Domestication-driven changes in plant traits associated with changes in the assembly of the rhizosphere microbiota in tetraploid wheat
Abstract Despite the large morphological and physiological changes that plants have undergone through domestication, little is known about their impact on their microbiome. Here we characterized rhizospheric bacterial and fungal communities as well as the abundance of N-cycling microbial guilds acro...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2020-07-01
|
| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-020-69175-9 |
| _version_ | 1818342732536479744 |
|---|---|
| author | Aymé Spor Agathe Roucou Arnaud Mounier David Bru Marie-Christine Breuil Florian Fort Denis Vile Pierre Roumet Laurent Philippot Cyrille Violle |
| author_facet | Aymé Spor Agathe Roucou Arnaud Mounier David Bru Marie-Christine Breuil Florian Fort Denis Vile Pierre Roumet Laurent Philippot Cyrille Violle |
| author_sort | Aymé Spor |
| collection | DOAJ |
| description | Abstract Despite the large morphological and physiological changes that plants have undergone through domestication, little is known about their impact on their microbiome. Here we characterized rhizospheric bacterial and fungal communities as well as the abundance of N-cycling microbial guilds across thirty-nine accessions of tetraploid wheat, Triticum turgidum, from four domestication groups ranging from the wild subspecies to the semi dwarf elite cultivars. We identified several microbial phylotypes displaying significant variation in their relative abundance depending on the wheat domestication group with a stronger impact of domestication on fungi. The relative abundance of potential fungal plant pathogens belonging to the Sordariomycetes class decreased in domesticated compared to wild emmer while the opposite was found for members of the Glomeromycetes, which are obligate plant symbionts. The depletion of nitrifiers and of arbuscular mycorrhizal fungi in elite wheat cultivars compared to primitive domesticated forms suggests that the Green Revolution has decreased the coupling between plant and rhizosphere microbes that are potentially important for plant nutrient availability. Both plant diameter and fine root percentage exhibited the highest number of associations with microbial taxa, highlighting their putative role in shaping the rhizosphere microbiota during domestication. Aside from domestication, significant variation of bacterial and fungal community composition was found among accessions within each domestication group. In particular, the relative abundances of Ophiostomataceae and of Rhizobiales were strongly dependent on the host accession, with heritability estimates of ~ 27% and ~ 25%, indicating that there might be room for genetic improvement via introgression of ancestral plant rhizosphere-beneficial microbe associations. |
| first_indexed | 2024-12-13T16:19:22Z |
| format | Article |
| id | doaj.art-f345cd47ec1740b89f1807e91af10c44 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-12-13T16:19:22Z |
| publishDate | 2020-07-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-f345cd47ec1740b89f1807e91af10c442022-12-21T23:38:46ZengNature PortfolioScientific Reports2045-23222020-07-0110111210.1038/s41598-020-69175-9Domestication-driven changes in plant traits associated with changes in the assembly of the rhizosphere microbiota in tetraploid wheatAymé Spor0Agathe Roucou1Arnaud Mounier2David Bru3Marie-Christine Breuil4Florian Fort5Denis Vile6Pierre Roumet7Laurent Philippot8Cyrille Violle9Université Bourgogne Franche-Comté, INRAE, AgroSup Dijon, AgroécologieCEFE, Univ Montpellier, CNRS, EPHE, IRD, Université Paul ValéryAgroécologie, AgroSup Dijon, CNRS, INRAE, Univ. Bourgogne, Univ. Bourgogne Franche-ComtéUniversité Bourgogne Franche-Comté, INRAE, AgroSup Dijon, AgroécologieUniversité Bourgogne Franche-Comté, INRAE, AgroSup Dijon, AgroécologieCEFE, Univ Montpellier, CNRS, EPHE, Institut Agro, IRD, Université Paul ValéryLEPSE, INRAE, Institut Agro, Univ MontpellierAGAP, Univ Montpellier, CIRAD, INRAE, Institut AgroUniversité Bourgogne Franche-Comté, INRAE, AgroSup Dijon, AgroécologieCEFE, Univ Montpellier, CNRS, EPHE, IRD, Université Paul ValéryAbstract Despite the large morphological and physiological changes that plants have undergone through domestication, little is known about their impact on their microbiome. Here