Metabolic regulation of the maize rhizobiome by benzoxazinoids

T E Anne Cotton,Duncan D Cameron,Moaed Al Meselmani,Roland Schwarzenbacher,Jurriaan Ton,Pierre Pétriacq,Stephen A Rolfe

doi:10.1038/s41396-019-0375-2

T E Anne Cotton, Duncan D Cameron + Show 5 more

Open Access

https://doi.org/10.1038/s41396-019-0375-2

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Abstract

The rhizobiome is an important regulator of plant growth and health. Plants shape their rhizobiome communities through production and release of primary and secondary root metabolites. Benzoxazinoids (BXs) are common tryptophan-derived secondary metabolites in grasses that regulate belowground and aboveground biotic interactions. In addition to their biocidal activity, BXs can regulate plant–biotic interactions as semiochemicals or within-plant defence signals. However, the full extent and mechanisms by which BXs shape the root-associated microbiome has remained largely unexplored. Here, we have taken a global approach to examine the regulatory activity of BXs on the maize root metabolome and associated bacterial and fungal communities. Using untargeted mass spectrometry analysis in combination with prokaryotic and fungal amplicon sequencing, we compared the impacts of three genetic mutations in different steps in the BX pathway. We show that BXs regulate global root metabolism and concurrently influence the rhizobiome in a root type-dependent manner. Correlation analysis between BX-controlled root metabolites and bacterial taxa suggested a dominant role for BX-dependent metabolites, particularly flavonoids, in constraining a range of soil microbial taxa, while stimulating methylophilic bacteria. Our study supports a multilateral model by which BXs control root–microbe interactions via a global regulatory function in root secondary metabolism.

Highlights

Supplementary information The online version of this article contains supplementary material, which is available to authorised users.The root-associated microbiome influences plant development and health
It is possible that mutations in Bx1, Bx2 and Bx6 affect a wider set of root metabolites than BXs which, in turn, could influence the composition of the rhizobiome
It has previously been reported that the BX compound DIMBOA stimulates colonisation of maize roots by the plantbeneficial bacterial strain P. putida KT2440 [19]

Summary

Present address

UMR1332 Biologie du Fruit et Pathologie/Équipe Métabolisme, INRA de Bordeaux & Université de Bordeaux, F33883 Villenave d’Ornon, France. Few studies have explored the impacts of mutations in single plant genes on root-associated microbial communities, and none of these have characterised the associated changes in metabolic root profiles, making elucidation of the underpinning mechanisms challenging [14, 24, 25, 27] Addressing this challenge requires an integrated and global approach that combines metataxonomic profiling with untargeted metabolomic analysis. Considering the variable quantities of BXs in different root types [20] and their regulatory role in plant defence [17, 18], we hypothesise that the impacts of BXs on the rhizobiome differ between root types, and are partially driven by their activity as regulatory signals of plant secondary metabolism To address these hypotheses, we have analysed the effects of bx mutations on root metabolism and root-associated bacterial and fungal rhizobiome communities of maize. Using untargeted mass spectrometry analysis in combination with rRNA gene and internal transcribed spacer (ITS) sequencing, we have compared the effects of three mutations in different steps of the BX biosynthesis pathway (bx, bx2 and bx; Fig. 1a) to establish relationships between Bx-regulated root metabolites and Bxdependent rhizosphere microbiota

Methods

Results

More common in mutant

Discussion

Compliance with ethical standards