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

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: ; 1 School 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 Background The world’s population is projected to be over 9 billion by 2050 and will require 60% more food [1]. Up to 80% of this requirement could be met by closing the yield gap of agricultural crops, which represents the difference between the actual and achievable yield [1]. Crops may not reach their achievable yield due to a variety of abiotic factors such as climate or crop management as well as biotic factors [2–4]. 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]. A major factor implicated in yield decline is dysbiosis of the rhizosphere microbiome. Within rotations, break crops are used to disrupt the life cycles of both pathogens and deleterious rhizosphere microbiota, reducing the amount of inoculum that can accumulate within soil. Frequent cropping may result in build-up and carry over of pathogen inoculum, and particularly 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]. Various plant, soil and environmental variables interact with agronomic factors to determine assembly of the rhizosphere microbiome and its effects on crop health [2, 3]. While management of the rhizosphere microbiome has great practical significance for improving the sustainability of agricultural systems, we lack a systematic comparative understanding of the relative importance and interactions of the varied factors which shape the rhizosphere microbiota, and its consequences for crop health and yield, under real-world settings [5–8]. Importantly, despite widespread recognition of the importance of establishing causative links between plant health and the rhizosphere microbiome [9], field-based ecological analysis of the rhizosphere microbiome remains descriptive and functional interpretation of microbiome composition is still largely based on profiling specific microbial taxa which have known beneficial or detrimental impacts on plant health and nutrition, such as pathogens and mycorrhizal fungi [10, 11] Eukaryotes such as fungi, and particularly protists are largely neglected in studies of the plant microbiome [5, 12–14] despite their important contribution to plant health and regulation of the structure and function of microbial communities [15, 16]. Recent evidence suggests strong eukaryote-bacteria interactions within the rhizosphere which may control community stability and confer host resistance to pathogens [17], emphasising the need for (...truncated)