Effect of Rhizobium mechanisms in improving tolerance to saline stress in lettuce plants

Abstract Background Soils affected by salinity are a recurring problem that is continually increasing due to the impact of climate change on weather conditions and ineffective agricultural management practices. The use of plant growth promoting (PGP) Bacteria can alleviate its effects. In this regar...

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Main Authors: Miguel Ayuso-Calles, José David Flores-Félix, Filipa Amaro, Ignacio García-Estévez, Alejandro Jiménez-Gómez, Paula Guedes de Pinho, M. Teresa Escribano-Bailón, Raúl Rivas
Format: Article
Language:English
Published: SpringerOpen 2023-09-01
Series:Chemical and Biological Technologies in Agriculture
Subjects:
Online Access:https://doi.org/10.1186/s40538-023-00463-y
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author Miguel Ayuso-Calles
José David Flores-Félix
Filipa Amaro
Ignacio García-Estévez
Alejandro Jiménez-Gómez
Paula Guedes de Pinho
M. Teresa Escribano-Bailón
Raúl Rivas
author_facet Miguel Ayuso-Calles
José David Flores-Félix
Filipa Amaro
Ignacio García-Estévez
Alejandro Jiménez-Gómez
Paula Guedes de Pinho
M. Teresa Escribano-Bailón
Raúl Rivas
author_sort Miguel Ayuso-Calles
collection DOAJ
description Abstract Background Soils affected by salinity are a recurring problem that is continually increasing due to the impact of climate change on weather conditions and ineffective agricultural management practices. The use of plant growth promoting (PGP) Bacteria can alleviate its effects. In this regard, the genus Rhizobium has demonstrated excellent PGP capabilities through various plant growth promotion mechanisms and may therefore be a promising biofortifier under saline conditions. However, little is known about the production of volatile organic compounds (VOCs) by bacteria of this genus and their effects on plant development. Here, we aim to characterize the volatilome (the set of volatile metabolites synthesized by an organism) of Rhizobium for the first time and to further investigate the direct and VOC-mediated interaction between a strain of this genus and lettuce, a crop severely affected by salinity, both under saline and non-saline conditions. Results In this study, it was shown that the use of Rhizobium sp. GPTR29 was able to increase the production of lettuce (Lactuca sativa L.) under normal and saline conditions. We analyzed the Rhizobium volatilome under non-saline (0 mM NaCl) and saline (100 mM NaCl) conditions by HS-SPME-GC‒MS and found a differential composition in response to salinity. We detected 20 different compounds, where 3-methyl-1-butanol, 2-methyl-1-butanol, and α-pinene were the backbone of the Rhizobium volatilome. Exposure to these compounds in bicameral plates under salt stress resulted in increases in plant development of 17.1%, 16.0% and 33.1% in aerial part size, number of leaves and root length, respectively. Under greenhouse conditions and salinity, the inoculation of Rhizobium sp. GPTR29 resulted in an increase of 17.8% and 27.4% in shoot fresh and dry weight, respectively. Phenolic compounds were analyzed by HPLC–DAD-MS, revealing an increase in total flavonoid content under salinity conditions (100 mM NaCl) and apigenin derivative, luteolin 7-O-glucoside and quercetin 3-O-glucuronide individually. Conclusions These results provide new avenues for the study of PGP mechanisms in this bacterial genus, such as VOCs and their effects on plant growth, which play an important role in mediating plant–microorganism interactions. Graphical abstract
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spelling doaj.art-af5390aa26b0460b940665fe7007273e2023-11-26T12:33:22ZengSpringerOpenChemical and Biological Technologies in Agriculture2196-56412023-09-0110111910.1186/s40538-023-00463-yEffect of Rhizobium mechanisms in improving tolerance to saline stress in lettuce plantsMiguel Ayuso-Calles0José David Flores-Félix1Filipa Amaro2Ignacio García-Estévez3Alejandro Jiménez-Gómez4Paula Guedes de Pinho5M. Teresa Escribano-Bailón6Raúl Rivas7Microbiology and Genetics Department, University of SalamancaMicrobiology and Genetics Department, University of SalamancaAssociate Laboratory i4HB—Institute for Health and Bioeconomy, Laboratory of