Specific and conserved patterns of microbiota-structuring by maize benzoxazinoids in the field.


Journal

Microbiome
ISSN: 2049-2618
Titre abrégé: Microbiome
Pays: England
ID NLM: 101615147

Informations de publication

Date de publication:
07 05 2021
Historique:
received: 10 12 2020
accepted: 15 03 2021
entrez: 8 5 2021
pubmed: 9 5 2021
medline: 20 5 2021
Statut: epublish

Résumé

Plants influence their root and rhizosphere microbial communities through the secretion of root exudates. However, how specific classes of root exudate compounds impact the assembly of root-associated microbiotas is not well understood, especially not under realistic field conditions. Maize roots secrete benzoxazinoids (BXs), a class of indole-derived defense compounds, and thereby impact the assembly of their microbiota. Here, we investigated the broader impacts of BX exudation on root and rhizosphere microbiotas of adult maize plants grown under natural conditions at different field locations in Europe and the USA. We examined the microbiotas of BX-producing and multiple BX-defective lines in two genetic backgrounds across three soils with different properties. Our analysis showed that BX secretion affected the community composition of the rhizosphere and root microbiota, with the most pronounced effects observed for root fungi. The impact of BX exudation was at least as strong as the genetic background, suggesting that BX exudation is a key trait by which maize structures its associated microbiota. BX-producing plants were not consistently enriching microbial lineages across the three field experiments. However, BX exudation consistently depleted Flavobacteriaceae and Comamonadaceae and enriched various potential plant pathogenic fungi in the roots across the different environments. These findings reveal that BXs have a selective impact on root and rhizosphere microbiota composition across different conditions. Taken together, this study identifies the BX pathway as an interesting breeding target to manipulate plant-microbiome interactions. Video Abstract.

Sections du résumé

BACKGROUND
Plants influence their root and rhizosphere microbial communities through the secretion of root exudates. However, how specific classes of root exudate compounds impact the assembly of root-associated microbiotas is not well understood, especially not under realistic field conditions. Maize roots secrete benzoxazinoids (BXs), a class of indole-derived defense compounds, and thereby impact the assembly of their microbiota. Here, we investigated the broader impacts of BX exudation on root and rhizosphere microbiotas of adult maize plants grown under natural conditions at different field locations in Europe and the USA. We examined the microbiotas of BX-producing and multiple BX-defective lines in two genetic backgrounds across three soils with different properties.
RESULTS
Our analysis showed that BX secretion affected the community composition of the rhizosphere and root microbiota, with the most pronounced effects observed for root fungi. The impact of BX exudation was at least as strong as the genetic background, suggesting that BX exudation is a key trait by which maize structures its associated microbiota. BX-producing plants were not consistently enriching microbial lineages across the three field experiments. However, BX exudation consistently depleted Flavobacteriaceae and Comamonadaceae and enriched various potential plant pathogenic fungi in the roots across the different environments.
CONCLUSIONS
These findings reveal that BXs have a selective impact on root and rhizosphere microbiota composition across different conditions. Taken together, this study identifies the BX pathway as an interesting breeding target to manipulate plant-microbiome interactions. Video Abstract.

Identifiants

pubmed: 33962687
doi: 10.1186/s40168-021-01049-2
pii: 10.1186/s40168-021-01049-2
pmc: PMC8106187
doi:

Substances chimiques

Benzoxazines 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Video-Audio Media

Langues

eng

Sous-ensembles de citation

IM

Pagination

103

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Auteurs

Selma Cadot (S)

Division of Agroecology and Environment, Agroscope, Zurich, Switzerland.
Department of Environmental Sciences, University of Basel, Bernoullistrasse 32, 4056, Basel, Switzerland.
Institute of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland.

Hang Guan (H)

Institute of Geography, University of Bern, Bern, Switzerland.

Moritz Bigalke (M)

Institute of Geography, University of Bern, Bern, Switzerland.

Jean-Claude Walser (JC)

Genetic Diversity Centre, D-USYS, ETH Zurich, Zurich, Switzerland.

Georg Jander (G)

Boyce Thompson Institute, Ithaca, NY, USA.

Matthias Erb (M)

Institute of Plant Sciences, University of Bern, Bern, Switzerland.

Marcel G A van der Heijden (MGA)

Division of Agroecology and Environment, Agroscope, Zurich, Switzerland.
Institute of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland.
Institute of Environmental Biology, Utrecht University, Utrecht, The Netherlands.

Klaus Schlaeppi (K)

Division of Agroecology and Environment, Agroscope, Zurich, Switzerland. klaus.schlaeppi@unibas.ch.
Department of Environmental Sciences, University of Basel, Bernoullistrasse 32, 4056, Basel, Switzerland. klaus.schlaeppi@unibas.ch.
Institute of Plant Sciences, University of Bern, Bern, Switzerland. klaus.schlaeppi@unibas.ch.

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Classifications MeSH