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

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Hilton, Sally, Picot, Emma, Schreiter, Susanne, Bass, David, Norman, Keith, Oliver, Anna E., Moore, Jonathan D., Mauchline, Tim H., Mills, Peter R., Teakle, Graham R., Clark, Ian. M., Hirsch, Penny. R., van der Gast, Christopher J. and Bending, G. D. (2021) Identification of microbial signatures linked to oilseed rape yield decline at the landscape scale. Microbiome, 9 . 19. doi:10.1186/s40168-020-00972-0

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Official URL: https://doi.org/10.1186/s40168-020-00972-0

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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.

Item Type: Journal Article
Subjects: Q Science > QK Botany
Q Science > QR Microbiology
S Agriculture > SB Plant culture
Divisions: Faculty of Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH): Rapeseed , Rape (Plant), Rape (Plant) -- Yields, Rape (Plant) -- Diseases and pests , Plant-microbe relationships, Rhizosphere
Journal or Publication Title: Microbiome
Publisher: BMC
ISSN: 2049-2618
Official Date: 22 January 2021
Dates:
DateEvent
22 January 2021Published
7 December 2020Accepted
Date of first compliant deposit: 26 November 2020
Volume: 9
Article Number: 19
DOI: 10.1186/s40168-020-00972-0
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Open Access
RIOXX Funder/Project Grant:
Project/Grant IDRIOXX Funder NameFunder ID
BB/L025892/1[BBSRC] Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
BB/L025892/1[NERC] Natural Environment Research Councilhttp://dx.doi.org/10.13039/501100000270
BB/E/C/0005196[BBSRC] Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
BBS/E/C/000IO310[BBSRC] Biotechnology and Biological Sciences Research Councilhttp://dx.doi.org/10.13039/501100000268
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