we characterized rhizospheric bacterial and fungal communities as well as the abundance of N-cycling microbial guilds across thirty-nine accessions of tetraploid wheat, Triticum turgidum, from four domestication groups ranging from the wild subspecies to the semi dwarf elite cultivars. We identified several microbial phylotypes displaying significant variation in their relative abundance depending on the wheat domestication group with a stronger impact of domestication on fungi. The relative abundance of potential fungal plant pathogens belonging to the Sordariomycetes class decreased in domesticated compared to wild emmer while the opposite was found for members of the Glomeromycetes, which are obligate plant symbionts. The depletion of nitrifiers and of arbuscular mycorrhizal fungi in elite wheat cultivars compared to primitive domesticated forms suggests that the Green Revolution has decreased the coupling between plant and rhizosphere microbes that are potentially important for plant nutrient availability. Both plant diameter and fine root percentage exhibited the highest number of associations with microbial taxa, highlighting their putative role in shaping the rhizosphere microbiota during domestication. Aside from domestication, significant variation of bacterial and fungal community composition was found among accessions within each domestication group. In particular, the relative abundances of Ophiostomataceae and of Rhizobiales were strongly dependent on the host accession, with heritability estimates of ~ 27% and ~ 25%, indicating that there might be room for genetic improvement via introgression of ancestral plant rhizosphere-beneficial microbe associations.https://doi.org/10.1038/s41598-020-69175-9 |
| spellingShingle | Aymé Spor Agathe Roucou Arnaud Mounier David Bru Marie-Christine Breuil Florian Fort Denis Vile Pierre Roumet Laurent Philippot Cyrille Violle Domestication-driven changes in plant traits associated with changes in the assembly of the rhizosphere microbiota in tetraploid wheat Scientific Reports |
| title | Domestication-driven changes in plant traits associated with changes in the assembly of the rhizosphere microbiota in tetraploid wheat |
| title_full | Domestication-driven changes in plant traits associated with changes in the assembly of the rhizosphere microbiota in tetraploid wheat |
| title_fullStr | Domestication-driven changes in plant traits associated with changes in the assembly of the rhizosphere microbiota in tetraploid wheat |
| title_full_unstemmed | Domestication-driven changes in plant traits associated with changes in the assembly of the rhizosphere microbiota in tetraploid wheat |
| title_short | Domestication-driven changes in plant traits associated with changes in the assembly of the rhizosphere microbiota in tetraploid wheat |
| title_sort | domestication driven changes in plant traits associated with changes in the assembly of the rhizosphere microbiota in tetraploid wheat |
| url | https://doi.org/10.1038/s41598-020-69175-9 |
| work_keys_str_mv | AT aymespor domesticationdrivenchangesinplanttraitsassociatedwithchangesintheassemblyoftherhizospheremicrobiotaintetraploidwheat AT agatheroucou domesticationdrivenchangesinplanttraitsassociatedwithchangesintheassemblyoftherhizospheremicrobiotaintetraploidwheat AT arnaudmounier domesticationdrivenchangesinplanttraitsassociatedwithchangesintheassemblyoftherhizospheremicrobiotaintetraploidwheat AT davidbru domesticationdrivenchangesinplanttraitsassociatedwithchangesintheassemblyoftherhizospheremicrobiotaintetraploidwheat AT mariechristinebreuil domesticationdrivenchangesinplanttraitsassociatedwithchangesintheassemblyoftherhizospheremicrobiotaintetraploidwheat AT florianfort domesticationdrivenchangesinplanttraitsassociatedwithchangesintheassemblyoftherhizospheremicrobiotaintetraploidwheat AT denisvile domesticationdrivenchangesinplanttraitsassociatedwithchangesintheassemblyoftherhizospheremicrobiotaintetraploidwheat AT pierreroumet domesticationdrivenchangesinplanttraitsassociatedwithchangesintheassemblyoftherhizospheremicrobiotaintetraploidwheat AT laurentphilippot domesticationdrivenchangesinplanttraitsassociatedwithchangesintheassemblyoftherhizospheremicrobiotaintetraploidwheat AT cyrilleviolle domesticationdrivenchangesinplanttraitsassociatedwithchangesintheassemblyoftherhizospheremicrobiotaintetraploidwheat |