Bioactive diterpenoids impact the composition of the root-associated microbiome in maize (Zea mays)

Abstract Plants deploy both primary and species-specific, specialized metabolites to communicate with other organisms and adapt to environmental challenges, including interactions with soil-dwelling microbial communities. However, the role of specialized metabolites in modulating plant-microbiome in...

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Main Authors: Katherine M. Murphy, Joseph Edwards, Katherine B. Louie, Benjamin P. Bowen, Venkatesan Sundaresan, Trent R. Northen, Philipp Zerbe
Format: Article
Language:English
Published: Nature Publishing Group 2021-01-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-020-79320-z
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spelling doaj-1c1dd7d553454d948130e0814ea466032021-01-17T12:40:18ZengNature Publishing GroupScientific Reports2045-23222021-01-0111111310.1038/s41598-020-79320-zBioactive diterpenoids impact the composition of the root-associated microbiome in maize (Zea mays)Katherine M. Murphy0Joseph Edwards1Katherine B. Louie2Benjamin P. Bowen3Venkatesan Sundaresan4Trent R. Northen5Philipp Zerbe6Department of Plant Biology, University of California-DavisIntegrative Biology, University of Texas, AustinJoint Genome Institute, Lawrence Berkeley National LaboratoryEnvironmental Genomics and Systems Biology, Lawrence Berkeley National LaboratoryDepartment of Plant Biology, University of California-DavisEnvironmental Genomics and Systems Biology, Lawrence Berkeley National LaboratoryDepartment of Plant Biology, University of California-DavisAbstract Plants deploy both primary and species-specific, specialized metabolites to communicate with other organisms and adapt to environmental challenges, including interactions with soil-dwelling microbial communities. However, the role of specialized metabolites in modulating plant-microbiome interactions often remains elusive. In this study, we report that maize (Zea mays) diterpenoid metabolites with known antifungal bioactivities also influence rhizosphere bacterial communities. Metabolite profiling showed that dolabralexins, antibiotic diterpenoids that are highly abundant in roots of some maize varieties, can be exuded from the roots. Comparative 16S rRNA gene sequencing determined the bacterial community composition of the maize mutant Zman2 (anther ear 2), which is deficient in dolabralexins and closely related bioactive kauralexin diterpenoids. The Zman2 rhizosphere microbiome differed significantly from the wild-type sibling with the most significant changes observed for Alphaproteobacteria of the order Sphingomonadales. Metabolomics analyses support that these differences are attributed to the diterpenoid deficiency of the Zman2 mutant, rather than other large-scale metabolome alterations. Together, these findings support physiological functions of maize diterpenoids beyond known chemical defenses, including the assembly of the rhizosphere microbiome.https://doi.org/10.1038/s41598-020-79320-z
collection DOAJ
language English
format Article
sources DOAJ
author Katherine M. Murphy
Joseph Edwards
Katherine B. Louie
Benjamin P. Bowen
Venkatesan Sundaresan
Trent R. Northen
Philipp Zerbe
spellingShingle Katherine M. Murphy
Joseph Edwards
Katherine B. Louie
Benjamin P. Bowen
Venkatesan Sundaresan
Trent R. Northen
Philipp Zerbe
Bioactive diterpenoids impact the composition of the root-associated microbiome in maize (Zea mays)
Scientific Reports
author_facet Katherine M. Murphy
Joseph Edwards
Katherine B. Louie
Benjamin P. Bowen
Venkatesan Sundaresan
Trent R. Northen
Philipp Zerbe
author_sort Katherine M. Murphy
title Bioactive diterpenoids impact the composition of the root-associated microbiome in maize (Zea mays)
title_short Bioactive diterpenoids impact the composition of the root-associated microbiome in maize (Zea mays)
title_full Bioactive diterpenoids impact the composition of the root-associated microbiome in maize (Zea mays)
title_fullStr Bioactive diterpenoids impact the composition of the root-associated microbiome in maize (Zea mays)
title_full_unstemmed Bioactive diterpenoids impact the composition of the root-associated microbiome in maize (Zea mays)
title_sort bioactive diterpenoids impact the composition of the root-associated microbiome in maize (zea mays)
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2021-01-01
description Abstract Plants deploy both primary and species-specific, specialized metabolites to communicate with other organisms and adapt to environmental challenges, including interactions with soil-dwelling microbial communities. However, the role of specialized metabolites in modulating plant-microbiome interactions often remains elusive. In this study, we report that maize (Zea mays) diterpenoid metabolites with known antifungal bioactivities also influence rhizosphere bacterial communities. Metabolite profiling showed that dolabralexins, antibiotic diterpenoids that are highly abundant in roots of some maize varieties, can be exuded from the roots. Comparative 16S rRNA gene sequencing determined the bacterial community composition of the maize mutant Zman2 (anther ear 2), which is deficient in dolabralexins and closely related bioactive kauralexin diterpenoids. The Zman2 rhizosphere microbiome differed significantly from the wild-type sibling with the most significant changes observed for Alphaproteobacteria of the order Sphingomonadales. Metabolomics analyses support that these differences are attributed to the diterpenoid deficiency of the Zman2 mutant, rather than other large-scale metabolome alterations. Together, these findings support physiological functions of maize diterpenoids beyond known chemical defenses, including the assembly of the rhizosphere microbiome.
url https://doi.org/10.1038/s41598-020-79320-z
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