Abstract

BackgroundThe plant microbiome plays a vital role in determining host health and productivity. However, we lack real-world comparative understanding of the factors which shape assembly of its diverse biota, and crucially relationships between microbiota composition and plant health. Here we investigated landscape scale rhizosphere microbial assembly processes in oilseed rape (OSR), the UK’s third most cultivated crop by area and the world's third largest source of vegetable oil, which suffers from yield decline associated with the frequency it is grown in rotations. By including 37 conventional farmers’ fields with varying OSR rotation frequencies, we present an innovative approach to identify microbial signatures characteristic of microbiomes which are beneficial and harmful to the host.ResultsWe show that OSR yield decline is linked to rotation frequency in real-world agricultural systems. We demonstrate fundamental differences in the environmental and agronomic drivers of protist, bacterial and fungal communities between root, rhizosphere soil and bulk soil compartments. We further discovered that the assembly of fungi, but neither bacteria nor protists, was influenced by OSR rotation frequency. However, there were individual abundant bacterial OTUs that correlated with either yield or rotation frequency. A variety of fungal and protist pathogens were detected in roots and rhizosphere soil of OSR, and several increased relative abundance in root or rhizosphere compartments as OSR rotation frequency increased. Importantly, the relative abundance of the fungal pathogen Olpidium brassicae both increased with short rotations and was significantly associated with low yield. In contrast, the root endophyte Tetracladium spp. showed the reverse associations with both rotation frequency and yield to O. brassicae, suggesting that they are signatures of a microbiome which benefits the host. We also identified a variety of novel protist and fungal clades which are highly connected within the microbiome and could play a role in determining microbiome composition.ConclusionsWe show that at the landscape scale, OSR crop yield is governed by interplay between complex communities of both pathogens and beneficial biota which is modulated by rotation frequency. Our comprehensive study has identified signatures of dysbiosis within the OSR microbiome, grown in real-world agricultural systems, which could be used in strategies to promote crop yield.9LHMp6srYAP4ntBATPUdWaVideo abstract

Highlights

  • The plant microbiome plays a vital role in determining host health and productivity

  • Taxa which increased in relative abundance as the compartment shifted from bulk soil (BS) through rhizosphere (RH) soil to root (RO) were the bacterial phyla Proteobacteria (⍺) (BS = 14.4%, RH = 15.7%, RO = 23.4%), Proteobacteria (β) (BS = 4.0%, RH = 8.4%, RO = 17.1%) and Bacteroidetes (BS = 16.9%, RH = 21.0%, RO = 25.0%), the fungal classes Chytridiomycetes

  • Our study shows that the microbiomes of the three compartments, across the landscape, clustered into welldefined groups, indicating that similar communities were selected into the rhizosphere soil or root at different sampling locations, irrespective of soil and climate variation

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Summary

Introduction

The plant microbiome plays a vital role in determining host health and productivity. we lack real-world comparative understanding of the factors which shape assembly of its diverse biota, and crucially relationships between microbiota composition and plant health. We investigated landscape scale rhizosphere microbial assembly processes in oilseed rape (OSR), the UK’s third most cultivated crop by area and the world's third largest source of vegetable oil, which suffers from yield decline associated with the frequency it is grown in rotations. In most crops, including maize, wheat, soybean, sugarcane and oilseed rape, frequent cropping on the same land is associated with a decline in yield, of typically between 10 and 30%, and this may be a key contributor to the yield gap [4]. Frequent cropping may result in build-up and carry over of pathogen inoculum, and the development of multi-species pathogen complexes, which may result in a shift from a rhizosphere microbiome which benefits the host, to one which is harmful [4]

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