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View a Copy of This Licence, Visit Hilton et al. Microbiome (2021) 9:19 https://doi.org/10.1186/s40168-020-00972-0 RESEARCH Open Access Identification of microbial signatures linked to oilseed rape yield decline at the landscape scale Sally Hilton1* , Emma Picot1, Susanne Schreiter2, David Bass3,4, Keith Norman5, Anna E. Oliver6, Jonathan D. Moore7, Tim H. Mauchline2, Peter R. Mills8, Graham R. Teakle1, Ian M. Clark2, Penny R. Hirsch2, Christopher J. van der Gast9 and Gary D. Bending1* 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. Keywords: Oilseed rape, Microbiome, Rhizosphere, Roots, Landscape, Yield decline * Correspondence: [email protected]; [email protected] 1School of Life Sciences, The University of Warwick, Coventry CV4 7AL, UK Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Hilton et al. Microbiome (2021) 9:19 Page 2 of 15 Background community, with few comparative studies, despite evi- The world’s population is projected to be over 9 billion dence suggesting that drivers of community assembly in by 2050 and will require 60% more food [1]. Up to 80% these compartments will be different, reflecting the con- of this requirement could be met by closing the yield trasting importance of direct and indirect plant- gap of agricultural crops, which represents the difference interaction pathways [16, 18]. between the actual and achievable yield [1]. Crops may Oilseed rape (Brassica napus) is the third most culti- not reach their achievable yield due to a variety of abi- vated crop in the UK and the world's third largest source otic factors such as climate or crop management as well of vegetable oil, with 70 million tonnes produced annu- as biotic factors [2–4]. In most crops, including maize, ally worldwide [19, 20]. Field experiments have indicated wheat, soybean, sugarcane and oilseed rape, frequent that oilseed rape (OSR) yield declines proportionally cropping on the same land is associated with a decline with the frequency it is grown in rotation, and yield in yield, of typically between 10 and 30%, and this may losses of up to 25 % have been reported [21–25]. This be a key contributor to the yield gap [4]. A major factor has been associated with changes to rhizosphere bacter- implicated in yield decline is dysbiosis of the rhizosphere ial and fungal community composition, and increased microbiome. Within rotations, break crops are used to abundance of a number of putative pathogens [21, 26], disrupt the life cycles of both pathogens and deleterious but the nature of the microbial interactions which rhizosphere microbiota, reducing the amount of inocu- underlie a shift from a beneficial to a deleterious micro- lum that can accumulate within soil. Frequent cropping biome remain elusive. may result in build-up and carry over of pathogen inocu- In the current study, we used a landscape sampling ap- lum, and particularly the development of multi-species proach to link the relationship between the below- pathogen complexes, which may result in a shift from a ground OSR microbiome and plant health. OSR root, rhizosphere microbiome which benefits the host, to one rhizosphere soil and bulk soil compartments were sam- which is harmful [4]. pled from 37 commercial farms in the UK, which were Various plant, soil and environmental variables inter- chosen to include a range of OSR cropping frequencies act with agronomic factors to determine assembly of the within rotations. Comprehensive analysis of metadata rhizosphere microbiome and its effects on crop health across sites was used to identify the specific manage- [2, 3]. While management of the rhizosphere micro- ment practices, climatic variables and soil physico- biome has great practical significance for improving the chemical properties which determined assembly of each sustainability of agricultural systems, we lack a system- microbial kingdom within the compartments. We identi- atic comparative understanding of the relative import- fied root and rhizosphere specialist microbial taxa, in- ance and interactions of the varied factors which shape cluding several novel rhizosphere protist and fungal the rhizosphere microbiota, and its consequences for clades. Lastly, we characterised microbial co-occurrence crop health and yield, under real-world settings [5–8]. patterns within the root and rhizosphere compartments Importantly, despite widespread recognition of the im- and used these to identify microbial taxa which were portance of establishing causative links between plant positively or negatively associated with both OSR rota- health and the rhizosphere microbiome [9], field-based tion frequency and OSR yield, thereby identifying puta- ecological analysis of the rhizosphere microbiome re- tive microbial signatures of crop health. mains descriptive and functional interpretation of micro- biome composition is still largely based on profiling Materials and methods specific microbial taxa which have known beneficial or Sample collection detrimental impacts on plant health and nutrition, such Thirty-seven OSR field sites from 25 commercial farms as pathogens and mycorrhizal fungi [10, 11] located within the main UK OSR growing region were Eukaryotes such as fungi, and particularly protists are sampled in March 2015 (Fig. 1). Agronomic metadata largely neglected in studies of the plant microbiome [5, for each farm was collected including rotation length 12–14] despite their important contribution to plant (years since OSR was grown previously), cropping his- health and regulation of the structure and function of tory, sowing date, variety, pesticide use and the subse- microbial communities [15, 16]. Recent evidence sug- quent seed yield (Supplementary Tables 1 and 2). gests strong eukaryote-bacteria interactions within the Meteorological data for rainfall and temperature at each rhizosphere which may control community stability and field site were obtained from the UK Met-Office (www. confer host resistance to pathogens [17], emphasising metoffice.gov.uk). Soil textural analysis was determined the need for holistic
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