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

Selma Cadot,Marcel G A Van Der Heijden,Moritz Bigalke,Matthias Erb,Hang Guan,Georg Jander,Klaus Schlaeppi,Jean-Claude Walser

doi:10.1186/s40168-021-01049-2

Abstract

BackgroundPlants 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.ResultsOur 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.ConclusionsThese 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.4atbM_n1-Xmh1rBaQ1rPHqVideo

Highlights

Plants influence their root and rhizosphere microbial communities through the secretion of root exudates
While the plant genotype, which defines a plant’s exudation profile, is recognized as an important factor for plant microbiota assembly, relatively little is known about specific classes of exudate compounds impacting root and rhizosphere microbiota composition
As microbiota assembly can be highly dependent on context and soil properties, we investigated the broader impacts of BX exudation on the root and rhizosphere microbiotas of 3-month-old maize plants grown under agriculturally relevant conditions at different field locations in Europe and the USA

Summary

Introduction

Plants influence their root and rhizosphere microbial communities through the secretion of root exudates. In addition to ‘soil properties’ as a main driver of plant microbiota composition, the plant genotype has a smaller impact, explaining around 5% of the variation in microbiota composition [7, 16] Plants mainly influence their root and rhizosphere microbial communities through the secretion of root exudates, which probably present the mechanistic link between host genetic variation and observed differences in microbiota composition between different genotypes [17]. While the plant genotype, which defines a plant’s exudation profile, is recognized as an important factor for plant microbiota assembly, relatively little is known about specific classes of exudate compounds impacting root and rhizosphere microbiota composition. It is unknown whether there are conserved microbiota responses to root exudation patterns across different soils. For groups with large differences in the mean sequencing depth between groups, rarefying improves the clustering of samples according to biological origin, as well as decreasing the false discovery rate in differential abundance testing

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