Role of the SYM pathway in selecting the root microbiota
Lead Research Organisation:
University of Oxford
Department Name: Biology
Abstract
Plant roots are critical for the uptake of mineral nutrients by plants. In addition, they interact with the soil environment and a complex assemblage of bacteria, fungi, single celled animal cells, nematodes and other organisms. The area directly around roots that is occupied by these organisms is known as the rhizosphere and the collective name for the organisms is the rhizosphere microbiota. Microorganisms also reside inside plant roots, usually between plant cells and are knows as endophytes. Together the rhizosphere and endosphere microbiotas makes up the root microbiota of a plant. It has been shown over the last few years that the root microbiota is critical for the health and growth of plants, with many microorganisms shown to be plant growth promoting. Bacteria are simple single celled microorganisms that lack the membrane bound structures found in higher cells of plants and animals. However, while bacteria may have a less complex cellular organisation they carry out a huge range of chemical reactions not found in plants and animals. Bacteria are responsible for the cycling of many nutrients such as N2 (N2 is also known as nitrogen gas and consists of two nitrogen atoms bound by a strong triple bond), which is a very inert atmospheric gas. N2 makes up 78% of the atmosphere but is very unreactive and cannot be used directly as a source of nitrogen, which is needed for amino acid, protein and DNA synthesis. However, a small number of bacteria can reduce (add hydrogen) to N2 and convert it into ammonia (NH3), which is readily incorporated into amino acids and then all the other building blocks of life, by a wide range of organisms including bacteria and plants. In many parts of the world the limitation to growth of plants, which in turn support animal life, is the supply of nitrogen as ammonia or nitrate. In the past, much of the nitrogen was provided by biological nitrogen fixation, particularly by a group of plants known as legumes. The legumes form nodules on their roots which house bacteria, called rhizobia, which reduce N2 to ammonia and supply it to plants in return for a carbon and energy source. However, more recently legume use has declined and nitrogen is mainly provided to crops by chemically synthesised fertiliser. One of the other limiting nutrients in the biosphere is phosphate, which is often naturally provided to the plant by a group of fungi known as the arbuscular mycorrhizae (AM fungi). Nitrogen and phosphate are so crucial to plant growth and crop yield that they are often both added in very large amounts to agricultural soils. This has led to widespread pollution of ground water with these nutrients, leading to run off into water ways and oceans that causes eutrophication where the growth in particular of algae is promoted. Remarkably it turns out that both AM fungi and rhizobia interact with plants using a common signalling network known as the common symbiosis pathway (SYM). In this work, we are investigating how the SYM pathway controls the microbiota of legumes and cereals. Our aim is to understand how the pathways control different members of the microbiota. In addition, we will move beyond simple characterisation of the components of the microbiota to examine the mechanism of control. This research will lead to a step change in characterisation of the plant microbiota of agriculturally critical crops, including pea and rice. Not only will we characterise which microorganisms are present but we will also culture and characterize the function of key members of the microbiota. This work moves beyond simple characterisation of which microorganisms are present to identification of functional community members.
Technical Summary
The best-characterised and probably most important plant microbe interactions are between legumes and Rhizobium, leading to nodulation, and between most land plants and arbuscular mycorrhizae (AM). These symbioses are critical drivers of plant productivity and agricultural yield. N2-fixation by rhizobia in association with crop legumes provides up to 22 Tg of nitrogen a year (15), while around 80% of land plants are infected by mycorrhizal fungi, which make a substantial contribution to plant nutrition particularly of phosphate but also nitrogen and water among others . A common SYM pathway controls both nodulation of legumes and mycorrhization of most land plants. This suggests that legume nodulation, which evolved approximately 60 Million Years Ago, adapted to use the more ancient AM symbiosis (~400 MYA) pathway. In this study, we will use Medicago truncatula as our main test plant to examine the impact of the SYM pathway on the root microbiota. Results in M. truncatula will then be compared to pea SYM mutants defective in either nodulation or nodulation and mycorrhization and rice mutants defective in mycorrhization. This work will then be followed by the isolation of bacteria for combination into Synthetic Communities (SynComs), to bridge the hitherto insuperable barrier between community analysis and molecular understanding. The role of the SYM pathway in controlling bacterial chemotaxis, adhesion, colonisation and tissue localisation will be determined. Metabolite secretion from roots of wildtype and SYM mutant lines will be compared to determine if altered secretion profiles directly control the microbiota. This will pave the way for future work on transcriptomics and genetic analysis to pinpoint the bacterial factors controlling interaction with roots and survival in complex root communities.
