Rooting around the wheat microbiome

Golden wheat field
© iStock/IakovKalinin

As part of our 75th Anniversary, The Microbiology Society undertook a project entitled “A Sustainable Future, which aimed to highlight the Sustainable Development Goals (SDGs) to our members and empower them to use their research to evidence and impact the goals. In 2020, we put a call out to our members to submit case studies in the following three areas: antimicrobial resistance, soil health and the circular economy.

This case study was written by Dr Tim Mauchline, who is a plant and soil microbiologist at Rothamsted Research, UK. It focuses on Soil Health; maintaining the health of our soils has gained increasing prominence in recent years. Soils are essential for the global food system and regulate water, carbon and nitrogen cycles, but are put under pressure from population growth and climate change.

The current rate of agrochemical application to agricultural systems is unsustainable. When this is considered along with continued growth of the human population, which by 2050, will exceed nine billion people (United Nations, 2019); predictions are that food production, based on current rates, must increase by 70% in order to sustain this global population (FAO, 2009).

Alternative strategies and technologies must be implemented to achieve the grand challenge of sustainable intensification (SI) of agricultural systems, which aims to increase crop yields with fewer inputs (Giller et al., 2015; Rockström et al., 2017). It is likely that SI will adopt a mixture of existing practices, such as soil conservation through reduced tillage, as well as the incorporation of cover crops/green manures to improve soil structure (Giller et al., 2015). Hi-tech approaches, such as the use of crop varieties with improved yield (Chen et al., 2019; Zhu et al., 2020) and tolerance to environmental stresses will be crucial. This will be underpinned by satellite and drone data to predict pest and disease outbreaks, to create high resolution nutrient prescription maps, which will be implemented to guide precision agriculture (Balafoutis et al., 2017).

However, in addition to these innovations, it could be that part of the answer to the solution of SI lies beneath our feet. It is known that naturally occurring soil micro-organisms, especially those in the plant root zone, can benefit plants either through the provision of nutrients, as well as protection against abiotic and biotic stresses. This highly complex microbial community, known as the root microbiome, can be subdivided into the rhizosphere, rhizoplane and endosphere compartments and it can now be studied in high resolution due to the development of next generation sequencing technologies (Compant et al., 2019).

At Rothamsted Research, plant microbiome studies have focused on studying the root microbiome of wheat, the UK’s most cultivated crop. Rothamsted is home to many long-term experiments and we have utilised some of these to demonstrate the importance of various factors in shaping the wheat microbiome. For example, we have utilised the Broadbalk experiment to demonstrate the importance of fertilisation regime (Robinson et al., 2016; Kavamura et al., 2018), as well as land use conversion at the Highfield experiment (Kavamura et al., 2019). We found that these factors impact root microbiome composition in both the rhizosphere as well as the endosphere. We also found that increases in inorganic nitrogen fertilisation application results in a decrease in microbial species richness (Kavamura et al., 2018). In addition, in a wheat ‘heritage’ experiment we found evidence that wheat genotype has an influence on rhizosphere microbiome structure and that this can be linked to the incorporation of reduced height mutant alleles into their genomes. The work demonstrated an increased species richness in modern wheat cultivars, but network analysis predicted that this community was less well interconnected than tall cultivars, suggesting that microbial community interactions and possibly plant-microbe interactions may have been disrupted by wheat dwarfing (Kavamura et al., 2020).

In addition to describing microbiome community structure, it is also important to elucidate the activity of microbes and to establish whether they convey functions that are beneficial to plants. A collaboration between scientists at Rothamsted and the John Innes Centre (JIC) identified shifts in Pseudomonas wheat root population structure in a take-all infested field (Mauchline et al., 2015). Cropping sequence was found to influence build-up of pathogen inoculum as well as bacterial community profiles. Differences in Pseudomonas genome structure, as well as the ability of pseudomonads to suppress the pathogen were found, and intriguingly the Pseudomonas spp. diversity was negatively associated with suppression of the wheat take-all pathogen (Mehrabi et al., 2016). The approach of combining whole microbiome analysis with functional microbiology of plant root and soil associated microbes is increasingly feasible due to advances in culturing techniques (Bai et al., 2015; Mauchline and Malone, 2017). Cultured microbes can be tested with a suite of in vitro screens to identify putative plant growth promoting and disease suppressing microbes and promising candidates taken forward for in planta screening. At Rothamsted we recently developed a manipulatable compost-based screening system in which nutrient levels can be controlled and their effect on plant growth disentangled from the growth medium structure. This system has been used to demonstrate that a phosphate solubilising pseudomonad significantly boosted wheat growth (Masters-Clark et al., 2020).

