Roots of Decline? Assembly and Function of the Rhizosphere Microbiome in Relation to Crop Yield

Lead Research Organisation: Rothamsted Research
Department Name: Sustainable Agriculture Sciences-H

Abstract

Plant roots live in close association with diverse communities of microbes, including prokaryotes such as bacteria, and eukaryotes such as fungi. These microbes are selectively recruited from the diverse communities which inhabit soil as a result of their growth on carbon exuded from roots. Root associated microbes interact with the plant in a myriad of ways; some act as symbionts which promote plant growth, while others are parasites which can have deleterious impacts on growth and development. Some control of rhizosphere microbes has been achieved in the last few decades through the use of crop genotypes resistant to specific pathogens, and via pesticides, which can reduce colonization of roots by some pathogens. However, the recruitment of detrimental biota to the rhizosphere of crop plants is responsible for global losses of many hundreds of billions of pounds annually. Strategies to robustly predict and manipulate the communities which assemble in the root zone, termed the rhizosphere, has potential to deliver great benefits to society.

Most studies of rhizosphere microbial communities have been conducted at disparate sites using techniques which do not allow robust identification of taxa present. As a result, there is a fundamental lack of understanding about how communities become recruited from the soil into the rhizosphere, particularly processes which operate on the landscape scale. Furthermore, our ability to understand how microbial communities interact with each other and with plant roots is largely limited to specific microbes which are amenable to study in the laboratory. Advances in the power of next generation sequencing (NGS) technologies provide opportunities for a paradigm shift in our ability to resolve the structure and function of rhizosphere microbial communities.

We will use the latest NGS methods to derive fundamental new understanding of the processes which shape the composition of rhizosphere communities, and unravel the interactions and functions within the community which determine their effects on plants. We will use oilseed rape (OSR) as a model system, because OSR yields suffer 6-25 % annual losses, termed yield decline, because of the development of detrimental rhizosphere biota, for which there is no treatment. Crucially, our earlier work has begun to unravel microbial shifts associated with a change from healthy to diseased OSR crops, identifying a complex of pathogens associated with yield decline.

We will elucidate the relative roles of soil biodiversity, local climate, soil properties, rotation and geographical distance in shaping the rhizosphere microbial community, and we will particularly seek to understand factors which control the enrichment of detrimental biota within the rhizosphere. We will resolve specific microbe-microbe interactions which lead to exclusion or recruitment of microbes, including pathogens.

We will use powerful metatranscriptomic methods to determine the specific genes which are expressed by plants and microbes in the rhizosphere. We will investigate these changes in rotational experiments at three field sites, so that we can understand the specific changes associated with a change from a healthy rhizosphere to one in which yield is impacted by development of an detrimental biota. Lastly we will identify the potential to manipulate recruitment of soil biota into the rhizosphere, including detrimental biota, using crop genotype and soil management.

Importantly, our work will be conducted in the field, using commercial crops of OSR, so that the results of our work will have immediate agronomic relevance. In addition to providing fundamental new understanding of rhizosphere biology, we will derive specific understanding of yield decline in OSR. This will include strategies to deliver tangible opportunities for industrial stakeholders to increase crop productivity in the short and medium term.

Technical Summary

Using established field sites across the UK, rhizosphere samples will be collected from 32 OSR cropping locations. Prokaryotic and eukaryotic microbe community composition will be determined using amplicon sequencing. Communities will be differentiated into core species which are widely distributed and locally abundant, and satellite species which are infrequent and rare. We will elucidate the role of management, environmental variables and distance as drivers of community assembly. Co-occurrence and co-exclusion relationships of rhizosphere taxa will also be determined. We will also focus on understanding those factors which determine distribution and assembly of specific taxa which our earlier work has suggested contribute to OSR yield decline. We will also determine relationships between microbiome composition and yield. Field experiments will be used to investigate changes in microbial community organisation and functioning during the transition from a healthy to a diseased state associated with yield decline. We will use 3 separate locations in order to investigate the extent to which changes in function are conserved across the landscape. Rhizosphere soil metatranscriptomes and root transcriptomes will be sequenced, and in particular, networks associated with microbial pathogenesis, and host defence and nutrition will be characterised. We will investigate the potential to manipulate the assembly of the rhizosphere microbiome through crop genotype and soil management. Four OSR genotypes which we have shown have contrasting root metabolomes will be grown in rotational field experiments and targeted amplicon sequencing used to study community assembly, including pathogens associated with yield decline. We will use a unique field resource at Rothamsted to determine scope for using soil management to influence recruitment of taxa into the root microbiome, including pathogens associated with yield decline.

