Soil microorganisms buffer the reduction in plant growth and physiological performance under combined abiotic stress in the halophyte Salicornia ramosissima

The impact of multifactorial abiotic stress combinations on plant functional responses remains controversial, and general patterns of response are yet to emerge. This knowledge gap is particularly relevant for species with innate tolerance to environmental stress. Using the halophyte Salicornia ramo...

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Autores: Mateos Naranjo, Enrique, Pérez Romero, Jesús Alberto, Puglielli, Giacomo, López Jurado, Javier, Mesa Marín, Jennifer, Pajuelo Domínguez, Eloísa, Rodríguez Llorente, Ignacio David, Redondo Gómez, Susana
Tipo de recurso: artículo
Estado:Versión aceptada para publicación
Fecha de publicación:2023
País:España
Institución:Universidad de Sevilla (US)
Repositorio:idUS. Depósito de Investigación de la Universidad de Sevilla
OAI Identifier:oai:idus.us.es:11441/162501
Acceso en línea:https://hdl.handle.net/11441/162501
https://doi.org/10.1016/j.envexpbot.2023.105550
Access Level:acceso abierto
Palabra clave:CO2 enrichment
Drought
Halophyte
Functional traits
Multifactorial stress combination
Rhizomicrobiome
NaCl-stress
Temperature
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spelling Soil microorganisms buffer the reduction in plant growth and physiological performance under combined abiotic stress in the halophyte Salicornia ramosissimaMateos Naranjo, EnriquePérez Romero, Jesús AlbertoPuglielli, GiacomoLópez Jurado, JavierMesa Marín, JenniferPajuelo Domínguez, EloísaRodríguez Llorente, Ignacio DavidRedondo Gómez, SusanaCO2 enrichmentDroughtHalophyteFunctional traitsMultifactorial stress combinationRhizomicrobiomeNaCl-stressTemperatureThe impact of multifactorial abiotic stress combinations on plant functional responses remains controversial, and general patterns of response are yet to emerge. This knowledge gap is particularly relevant for species with innate tolerance to environmental stress. Using the halophyte Salicornia ramosissima as a model species, we performed a multifactorial study with 16 experimental scenarios that included or not beneficial microorganisms in order to quantify their impact on plant growth, photosynthetic performance, osmotic adjustment and ion homeostasis. The experimental scenarios were characterized by the combination of four factors with two levels (salinity: 171 and 510 mM NaCl; water stress: yes and no; temperature min/max range: 14/25 and 18/29ºC and atmospheric CO2 concentration: 400 and 700 ppm). A plant growth-promoting rhizobacteria (PGPR) consortium was used as a proxy for positive biological interaction. The results revealed that the multifactorial stress combinations triggered unique functional responses, depending on the stress factors involved. However, there was an overall more negative impact on plant functional traits under the most extreme scenario (i.e., 510 mM NaCl + water stress + high temperature). Interestingly, the presence of PGPR was able to reverse this negative influence, although this effect was negligible under non-stressful conditions. Furthermore, the positive effect of PGPR was even magnified when coexisting with elevated atmospheric CO2 concentration. This response is associated with mitigation of the negative impacts of suboptimal factor combinations on plant growth, photosynthetic performance/efficiency, and water/nutrient homeostasis. Therefore, we conclude that the positive impact of microorganisms on halophyte tolerance in complex environmental matrices would only be determinant under extreme conditions in which plant intrinsic tolerance mechanisms would not be sufficient. Remarkably, this effect could be accentuated by increasing atmospheric CO2 concentration.Ministerio de Ciencia e Innovación-AEI-FEDER PID2021-124750NB-I00, TED2021–131605B-I00, IJC2020–043331-I, PID2021–122214NA-I00ElsevierBiología Vegetal y EcologíaMicrobiologíaMinisterio de Ciencia e Innovación (MICIN). EspañaAgencia Estatal de Investigación. EspañaEuropean Commission (EC). Fondo Europeo de Desarrollo Regional (FEDER)2023info:eu-repo/semantics/articleinfo:eu-repo/semantics/acceptedVersionapplication/pdfapplication/pdfhttps://hdl.handle.net/11441/162501https://doi.org/10.1016/j.envexpbot.2023.105550reponame:idUS. Depósito de Investigación de la Universidad de Sevillainstname:Universidad de Sevilla (US)InglésEnvironmental and Experimental Botany, 217, 105550.PID2021-124750NB-I00TED2021–131605B-I00IJC2020–043331-IPID2021–122214NA-I00https://dx.doi.org/10.1016/j.envexpbot.2023.105550info:eu-repo/semantics/openAccessoai:idus.us.es:11441/1625012026-06-17T12:51:07Z
dc.title.none.fl_str_mv Soil microorganisms buffer the reduction in plant growth and physiological performance under combined abiotic stress in the halophyte Salicornia ramosissima
title Soil microorganisms buffer the reduction in plant growth and physiological performance under combined abiotic stress in the halophyte Salicornia ramosissima
