Metabolomics and transcriptomics to decipher molecular mechanisms underlying ectomycorrhizal root colonization of an oak tree

Abstract Mycorrhizas are known to have a positive impact on plant growth and ability to resist major biotic and abiotic stresses. However, the metabolic alterations underlying mycorrhizal symbiosis are still understudied. By using metabolomics and transcriptomics approaches, cork oak roots colonized...

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Main Authors: M. Sebastiana, A. Gargallo-Garriga, J. Sardans, M. Pérez-Trujillo, F. Monteiro, A. Figueiredo, M. Maia, R. Nascimento, M. Sousa Silva, A. N. Ferreira, C. Cordeiro, A. P. Marques, L. Sousa, R. Malhó, J. Peñuelas
Format: Article
Language:English
Published: Nature Publishing Group 2021-04-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-87886-5
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spelling doaj-bec0ee55fdce4e6da508acd89826a24d2021-04-25T11:32:19ZengNature Publishing GroupScientific Reports2045-23222021-04-0111111610.1038/s41598-021-87886-5Metabolomics and transcriptomics to decipher molecular mechanisms underlying ectomycorrhizal root colonization of an oak treeM. Sebastiana0A. Gargallo-Garriga1J. Sardans2M. Pérez-Trujillo3F. Monteiro4A. Figueiredo5M. Maia6R. Nascimento7M. Sousa Silva8A. N. Ferreira9C. Cordeiro10A. P. Marques11L. Sousa12R. Malhó13J. Peñuelas14Plant Functional Genomics Group, BioISI – Instituto de Biosistemas e Ciências Integrativas, Faculdade de Ciências, Universidade de LisboaGlobal Change Research Institute of the Czech Academy of SciencesCREAFServei de Ressonàcia Magnètica Nuclear, Universitat Autònoma de BarcelonaCentre for Ecology, Evolution and Environmental Changes (CE3C), Faculdade de Ciências, Universidade de LisboaPlant Functional Genomics Group, BioISI – Instituto de Biosistemas e Ciências Integrativas, Faculdade de Ciências, Universidade de LisboaPlant Functional Genomics Group, BioISI – Instituto de Biosistemas e Ciências Integrativas, Faculdade de Ciências, Universidade de LisboaPlant Functional Genomics Group, BioISI – Instituto de Biosistemas e Ciências Integrativas, Faculdade de Ciências, Universidade de LisboaLaboratório de FTICR e Espectrometria de Massa Estrutural, Departamento de Química e Bioquímica, Faculdade de Ciências, Universidade de LisboaLaboratório de FTICR e Espectrometria de Massa Estrutural, Departamento de Química e Bioquímica, Faculdade de Ciências, Universidade de LisboaLaboratório de FTICR e Espectrometria de Massa Estrutural, Departamento de Química e Bioquímica, Faculdade de Ciências, Universidade de LisboaLaboratório de FTICR e Espectrometria de Massa Estrutural, Departamento de Química e Bioquímica, Faculdade de Ciências, Universidade de LisboaCEAUL - Centro de Estatística e Aplicações, Faculdade de Ciências, Universidade de LisboaPlant Functional Genomics Group, BioISI – Instituto de Biosistemas e Ciências Integrativas, Faculdade de Ciências, Universidade de LisboaCREAFAbstract Mycorrhizas are known to have a positive impact on plant growth and ability to resist major biotic and abiotic stresses. However, the metabolic alterations underlying mycorrhizal symbiosis are still understudied. By using metabolomics and transcriptomics approaches, cork oak roots colonized by the ectomycorrhizal fungus Pisolithus tinctorius were compared with non-colonized roots. Results show that compounds putatively corresponding to carbohydrates, organic acids, tannins, long-chain fatty acids and monoacylglycerols, were depleted in ectomycorrhizal cork oak colonized roots. Conversely, non-proteogenic amino acids, such as gamma-aminobutyric acid (GABA), and several putative defense-related compounds, including oxylipin-family compounds, terpenoids and B6 vitamers were induced in mycorrhizal roots. Transcriptomic analysis suggests the involvement of GABA in ectomycorrhizal symbiosis through increased synthesis and inhibition of degradation in mycorrhizal roots. Results from this global metabolomics analysis suggest decreases in root metabolites which are common components of exudates, and in compounds related to root external protective layers which could facilitate plant-fungal contact and enhance symbiosis. Root metabolic pathways involved in defense against stress were induced in ectomycorrhizal roots that could be involved in a plant mechanism to avoid uncontrolled growth of the fungal symbiont in the root apoplast. Several of the identified symbiosis-specific metabolites, such as GABA, may help to understand how ectomycorrhizal fungi such as P. tinctorius benefit their host plants.https://doi.org/10.1038/s41598-021-87886-5