Planned Impact

Plant -microbe interactions in the rhizosphere can have major impacts on crop yields, with pathogens generating global losses of billions of pound annually. In this project we provide fundamental new understanding about the factors which control the assembly of rhizosphere communities, and will use cutting edge next generation sequencing (NGS) methods to unravel the mechanisms by which plants affect, and are affected by, microbial communities. Importantly, we will use oilseed rape (OSR) as the model system for our research since it suffers from 'yield decline' arising from the development of a detrimental microbiome, which causes UK losses of £43-86 million/year. Our research will impact the following groups:

(1) The academic community, particularly those with interests in agricultural systems biology, plant-soil interactions, plant pathology and environmental microbiology. Researchers will particularly benefit from our use of NGS approaches to unravel plant-microbe-soil interactions, and from engineering the rhizosphere biota for beneficial functions. We will engage with researchers through journal papers and at key scientific conferences. The sequencing experiments are a valuable experimental resource for workers in related fields. We will open this data to other researchers for complimentary work, providing added value to the experiments.

(2) The agricultural industry, particularly stakeholders with an interest in promoting productivity and sustainability, including crop breeders, land managers and farmers. Industry will benefit from new scientific knowledge which will provide novel approaches to manage the rhizosphere: (a) we will identify microbial contributors to yield at the landscape scale, including, potentially, new pathogens, and soil and environmental characteristics which relate to pathogen distribution. This will underpin development of new crop protection strategies (eg via pesticides) (b) we will identify co-exclusion and co-occurrence relationships within the microbiome which could facilitate development of novel biocontrol approaches (c) we will identify changes in microbial function, and associated plant responses as it changes from a healthy to unhealthy state. This could lead to targeted gene and physiology based crop improvement strategies (d) we will provide soil management options to mitigate development of yield decline; this will provide tangible outputs to farmers within the project timeframe (e) we will elucidate the potential for rhizosphere microbiome engineering through crop genotype which could lead to rotational strategies, and breeding approaches, to manipulate the rhizosphere.

While providing outputs to the OSR industry (see letters of support from United Oilseeds and Elsoms) the principles of the work, and the tools we will develop, will be relevant to stakeholders across the industry (see letters of support from Agrii and Origin Fertilisers).
(3) Government (eg Defra) and industry organisations (eg NFU, HGCA) with a role in supporting and promoting the competitiveness of UK agriculture; in particular the research addresses the priorities of HGCA (see letter of support).

We will form a project steering group with industrial and government stakeholders which will advise on technology transfer. We will engage with these stakeholders through workshops at Warwick in months 24 and 42, project newsletters and the project website, which will provide a summary of project progress.

We also intend to engage strongly with the public. In addition to press releases, production of a video iCast and a project website, we plan a series of events at the Natural History Museum, London, where science derived from the project will be communicated directly to the public, including schoolchildren.

Society will benefit from trained researchers adept at multidisciplinary working, with skills in ecology, agricultural science and microbiology, and cutting edge NGS methods.