spellingShingle Soil microorganisms buffer the reduction in plant growth and physiological performance under combined abiotic stress in the halophyte Salicornia ramosissima
Mateos Naranjo, Enrique
CO2 enrichment
Drought
Halophyte
Functional traits
Multifactorial stress combination
Rhizomicrobiome
NaCl-stress
Temperature
title_short Soil microorganisms buffer the reduction in plant growth and physiological performance under combined abiotic stress in the halophyte Salicornia ramosissima
title_full Soil microorganisms buffer the reduction in plant growth and physiological performance under combined abiotic stress in the halophyte Salicornia ramosissima
title_fullStr Soil microorganisms buffer the reduction in plant growth and physiological performance under combined abiotic stress in the halophyte Salicornia ramosissima
title_full_unstemmed Soil microorganisms buffer the reduction in plant growth and physiological performance under combined abiotic stress in the halophyte Salicornia ramosissima
title_sort Soil microorganisms buffer the reduction in plant growth and physiological performance under combined abiotic stress in the halophyte Salicornia ramosissima
dc.creator.none.fl_str_mv Mateos Naranjo, Enrique
Pérez Romero, Jesús Alberto
Puglielli, Giacomo
López Jurado, Javier
Mesa Marín, Jennifer
Pajuelo Domínguez, Eloísa
Rodríguez Llorente, Ignacio David
Redondo Gómez, Susana
author Mateos Naranjo, Enrique
author_facet Mateos Naranjo, Enrique
Pérez Romero, Jesús Alberto
Puglielli, Giacomo
López Jurado, Javier
Mesa Marín, Jennifer
Pajuelo Domínguez, Eloísa
Rodríguez Llorente, Ignacio David
Redondo Gómez, Susana
author_role author
author2 Pérez Romero, Jesús Alberto
Puglielli, Giacomo
López Jurado, Javier
Mesa Marín, Jennifer
Pajuelo Domínguez, Eloísa
Rodríguez Llorente, Ignacio David
Redondo Gómez, Susana
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Biología Vegetal y Ecología
Microbiología
Ministerio de Ciencia e Innovación (MICIN). España
Agencia Estatal de Investigación. España
European Commission (EC). Fondo Europeo de Desarrollo Regional (FEDER)
dc.subject.none.fl_str_mv CO2 enrichment
Drought
Halophyte
Functional traits
Multifactorial stress combination
Rhizomicrobiome
NaCl-stress
Temperature
topic CO2 enrichment
Drought
Halophyte
Functional traits
Multifactorial stress combination
Rhizomicrobiome
NaCl-stress
Temperature
description The impact of multifactorial abiotic stress combinations on plant functional responses remains controversial, and general patterns of response are yet to emerge. This knowledge gap is particularly relevant for species with innate tolerance to environmental stress. Using the halophyte Salicornia ramosissima as a model species, we performed a multifactorial study with 16 experimental scenarios that included or not beneficial microorganisms in order to quantify their impact on plant growth, photosynthetic performance, osmotic adjustment and ion homeostasis. The experimental scenarios were characterized by the combination of four factors with two levels (salinity: 171 and 510 mM NaCl; water stress: yes and no; temperature min/max range: 14/25 and 18/29ºC and atmospheric CO2 concentration: 400 and 700 ppm). A plant growth-promoting rhizobacteria (PGPR) consortium was used as a proxy for positive biological interaction. The results revealed that the multifactorial stress combinations triggered unique functional responses, depending on the stress factors involved. However, there was an overall more negative impact on plant functional traits under the most extreme scenario (i.e., 510 mM NaCl + water stress + high temperature). Interestingly, the presence of PGPR was able to reverse this negative influence, although this effect was negligible under non-stressful conditions. Furthermore, the positive effect of PGPR was even magnified when coexisting with elevated atmospheric CO2 concentration. This response is associated with mitigation of the negative impacts of suboptimal factor combinations on plant growth, photosynthetic performance/efficiency, and water/nutrient homeostasis. Therefore, we conclude that the positive impact of microorganisms on halophyte tolerance in complex environmental matrices would only be determinant under extreme conditions in which plant intrinsic tolerance mechanisms would not be sufficient. Remarkably, this effect could be accentuated by increasing atmospheric CO2 concentration.
publishDate 2023
dc.date.none.fl_str_mv 2023
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/acceptedVersion
format article
status_str acceptedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/11441/162501
https://doi.org/10.1016/j.envexpbot.2023.105550
url https://hdl.handle.net/11441/162501
https://doi.org/10.1016/j.envexpbot.2023.105550
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Environmental and Experimental Botany, 217, 105550.
PID2021-124750NB-I00
TED2021–131605B-I00
IJC2020–043331-I
PID2021–122214NA-I00
https://dx.doi.org/10.1016/j.envexpbot.2023.105550
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 Elsevier
publisher.none.fl_str_mv Elsevier
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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