collection DOAJ
language English
format Article
sources DOAJ
author M. Sebastiana
A. Gargallo-Garriga
J. Sardans
M. Pérez-Trujillo
F. Monteiro
A. Figueiredo
M. Maia
R. Nascimento
M. Sousa Silva
A. N. Ferreira
C. Cordeiro
A. P. Marques
L. Sousa
R. Malhó
J. Peñuelas
spellingShingle M. Sebastiana
A. Gargallo-Garriga
J. Sardans
M. Pérez-Trujillo
F. Monteiro
A. Figueiredo
M. Maia
R. Nascimento
M. Sousa Silva
A. N. Ferreira
C. Cordeiro
A. P. Marques
L. Sousa
R. Malhó
J. Peñuelas
Metabolomics and transcriptomics to decipher molecular mechanisms underlying ectomycorrhizal root colonization of an oak tree
Scientific Reports
author_facet M. Sebastiana
A. Gargallo-Garriga
J. Sardans
M. Pérez-Trujillo
F. Monteiro
A. Figueiredo
M. Maia
R. Nascimento
M. Sousa Silva
A. N. Ferreira
C. Cordeiro
A. P. Marques
L. Sousa
R. Malhó
J. Peñuelas
author_sort M. Sebastiana
title Metabolomics and transcriptomics to decipher molecular mechanisms underlying ectomycorrhizal root colonization of an oak tree
title_short Metabolomics and transcriptomics to decipher molecular mechanisms underlying ectomycorrhizal root colonization of an oak tree
title_full Metabolomics and transcriptomics to decipher molecular mechanisms underlying ectomycorrhizal root colonization of an oak tree
title_fullStr Metabolomics and transcriptomics to decipher molecular mechanisms underlying ectomycorrhizal root colonization of an oak tree
title_full_unstemmed Metabolomics and transcriptomics to decipher molecular mechanisms underlying ectomycorrhizal root colonization of an oak tree
title_sort metabolomics and transcriptomics to decipher molecular mechanisms underlying ectomycorrhizal root colonization of an oak tree
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2021-04-01
description Abstract Mycorrhizas are known to have a positive impact on plant growth and ability to resist major biotic and abiotic stresses. However, the metabolic alterations underlying mycorrhizal symbiosis are still understudied. By using metabolomics and transcriptomics approaches, cork oak roots colonized by the ectomycorrhizal fungus Pisolithus tinctorius were compared with non-colonized roots. Results show that compounds putatively corresponding to carbohydrates, organic acids, tannins, long-chain fatty acids and monoacylglycerols, were depleted in ectomycorrhizal cork oak colonized roots. Conversely, non-proteogenic amino acids, such as gamma-aminobutyric acid (GABA), and several putative defense-related compounds, including oxylipin-family compounds, terpenoids and B6 vitamers were induced in mycorrhizal roots. Transcriptomic analysis suggests the involvement of GABA in ectomycorrhizal symbiosis through increased synthesis and inhibition of degradation in mycorrhizal roots. Results from this global metabolomics analysis suggest decreases in root metabolites which are common components of exudates, and in compounds related to root external protective layers which could facilitate plant-fungal contact and enhance symbiosis. Root metabolic pathways involved in defense against stress were induced in ectomycorrhizal roots that could be involved in a plant mechanism to avoid uncontrolled growth of the fungal symbiont in the root apoplast. Several of the identified symbiosis-specific metabolites, such as GABA, may help to understand how ectomycorrhizal fungi such as P. tinctorius benefit their host plants.
url https://doi.org/10.1038/s41598-021-87886-5
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