Abstract

The rhizosphere, the thin layer of soil surrounding and influenced by plant roots, defines a distinct and selective microbial habitat compared to unplanted soil. The microbial communities inhabiting the rhizosphere, the rhizosphere microbiota, engage in interactions with their host plants which span from parasitism to mutualism. Therefore, the rhizosphere microbiota emerges as one of the determinants of yield potential in crops. Studies conducted with different plant species have unequivocally pointed to the host plant as a driver of the microbiota thriving at the root–soil interface. Thus far, the host genetic traits shaping the rhizosphere microbiota are not completely understood. As root hairs play a critical role in resource exchanges between plants and the rhizosphere, we hypothesized that they can act as a determinant of the microbiota thriving at the root–soil interface. To test this hypothesis, we took advantage of barley (Hordeum vulgare) mutant lines contrasting for their root hair characteristics. Plants were grown in two agricultural soils, differentiating in their organic matter contents, under controlled environmental conditions. At early stem elongation rhizosphere specimens were collected and subjected to high-resolution 16S rRNA gene profiling. Our data revealed that the barley rhizosphere microbiota is largely dominated by members of the phyla Bacteroidetes and Proteobacteria, regardless of the soil type and the root hair characteristics of the host plant. Conversely, ecological indices calculated using operational taxonomic units (OTUs) presence, abundance, and phylogeny revealed a significant impact of root hair mutations on the composition of the rhizosphere microbiota. In particular, our data indicate that mutant plants host a reduced-complexity community compared to wild-type genotypes and unplanted soil controls. Congruently, the host genotype explained up to 18% of the variation in ecological distances computed for the rhizosphere samples. Importantly, this effect is manifested in a soil-dependent manner. A closer inspection of the sequencing profiles revealed that the root hair-dependent diversification of the microbiota is supported by a taxonomically narrow group of bacteria, with a bias for members of the orders Actinomycetales, Burkholderiales, Rhizobiales, Sphingomonadales, and Xanthomonadales. Taken together, our results indicate that the presence and function of root hairs are a determinant of the bacterial community thriving in the rhizosphere and their perturbations can markedly impact on the recruitment of individual members of the microbiota.

Highlights

  • The rhizosphere, the thin layer of soil tightly adhering to plant roots and influenced by plant growth and development, represents an environment whose chemical and physical properties are markedly distinct from unplanted soil (Cardon and Gage, 2006)

  • We initially investigated the impact of soil type and the host genotype on the barley rhizosphere microbiota by inspecting the total amount of DNA recovered from our preparations

  • Despite the observed perturbations in rhizosphere formation provoked by root hair mutations (Brown et al, 2012; George et al, 2014), our data suggests that fully developed root hairs are not necessary for microbial proliferation at the barley root– soil interface (Figure 2)

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Summary

Introduction

The rhizosphere, the thin layer of soil tightly adhering to plant roots and influenced by plant growth and development, represents an environment whose chemical and physical properties are markedly distinct from unplanted soil (Cardon and Gage, 2006). The rhizosphere defines the interface between plant roots and soil and, as such, is the site of transfer of most mineral elements and water from the terrestrial to the biological sphere, with implications for biogeochemical and hydrological cycles on a global scale (White et al, 2013). In barley (Hordeum vulgare), plants capable of forming a consistent rhizosphere (i.e., exceeding 50 g soil/g roots) cope more efficiently with limitations in the availability of essential elements such as phosphorus (George et al, 2014). It has been demonstrated that individual members of the rhizosphere microbiota are capable of promoting plant performance by, predominantly, enhancing both mineral acquisition from soil (Terrazas et al, 2016) and strengthening pathogen protection (Berendsen et al, 2012). Deciphering the molecular mechanisms modulating rhizosphere formation and functioning is emerging as a key area of investigation for sustainable crop production

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