Planned Impact
Within this proposal, we will extend established work within our groups to develop a selection platform for the isolation and manipulation of members of the root microbiota. In particular, we will gain deep insight into how the common SYM pathway controls the root microbiota. This is particularly important to nitrogen and phosphate utilisation, but also has relevance to disease resistance and herbicide and pesticide use. In the bigger context nitrogen is at double its preindustrial level and now beyond the safe operating boundary of the earth, with widespread pollution of groundwater and ocean coastal zones by nitrates and phosphates leading to eutrophication and costal dead zones. These nutrients are leading players in the perfect storm, demanding increased agricultural production but requiring changes in agricultural practice to avoid environmental carnage. In addition, we will develop a synthetic community of bacteria (SynCom) that is a powerful resource to help tackle these issues and therefore has over-arching relevance to society and government policy. Furthermore, in a regulatory environment where less fertilizer and pesticide use are becoming mandatory, this work will offer tangible results to help meet these targets and assist the competitiveness of UK industry. We will maximize the potential impact of our research by directly engaging with a range of stakeholders, including crop breeders, policymakers and farmers via our existing knowledge transfer networks, including the UK Wheat Genetic Improvement Network (WGIN), landowner/farmers groups (e.g. NFU, SNFU, NFUW, HCC, Growers association, Soil Association), academic societies (BES, BSSS), conservation bodies and local/national government departments (Defra; EA), agencies (SEPA; Natural England; Natural Resources Wales, SNH), who will directly benefit from our findings and the formation of robust SynComs. Reducing inputs into agriculture while maintaining yields has direct benefits to British farming but also to maintenance of the countryside and its use and recreation by the British public. It will help the UK meet local and European environmental targets and help the long-term sustainability and stability of our environment. We will also be training the next generation of scientists to develop practical solutions to environmental problems and develop a whole raft of new microbial inoculants.
Organisations
Publications
Tkacz A
(2022)
Nodulation and nitrogen fixation in Medicago truncatula strongly alters the abundance of its root microbiota and subtly affects its structure
in Environmental Microbiology
Ledermann R
(2021)
How Rhizobia Adapt to the Nodule Environment.
in Journal of bacteriology
Crang N
(2021)
Role and Regulation of Poly-3-Hydroxybutyrate in Nitrogen Fixation in Azorhizobium caulinodans.
in Molecular plant-microbe interactions : MPMI
Schulte CCM
(2022)
Genome-Scale Metabolic Modelling of Lifestyle Changes in Rhizobium leguminosarum.
in mSystems
Schulte Carolin C. M.
(2022)
Genome-Scale Metabolic Modelling of Lifestyle Changes in
Rhizobium leguminosarum
in MSYSTEMS
Tkacz A
(2020)
The plant microbiome: The dark and dirty secrets of plant growth
in PLANTS, PEOPLE, PLANET
Jiang S
(2021)
NIN-like protein transcription factors regulate leghemoglobin genes in legume nodules.
in Science (New York, N.Y.)
Haskett TL
(2021)
Engineering rhizobacteria for sustainable agriculture.
in The ISME journal
Description | Legumes, such as Medicago, form symbiosis with bacteria (providing nitrogen) and fungi (providing phosphorus), two essential macronutrients for plant growth. We have shown that in Medicago symbiotic mutants which are unable to form an effective symbiotic relationship with nitrogen-fixing bacteria and AM fungi, there are effects on the general soil microbiota which these plants support. Effects on the colonisation of plant roots can be seen in both the community structure and also in the abundance of micro-organisms. Symbiotically impaired plants, if grown without these essential nutrients (N and P), do not support their microbial community. |
Exploitation Route | We are preparing a high impact publication describing the findings. Unfortunately due to Covid we were unable to present these results at any conference (i.e. European N2-fixing conference in Naples has been postponed to 2023). We have had an exchange student (Anna Martyn) who was involved in this study and this student now pursues PhD with our long-standing collaborators in legume N2 fixation in Aarhus, Denmark. |
Sectors | Agriculture, Food and Drink,Environment |
Description | Continuation of ENSA (RL) |
Amount | $226,932 (USD) |
Organisation | Foreign Commonwealth and Development Office (FCDO) |
Sector | Public |
Country | United Kingdom |
Start | 01/2021 |
End | 03/2024 |
Description | Factors controlling N2-fixing ability and competitiveness of rhizobia to nodulate legumes |
Amount | £784,606 (GBP) |
Funding ID | BB/W006219/1 |
Organisation | Biotechnology and Biological Sciences Research Council (BBSRC) |
Sector | Public |
Country | United Kingdom |
Start | 02/2022 |
End | 01/2025 |
Description | Marie Curie (IA) |
Amount | € 224,933 (EUR) |
Organisation | Marie Curie |
Sector | Charity/Non Profit |
Country | United Kingdom |
Start | 06/2021 |
End | 06/2023 |
