustin Alberto; Omacini, Marina; Multi-symbiotic systems: functional implications of the coexistence of grass-endophyte and legume-rhizobia symbioses; Wiley; Oikos; 124; 5; 10-2014; 553-560
0030-1299
url http://hdl.handle.net/11336/4209
identifier_str_mv Garcia Parisi, Pablo Adrian; Lattanzi, Fernando Alfredo; Grimoldi, Agustin Alberto; Omacini, Marina; Multi-symbiotic systems: functional implications of the coexistence of grass-endophyte and legume-rhizobia symbioses; Wiley; Oikos; 124; 5; 10-2014; 553-560
0030-1299
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/http://onlinelibrary.wiley.com/doi/10.1111/oik.01540/abstract
info:eu-repo/semantics/altIdentifier/issn/0030-1299
info:eu-repo/semantics/altIdentifier/doi/DOI:10.1111/oik.01540
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 Wiley
publisher.none.fl_str_mv Wiley
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
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score 13.070432

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