A multi-omics approach to unravel the interaction between heat and drought stress in the Arabidopsis thaliana holobiont

The impact of combined heat and drought stress was investigated in Arabidopsis thaliana and compared to individual stresses to reveal additive effects and interactions. A combination of plant metabolomics and root and rhizosphere bacterial metabarcoding were used to unravel effects at the plant holo...

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Main Authors: Biancamaria Senizza, Fabrizio Araniti, Simon Lewin, Sonja Wende, Steffen Kolb, Luigi Lucini
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-12-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2024.1484251/full
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author Biancamaria Senizza
Fabrizio Araniti
Simon Lewin
Sonja Wende
Steffen Kolb
Steffen Kolb
Luigi Lucini
author_facet Biancamaria Senizza
Fabrizio Araniti
Simon Lewin
Sonja Wende
Steffen Kolb
Steffen Kolb
Luigi Lucini
author_sort Biancamaria Senizza
collection DOAJ
description The impact of combined heat and drought stress was investigated in Arabidopsis thaliana and compared to individual stresses to reveal additive effects and interactions. A combination of plant metabolomics and root and rhizosphere bacterial metabarcoding were used to unravel effects at the plant holobiont level. Hierarchical cluster analysis of metabolomics signatures pointed out two main clusters, one including heat and combined heat and drought, and the second cluster that included the control and drought treatments. Overall, phenylpropanoids and nitrogen-containing compounds, hormones and amino acids showed the highest discriminant potential. A decrease in alpha-diversity of Bacteria was observed upon stress, with stress-dependent differences in bacterial microbiota composition. The shift in beta-diversity highlighted the pivotal enrichment of Proteobacteria, including Rhizobiales, Enterobacteriales and Azospirillales. The results corroborate the concept of stress interaction, where the combined heat and drought stress is not the mere combination of the single stresses. Intriguingly, multi-omics interpretations evidenced a good correlation between root metabolomics and root bacterial microbiota, indicating an orchestrated modulation of the whole holobiont.
format Article
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institution Kabale University
issn 1664-462X
language English
publishDate 2024-12-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Plant Science
spelling doaj-art-935e12ab19224bffa43aa4e4f0cacdd82024-12-19T06:24:02ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2024-12-011510.3389/fpls.2024.14842511484251A multi-omics approach to unravel the interaction between heat and drought stress in the Arabidopsis thaliana holobiontBiancamaria Senizza0Fabrizio Araniti1Simon Lewin2Sonja Wende3Steffen Kolb4Steffen Kolb5Luigi Lucini6Department for Sustainable Food Process, Università Cattolica del Sacro Cuore, Piacenza, ItalyDipartimento di Scienze Agrarie e Ambientali, Produzione, Territorio, Agroenergia (Di.S.A.A.), Università degli Studi di Milano, Milano, ItalyMicrobial Biogeochemistry, Research Area Landscape Functioning, Leibniz Center for Agricultural Landscape Research – Leibniz Center for Agricultural Landscape Research e.V. (ZALF), Muencheberg, GermanyMicrobial Biogeochemistry, Research Area Landscape Functioning, Leibniz Center for Agricultural Landscape Research – Leibniz Center for Agricultural Landscape Research e.V. (ZALF), Muencheberg, GermanyMicrobial Biogeochemistry, Research Area Landscape Functioning, Leibniz Center for Agricultural Landscape Research – Leibniz Center for Agricultural Landscape Research e.V. (ZALF), Muencheberg, GermanyThaer Institute, Faculty of Life Sciences, Humboldt University of Berlin, Berlin, GermanyDepartment for Sustainable Food Process, Università Cattolica del Sacro Cuore, Piacenza, ItalyThe impact of combined heat and drought stress was investigated in Arabidopsis thaliana and compared to individual stresses to reveal additive effects and interactions. A combination of plant metabolomics and root and rhizosphere bacterial metabarcoding were used to unravel effects at the plant holobiont level. Hierarchical cluster analysis of metabolomics signatures pointed out two main clusters, one including heat and combined heat and drought, and the second cluster that included the control and drought treatments. Overall, phenylpropanoids and nitrogen-containing compounds, hormones and amino acids showed the highest discriminant potential. A decrease in alpha-diversity of Bacteria was observed upon stress, with stress-dependent differences in bacterial microbiota composition. The shift in beta-diversity highlighted the pivotal enrichment of Proteobacteria, including Rhizobiales, Enterobacteriales and Azospirillales. The results corroborate the concept of stress interaction, where the combined heat and drought stress is not the mere combination of the single stresses. Intriguingly, multi-omics interpretations evidenced a good correlation between root metabolomics and root bacterial microbiota, indicating an orchestrated modulation of the whole holobiont.https://www.frontiersin.org/articles/10.3389/fpls.2024.1484251/fullheat stressdroughtmulti-omicsphytohormonesProteobacteriaRhizobiales
spellingShingle Biancamaria Senizza
Fabrizio Araniti
Simon Lewin
Sonja Wende
Steffen Kolb
Steffen Kolb
Luigi Lucini
A multi-omics approach to unravel the interaction between heat and drought stress in the Arabidopsis thaliana holobiont
Frontiers in Plant Science
heat stress
drought
multi-omics
phytohormones
Proteobacteria
Rhizobiales
title A multi-omics approach to unravel the interaction between heat and drought stress in the Arabidopsis thaliana holobiont
title_full A multi-omics approach to unravel the interaction between heat and drought stress in the Arabidopsis thaliana holobiont
title_fullStr A multi-omics approach to unravel the interaction between heat and drought stress in the Arabidopsis thaliana holobiont
title_full_unstemmed A multi-omics approach to unravel the interaction between heat and drought stress in the Arabidopsis thaliana holobiont
title_short A multi-omics approach to unravel the interaction between heat and drought stress in the Arabidopsis thaliana holobiont
title_sort multi omics approach to unravel the interaction between heat and drought stress in the arabidopsis thaliana holobiont
topic heat stress
drought
multi-omics
phytohormones
Proteobacteria
Rhizobiales
url https://www.frontiersin.org/articles/10.3389/fpls.2024.1484251/full
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