Root Hair Mutations Displace the Barley Rhizosphere Microbiota

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.

A footprint of plant eco-geographic adaptation on the composition of the barley rhizosphere bacterial microbiota

“…Although these findings were gathered from the individual soil tested and further validation across a range of soil types is required, a prediction from these observations is that the host control of the rhizosphere microbiota is exerted by a limited number of loci in the genome with a relatively large effect. This is congruent with our previous observation that mono-mendelian mutations in a single root trait, root hairs, impact on ~18% of the barley rhizosphere microbiota 25 .…”

“…The distribution of reads assigned to given phyla appears distinct in plant-associated communities which are dominated in terms of abundance by members of the phyla Acidobacteria, Actinobacteria, Bacteroidetes and Proteobacteria , with these two latter phyla significantly enriched in rhizosphere samples compared to bulk soil controls. This taxonomic affiliation is consistent with previous investigations in barley in either the same 25 or in a different soil type 15 as well as in other crop plants 26 . In summary, these data indicate that the higher taxonomic ranks of the barley rhizosphere microbiota are conserved across soil types as well as wild and domesticated genotypes.…”

“…The soil was sampled from the agricultural research fields of the James Hutton Institute, Invergowrie, Scotland, UK in the Quarryfield site (56°27’5”N 3°4’29”W; Sandy Silt Loam, pH 6.2; Organic Matter 5%; Table S1). This field was left unplanted and unfertilised in the three years preceding the investigations and previously used for barley-microbiota interactions investigations 25 .…”

“…The PCR primers had incorporated an Illumina flow cell adapter at their 5’ end and the reverse primers contained 12bp unique ‘barcode’ for simultaneous sequencing of several samples 63 . PCR, including No-Template Controls (NTCs) for each barcoded primer, was performed as previously reported with the exception of the BSA at 10mg/ml concentration per reaction 25 . Only samples whose NTCs yielded an undetectable PCR amplification were retained for further analysis.…”

The bacterial community associated with adult vine weevil (Otiorhynchus sulcatus) in UK populations growing on strawberry is dominated by Candidatus Nardonella

“…Furthermore, the bacterial community was dominated by members of the Proteobacteria phylum, with remarkably high abundance of a single bacterium belonging to the γ‐proteobacteria and classified as Candidatus Nardonella. These findings are consistent with those reported previously in insect bacterial community studies, which revealed a similarly low diversity of bacterial microbiota dominated by members of the Proteobacteria phylum, compared with analogous studies on vertebrates or soil (Broderick et al., ; Fierer & Jackson, ; Vasanthakumar et al., ; Corby‐Harris et al., ; Chandler et al., ; Douglas, ; Ishak et al., ; Wong et al., ; Colman et al., ; Jones et al., ; Bansal et al., ; Yun et al., ; Gauthier et al., ; Bili et al., ; Robertson‐Albertyn et al., ). This bacterial microbiota pattern seems to be common across insect clades even when targeting different 16S rRNA gene hypervariable regions (Suzuki & Giovannoni, ; Baker et al., ; Guo et al., ; Yang et al., ) or applying different DNA extraction procedures (Martin‐Laurent et al., ).…”