Identification of microbial signatures linked to oilseed rape yield decline at the landscape scale

Abstract

Background The 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. Results We 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. Conclusions We 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.

Contrasting Responses of Rhizosphere Bacterial, Fungal, Protist, and Nematode Communities to Nitrogen Fertilization and Crop Genotype in Field Grown Oilseed Rape (Brassica napus)

“…Tetracladium spp. have traditionally been considered as aquatic hyphomycetes, but evidence is emerging, supported here, that they are widely distributed root endophytes (Selosse et al, 2008) which may be indicators of a beneficial microbiome (Hilton et al, 2021). While there is no understanding of the interactions between these fungi with their host or plant pathogens, some related Heliotales may act as root symbionts which promote plant growth and nutrient supply (Almario et al, 2017).…”

“…Notably, nitrogen fertilization was associated with increases in relative abundance of a number of pathogens in the rhizosphere of OSR. This included Leptosphaeria maculans and L. biglobosa, which cause blackleg diseases which impact OSR yields globally (Fitt et al, 2006), Pyrenopeziza brassicae, responsible for light leaf spot, the predominant OSR disease in the UK (Dewage et al, 2018), Olpidium brassicae, which is associated with OSR yield decline (Hilton et al, 2013(Hilton et al, , 2021, and Mycosphaerella sp. which are common plant pathogens and includes several species which infect oilseed rape, such as M. brassicola (ringspot disease) and M. capsellae (white leaf spot disease).…”

“…To investigate shifts in community connectivity due to the altered nitrogen inputs, inter-kingdom network analysis (Hilton et al, 2021) was performed using the top quartile of most abundant bacterial, protist, nematode and fungal OTUs. Correlations were calculated using the Sparse Correlations for Compositional data algorithm (SparCC), and p-values calculated using 1000 bootstraps (Friedman and Alm, 2012).…”

“…Plants secrete up to 20% of the carbon they fix into the soil as exudates, particularly in the form of sugars and organic acids, and this drives the selective growth of microbes in the soil immediately adjacent to roots, and the recruitment of microbes onto the root surface and within the root itself (Morgan et al, 2005). The microbiota residing in roots and the soil surrounding the roots constitutes the rhizosphere microbiome, which can influence the plant through diverse direct and indirect interaction pathways (Hunter et al, 2014;Hilton et al, 2021).…”

“…Additionally, free-living rhizosphere microbes can indirectly exert beneficial and detrimental impacts on the plant, e.g., by stimulating or suppressing the growth of pathogens and symbionts, and through nutrient mobilization-immobilization processes (Morgan et al, 2005). There is considerable interest in understanding rhizosphere microbiome assembly processes in order to unravel what constitutes a microbiome which benefits the host, and the contributors to microbiome dysbiosis, which results in harm to the host (Tabrett and Horton, 2020;Hilton et al, 2021).…”