Description | 21st Congress on Nitrogen Fixation - 10th-15th Oct 2019, Wuhan, China - Philip Poole |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Professional Practitioners |
Results and Impact | Phil gave a talk at this international conference. He had many questions on his work and spent time exchanging ideas with colleagues in this research area. |
Year(s) Of Engagement Activity | 2019 |
URL | http://2019icnf.csp.escience.cn/dct/page/65580 |
Description | 5th Annual Missouri University Plant Research Symposium |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Professional Practitioners |
Results and Impact | Phil gave a talk entitled 'Improving legume symbiosis or engineering cereals' in this virtual symposium: The Next Green Revolution: Challenges and Strategies towards a Sustainable Agriculture. |
Year(s) Of Engagement Activity | 2021 |
URL | https://www.corteva.com/our-impact/innovation/symposiaseries.html |
Description | Australian Nitrogen Fixation Conference (ANFC-2022), Dec 2022 (BJ, RL, HK, TH) |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Professional Practitioners |
Results and Impact | Talks were presented at this international meeting. Student talk prize was presented to TU. |
Year(s) Of Engagement Activity | 2022 |
URL | https://rhizosphere.org/lab-news-current/ |
Description | Centre of Excellence for Plant and Microbial Science (CEPAMS), Shanghai, China - Philip Poole (Oct 2019) |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Professional Practitioners |
Results and Impact | Phil visited Dr Jeremy Murray at CEPAMS and gave a talk to scientists and students. |
Year(s) Of Engagement Activity | 2019 |
URL | https://rhizosphere.org/lab-news/ |
Description | Development of Poole Lab website (Rhizosphere.org) |
Form Of Engagement Activity | Engagement focused website, blog or social media channel |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Public/other audiences |
Results and Impact | The Rhizosphere website is used to describe work performed, profiles lab members, lists outreach activities and celebrates achievements. Also includes a list of Lab publications. |
Year(s) Of Engagement Activity | 2014,2015,2016,2017,2018,2019,2020 |
URL | https://rhizosphere.org |
Description | EMBL course, Heidelberg. Microbial Communities: Modelling meets Experiments (Dec 2019) - Andrzej Tkacz |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Professional Practitioners |
Results and Impact | Andrzej attended this course which is very relevant to his post-doctoral work. He engaged with the participants from all over Europe. |
Year(s) Of Engagement Activity | 2019 |
Description | Herborn University (June 2019( 33rd Old Herborn University Conference - Andrzej Tkacz |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Professional Practitioners |
Results and Impact | Andrzej gave a talk at this conference in Germany. |
Year(s) Of Engagement Activity | 2019 |
Description | Microbiome Capability Workshop (March 2020) - AT and PSP |
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 | Phil gave a talk to other interested parties at this BBSRC workshop |
Year(s) Of Engagement Activity | 2020 |
URL | https://rhizosphere.org/lab-news/ |
Description | Mini-symposium Chemical Signalling in the Rhizosphere (Cumbria, Sept. 2019)- Phil Poole |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Professional Practitioners |
Results and Impact | A group of international scientists focussed on a very defined problem in a retreat-like setting. |
Year(s) Of Engagement Activity | 2019 |
URL | https://rhizosphere.org/lab-news/ |
Description | Molecular Plant Biology Seminar Series, Dept. of Biology, Oxford (PSP) |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Professional Practitioners |
Results and Impact | A talk to other members of the department entitled: Rhizobium-Legume Symbiosis (PSP). Lots of discussion on how the work of the section could be integrated. |
Year(s) Of Engagement Activity | 2022 |
URL | https://rhizosphere.org/lab-news-current/ |
Description | Ohio State University, Student Seminar (PSP) |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Undergraduate students |
Results and Impact | Seminar for students in USA (held online). Talk entitled: Life-cycle transitions of rhizobia from bacteria to nitrogen-fixing symbionts. Lots of questions from interested audience. |
Year(s) Of Engagement Activity | 2022 |
URL | https://rhizosphere.org/lab-news-current/ |
Description | Organise and run OxBacNet meeting (May 2019) - Alison East |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Professional Practitioners |
Results and Impact | Organise this networking event to get the bacteriologists (located in many different departments across Oxford) together in one place to exchange information and ideas. The email list has 150 names and we get approx. 80 attending the termly meetings (lasting an afternoon). |
Year(s) Of Engagement Activity | 2019 |
URL | https://rhizosphere.org/oxbacnet/ |
Description | Organise and run OxBacNet meeting - Alison East |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Professional Practitioners |
Results and Impact | I plan and design the programme, inviting all the speakers and organising the whole meeting (from tea and coffee, projectors, display of posters and pizza delivery for the networking sessions). This is an extremely successful initiative reaching the bacteriologists working in the many different locations around Oxford. |