Publications

10 25 50
 
Description The Roots of Decline project has confirmed that crop yields are improved by increasing rotation length. This increase was associated with a decrease in plant pathogens. Microbial community structure was shown to be influenced by niche (roots, rhizosphere, bulk soil), treatment (rotation length), location (both locally and on the landscape scale) and abiotic factors such as pH. In addition, next generation sequencing identified specific bacteria, fungi and protists, previously unidentified microbes, potential new and known pathogens that correlated to rotation length and yield. It is hoped that correlations between high yielding cropping systems and associated microbial communities will lead to better farm management and the potential identification of plant growth promoting microbes. Comparison between metagenomic (DNA based) and metatranscriptomic (RNA) microbial methodologies showed that DNA based analysis of soil microbial populations within the crop showed evidence of the previous years crop and hence could potentially be used to determine potential plant pathogen levels in the following year. RNA based analysis showed the active microbes at the time sampling, future analysis should identify the level of plant growth promoting populations as well as the active plant pathogens.
Exploitation Route It is hoped that correlations between high yielding cropping systems and associated microbial communities will lead to better farm management and the potential identification of plant growth promoting microbes and whether it is a cohort of plant pathogens that contribute to yield decline and not just a single organism.
Sectors Agriculture, Food and Drink

 
Description Public talk for the International Year of Soil "Microbial biodiversity in agricultural soils - does it matter?", Rothamsted Research, Harpenden (July 16th 2015) Interactive public display "Journey to the centre of the earth - the first 23 cm" at the "Soil is Life" open day, Rothamsted Research, Harpenden (17 May 2015) Talk to farmers and agronomists "Can we manage the soil and root microbiome?", Laws Fertilisers Soils Seminar, Great Massingham, Norfolk (28 January 2016) Talk to farmers and agronomists at the RRA Spring meeting Managing Soil: Inputs vs Outputs - "The potential for controlling the N cycle in soil: reducing nitrous oxide emission", Rothamsted, Harpenden (3 March 2016) Interviewed by Brooke Borel for her online publication "Mental Floss" to discuss launch of the Global Soil Biodiversity Atlas (29 April 2016) Interviewed by Amanda Yorwerth from Radio Verulam for her programme "Environment Matters" (17 May 2016) Poster presentation: Life beneath your feet: the soil food web - Cereals 2016, Cambridgeshire (16 June 2016) Poster and presentation at "Science Uncovered" at the Natural History Museum, London (30 September 2016) Presentation: Yield Gap workshop, Rothamsted Research, Harpenden (19 December 2016) Presentation and interactive display: 'Roots of Decline: Oil Seed Rape Yield Decline' - Cereals 14th -15th June 2017)
First Year Of Impact 2015
Sector Agriculture, Food and Drink,Environment
Impact Types Cultural,Societal

 
Description 2nd Plant Microbiome Symposium Amsterdam 19th - 21st Feb 2018 - Roots of Decline? - Assembly and Function of the Rhizosphere Microbiome in Relation to Crop Yield 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Presented by S Schreiter, IM Clark, & PR Hirsch
Year(s) Of Engagement Activity 2018
 
Description Cereals 14th -15th June 2017 'Roots of Decline: Function of the rhizosphere microbiome' 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Industry/Business
Results and Impact Cereals is the leading technical event for the UK arable industry, attracting over 20,000 visitors. The presentation showed the importance of crop rotations in reducing yield decline, reducing the build up of below ground microbial pests and in maintaining a healthy soil.
Year(s) Of Engagement Activity 2016,2017
 
Description Festival of Ideas 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Celebration of 175th year with a Festival of Ideas. The festival brought together activities, exhibitions and demonstrations to immerse the general public in the science of feeding the world.
Year(s) Of Engagement Activity 2018
URL https://www.rothamsted.ac.uk/events/rothamsted-festival-ideas
 
Description Interactive public display at the "Soil is Life" open days 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact We updated our "Journey to the centre of the earth - the first 23 cm" interactive display for school and public open days to mark the International Year of Soils, exhibited at Rothamsted Research, Harpenden at part of the "Soil is Life" open days. New exhibits added to display included oilseed rape plants and a poster to explain the "Roots of Decline" Project
Year(s) Of Engagement Activity 2015
 
Description Invited Lecture: Rothamsted, The Long Game: classical and long-term experiments. 5th July 2017. Centre for AgriBioscience and Latrobe University, Victoria, Australia 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Professional Practitioners
Results and Impact As part of the BBSRC OCP Award 'Kenyak-yeye: UK-Australian Global Soil Meta-omic Programme' visited Centre for AgriBioscience and Latrobe University, Victoria, Australia. Station Seminar. Covered long-term experiments, yield decline and molecular approaches to N and P cycling in agricultural systems. Questions and discussions followed as similar experiments set up in Australia and interest in soil/plant and DNA archiving.
Year(s) Of Engagement Activity 2017
 