Toxicology, Department of Biological Sciences, Faculty of Pharmacy, University of PortoGrupo de Investigación en Polifenoles (GIP), Department of Analytical Chemistry, Nutrition and Bromatology, Faculty of Pharmacy, Universidad de SalamancaMicrobiology and Genetics Department, University of SalamancaAssociate Laboratory i4HB—Institute for Health and Bioeconomy, Laboratory of Toxicology, Department of Biological Sciences, Faculty of Pharmacy, University of PortoGrupo de Investigación en Polifenoles (GIP), Department of Analytical Chemistry, Nutrition and Bromatology, Faculty of Pharmacy, Universidad de SalamancaMicrobiology and Genetics Department, University of SalamancaAbstract Background Soils affected by salinity are a recurring problem that is continually increasing due to the impact of climate change on weather conditions and ineffective agricultural management practices. The use of plant growth promoting (PGP) Bacteria can alleviate its effects. In this regard, the genus Rhizobium has demonstrated excellent PGP capabilities through various plant growth promotion mechanisms and may therefore be a promising biofortifier under saline conditions. However, little is known about the production of volatile organic compounds (VOCs) by bacteria of this genus and their effects on plant development. Here, we aim to characterize the volatilome (the set of volatile metabolites synthesized by an organism) of Rhizobium for the first time and to further investigate the direct and VOC-mediated interaction between a strain of this genus and lettuce, a crop severely affected by salinity, both under saline and non-saline conditions. Results In this study, it was shown that the use of Rhizobium sp. GPTR29 was able to increase the production of lettuce (Lactuca sativa L.) under normal and saline conditions. We analyzed the Rhizobium volatilome under non-saline (0 mM NaCl) and saline (100 mM NaCl) conditions by HS-SPME-GC‒MS and found a differential composition in response to salinity. We detected 20 different compounds, where 3-methyl-1-butanol, 2-methyl-1-butanol, and α-pinene were the backbone of the Rhizobium volatilome. Exposure to these compounds in bicameral plates under salt stress resulted in increases in plant development of 17.1%, 16.0% and 33.1% in aerial part size, number of leaves and root length, respectively. Under greenhouse conditions and salinity, the inoculation of Rhizobium sp. GPTR29 resulted in an increase of 17.8% and 27.4% in shoot fresh and dry weight, respectively. Phenolic compounds were analyzed by HPLC–DAD-MS, revealing an increase in total flavonoid content under salinity conditions (100 mM NaCl) and apigenin derivative, luteolin 7-O-glucoside and quercetin 3-O-glucuronide individually. Conclusions These results provide new avenues for the study of PGP mechanisms in this bacterial genus, such as VOCs and their effects on plant growth, which play an important role in mediating plant–microorganism interactions. Graphical abstracthttps://doi.org/10.1186/s40538-023-00463-yRhizobiumLettuceSalinityVolatile organic compounds (VOCs)PhenolicsFlavonoids
spellingShingle Miguel Ayuso-Calles
José David Flores-Félix
Filipa Amaro
Ignacio García-Estévez
Alejandro Jiménez-Gómez
Paula Guedes de Pinho
M. Teresa Escribano-Bailón
Raúl Rivas
Effect of Rhizobium mechanisms in improving tolerance to saline stress in lettuce plants
Chemical and Biological Technologies in Agriculture
Rhizobium
Lettuce
Salinity
Volatile organic compounds (VOCs)
Phenolics
Flavonoids
title Effect of Rhizobium mechanisms in improving tolerance to saline stress in lettuce plants
title_full Effect of Rhizobium mechanisms in improving tolerance to saline stress in lettuce plants
title_fullStr Effect of Rhizobium mechanisms in improving tolerance to saline stress in lettuce plants
title_full_unstemmed Effect of Rhizobium mechanisms in improving tolerance to saline stress in lettuce plants
title_short Effect of Rhizobium mechanisms in improving tolerance to saline stress in lettuce plants
title_sort effect of rhizobium mechanisms in improving tolerance to saline stress in lettuce plants
topic Rhizobium
Lettuce
Salinity
Volatile organic compounds (VOCs)
Phenolics
Flavonoids
url https://doi.org/10.1186/s40538-023-00463-y
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