Year(s) Of Engagement Activity | 2020,2021 |
URL | https://rhizosphere.org/oxbacnet/ |
Description | Organised and ran the Nitrogen Network Annual Meeting, July 2022 |
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 | 60 scientists from the UK attended a one-day meeting, organised by the Poole Lab (AE). Talks from the Poole Lab included: Engineering nitrogen-fixing symbiosis between cereals and bacteria (TH), Analysis of the regulatory systems controlling carbon and nitrogen metabolism (CSC) and Understanding Plant Colonisation by Gammaproteobacteria Using Metabolic Modelling and Multi-Omics Approaches (BT). |
Year(s) Of Engagement Activity | 2022 |
URL | https://synthsym.org/nitrogen-network/ |
Description | OxBacNet Meeting, May 2022 |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Professional Practitioners |
Results and Impact | Organised and ran a one-day networking even for Oxford's bacteriologists. |
Year(s) Of Engagement Activity | 2022 |
URL | https://rhizosphere.org/lab-news-current/ |
Description | OxBacNet meeting (Feb 2020) - Andrzej Tkacz |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Postgraduate students |
Results and Impact | Andrzej gave a talk entitled 'A holistic approach to the plant microbiome' to an audience of 80 scientists at this networking and seminar series.There was a lively discussion concerning the work presented in the networking session at the end. |
Year(s) Of Engagement Activity | 2020 |
URL | https://rhizosphere.org/lab-news/ |
Description | OxBacNet meeting, Nov 2022 (AE) |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Professional Practitioners |
Results and Impact | Organised and ran the networking even for Oxford's bacteriologists. |
Year(s) Of Engagement Activity | 2022 |
URL | https://rhizosphere.org/lab-news-current/ |
Description | Plant Genomes, Systems Biology and Engineering, Cold Spring Harbor, 1st-3rd Dec 2021 |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Professional Practitioners |
Results and Impact | On-line conference. Plant Genomes, Systems Biology and Engineering. |
Year(s) Of Engagement Activity | 2021 |
URL | https://meetings.cshl.edu/meetings.aspx?meet=PLANTS&year=21 |
Description | Plant-Microbe Interactions Symposium, Society for Applied Microbiology, Oct 2020 (PSP) |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Postgraduate students |
Results and Impact | Phil gave a talk entitled 'Rhizobium from rhizosphere to root nodule' at this online conference. It reached a wide audience who asked a series of questions after the talk. |
Year(s) Of Engagement Activity | 2020 |
URL | https://sfam.org.uk/career/ems-event-calendar/plant-microbe-interactions-series-part-1.html |
Description | Rothamsted Research invited seminar - Phil Poole |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Professional Practitioners |
Results and Impact | Phil gave a lunch-time research seminar. |
Year(s) Of Engagement Activity | 2019 |
URL | https://rhizosphere.org/lab-news/ |
Description | Spain-UK Plant Biotechnology Forum - Chairperson |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Postgraduate students |
Results and Impact | Chairperson during session of this scientific meeting |
Year(s) Of Engagement Activity | 2022 |
URL | https://rhizosphere.org/lab-news-current/ |
Description | Talk at Curtin University, Western Australia - Phil Poole (Nov 2019) |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Professional Practitioners |
Results and Impact | Phil gave a seminar on his research to an audience of scientists. |
Year(s) Of Engagement Activity | 2019 |
URL | https://rhizosphere.org/lab-news/ |
Description | Twitter account Rhizosphere @PooleLabOxford |
Form Of Engagement Activity | Engagement focused website, blog or social media channel |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Public/other audiences |
Results and Impact | Twitter account to publicise the work of the Poole Lab |
Year(s) Of Engagement Activity | 2017,2018,2019,2020 |
URL | https://twitter.com |
Description | UK Legume Research Community Conference, Norfolk Jan 2023 (PSP) |
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 | Attended workshop and participated in networking and discussions concerning future research directions. |
Year(s) Of Engagement Activity | 2022 |
URL | https://rhizosphere.org/lab-news-current/ |
Description | Visit to Centre of Rhizobium Studies, Murdoch University, Perth - Philip Poole (Nov 2019) |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Postgraduate students |
Results and Impact | Phil visited CRS and gave a seminar. Also during his visit he was able to interact with post-graduate students. |
Year(s) Of Engagement Activity | 2019 |
URL | https://rhizosphere.org/lab-news/ |
Description | Visit to colleagues in Dundee (Nov 2019) - Andrzej Tkacz |
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 | Andrzej had a meeting with colleagues in Dundee working on similar research problems. There was an exchange of research ideas and project results. |
Year(s) Of Engagement Activity | 2019 |
Description | course at Hinxton EMBL NGS Bioinformatics (Sept. 2019) - Andrzej Tkacz |
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 | Andrzej attended this meeting and engaged with other students of NGS Bioinformatics. |
Year(s) Of Engagement Activity | 2019 |