Description Invited participant in AgMicrobiomes, NSF-funded workshop held in the Asilomar conference centre in California, USA 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Study participants or study members
Results and Impact Invited to take part in AgMicrobiomes workshop in the USA, organised to discuss the best approaches for obtaining funding for microbiome research in the field of crop science
Year(s) Of Engagement Activity 2016
 
Description John Innes Center, Women of the future, talk to students about careers for women in science 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Schools
Results and Impact About 160 pupils attended the Women in Science event at the John Innes Centre. Scientists from a wide background presented their work and talked to students about the opportunities and variety of careers available.
Year(s) Of Engagement Activity 2020
 
Description MMEG 2017: 14-15th December 2017: Warwick University 'Effect of land use intensity on soil microbial functions' Aimeric Blaud 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Postgraduate students
Results and Impact Molecular microbial ecology group, annual conference. Intended for PhDs and new post-docs to show case their current and developing research areas. Ideal conference for new collaborations and exchange of ideas and methodologies.
Year(s) Of Engagement Activity 2016,2017
 
Description Poster and presentation at "Science Uncovered" at the Natural History Museum, London 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Presentation - display and posters - at the "Science Uncovered" event held at the Natural History Museum, London aimed at the general public and schoolchildren
Year(s) Of Engagement Activity 2016
 
Description Poster presentation: Cereals 2016, Cambridgeshire 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Presented a poster "Life beneath your feet: the soil food web" at Cereals 2016, the main event for those involved in arable agriculture.
Year(s) Of Engagement Activity 2016
 
Description Public talk for the International Year of Soil "Microbial biodiversity in agricultural soils - does it matter?" 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Public lecture held in the evening at Rothamsted Research to mark the International Year of Soils, aimed at a general audience drawn from the locality, well attended, many questions from audience, based on my long research experience at Rothamsted but also highlighting new work
Year(s) Of Engagement Activity 2015
 
Description School Visit (Harpenden). Diversity of life in Soil 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact Demonstrations of soil erosion, diversity and benefits of the living things in soils (microbes to mesofauna) and how germs can be spread on hands. Given to a local junior school class of 32 pupils.
Year(s) Of Engagement Activity 2020
 
Description THE FUTURE OF LONG-TERM EXPERIMENTS IN AGRICULTURAL SCIENCE 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Assessment of the importance of long term field experiments in conjunction with changing agricultural practices
Year(s) Of Engagement Activity 2018
 
Description Talk to farmers and agronomists at the RRA Spring meeting Managing Soil: Inputs vs Outputs, Rothamsted Research, Harpenden 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Professional Practitioners
Results and Impact Talk to farmers and agronomists "The potential for controlling the N cycle in soil: reducing nitrous oxide emission" at a RRA meeting in Harpenden
Year(s) Of Engagement Activity 2016
 
Description member of the HSE Scientific advisory committee on Genetic modification (contained use) 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact I have been a member of the SACGM (CU) for many years to provide my expertise on the environmental risks of accidental release of GMOs form contained conditions. My expertise is based on all my BBSRC funding over the tears.
Year(s) Of Engagement Activity Pre-2006,2006,2007,2008,2009,2010,2011,2012,2013,2014,2015,2016,2017
 
Description member of the Microbiology Society Microbiome Expert Working Group 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact An expert working group set up by the Microbiology Society which has organised a stakeholder workshop and is drawing up a document to advise government and funding agencies on the important of microbiome research
Year(s) Of Engagement Activity 2016,2017
 
Description talk to farmers and agronomists at the Laws Fertilisers Soils Seminar, Great Massingham, Norfolk 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Industry/Business
Results and Impact Gave a talk to farmers in Norfolk "Can we manage the soil and root microbiome?" and answered questions
Year(s) Of Engagement Activity 2016