The importance of microbial culture-based solutions for agricultural problems is gaining more recognition. This can be via the use of plant growth promoting microbial inoculants as single isolates or as novel synthetic consortia. In addition, the exploitation of microbes as a source of natural products is a relatively untapped resource. A cross-disciplinary approach utilising microbial phenotyping, genomics, and genetics as well as analytical and synthetic chemistry is required for the discovery of microbial products for plant growth promotion or pathogen suppression. The initiation of the UK-Crop Microbiome Cryobank, a BBSRC BBR project led by CABI in collaboration with Rothamsted, JIC, The James Hutton Institute and Scotland’s Rural College exemplifies the increased interest in a culture led approach. This project aims to establish a comprehensive bank of microbial cultures from a range of crop species cultured in contrasting soil types. The resource will be the first of its kind in the UK and will include microbial genomic and phenotypic data alongside metagenomic and other metadata such as edaphic factors. It is hoped that this information and research in similar projects will aid optimization of plant yields with a microbially facilitated approach.

References

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Chen, K., Wang, Y., Zhang, R., Zhang, H., & Gao, C. (2019). CRISPR/Cas Genome Editing and Precision Plant Breeding in Agriculture. Annual Review Of Plant Biology, 70, 667–697. https://doi.org/10.1146/annurev-arplant-050718-100049

Compant, S., Samad, A., Faist, H., & Sessitsch, A. (2019). A review on the plant microbiome: Ecology, functions, and emerging trends in microbial application. Journal Of Advanced Research, 19, 29–37. https://doi.org/10.1016/j.jare.2019.03.004

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Kavamura, V. N., Robinson, R. J., Hughes, D., Clark, I., Rossmann, M., Melo, I. S., Hirsch, P. R., Mendes, R., & Mauchline, T. H. (2020). Wheat dwarfing influences selection of the rhizosphere microbiome. Scientific Reports, 10(1), 1452. https://doi.org/10.1038/s41598-020-58402-y

Kavamura, V. N., Hayat, R., Clark, I. M., Rossmann, M., Mendes, R., Hirsch, P. R., & Mauchline, T. H. (2018). Inorganic Nitrogen Application Affects Both Taxonomical and Predicted Functional Structure of Wheat Rhizosphere Bacterial Communities. Frontiers In Microbiology, 9, 1074. https://doi.org/10.3389/fmicb.2018.01074

Kavamura, V. N., Robinson, R. J., Hayat, R., Clark, I. M., Hughes, D., Rossmann, M., Hirsch, P. R., Mendes, R., & Mauchline, T. H. (2019). Land Management and Microbial Seed Load Effect on Rhizosphere and Endosphere Bacterial Community Assembly in Wheat. Frontiers In Microbiology, 10, 2625. https://doi.org/10.3389/fmicb.2019.02625

Masters-Clark, E., Shone, E., Paradelo, M., Hirsch, P. R., Clark, I. M., Otten, W., Brennan, F., & Mauchline, T. H. (2020). Development of a defined compost system for the study of plant-microbe interactions. Scientific Reports, 10(1), 7521. https://doi.org/10.1038/s41598-020-64249-0

Mauchline, T. H., & Malone, J. G. (2017). Life in earth - the root microbiome to the rescue? Current Opinion In Microbiology, 37, 23–28. https://doi.org/10.1016/j.mib.2017.03.005

Mehrabi, Z., McMillan, V. E., Clark, I. M., Canning, G., Hammond-Kosack, K. E., Preston, G., Hirsch, P. R., & Mauchline, T. H. (2016). Pseudomonas spp. diversity is negatively associated with suppression of the wheat take-all pathogen. Scientific Reports, 6, 29905. https://doi.org/10.1038/srep29905

Mauchline, T. H., Chedom-Fotso, D., Chandra, G., Samuels, T., Greenaway, N., Backhaus, A., McMillan, V., Canning, G., Powers, S. J., Hammond-Kosack, K. E., Hirsch, P. R., Clark, I. M., Mehrabi, Z., Roworth, J., Burnell, J., & Malone, J. G. (2015). An analysis of Pseudomonas genomic diversity in take-all infected wheat fields reveals the lasting impact of wheat cultivars on the soil microbiota. Environmental Microbiology, 17(11), 4764–4778. https://doi.org/10.1111/1462-2920.13038

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United Nations, Department of Economic and Social Affairs, Population Division (2019). World Population Prospects 2019: Highlights (ST/ESA/SER.A/423). Available at: https://population.un.org/wpp/Publications/Files/WPP2019_Highlights.pdf.

Zhu, H., Li, C., & Gao, C. (2020). Applications of CRISPR-Cas in agriculture and plant biotechnology. Nature Reviews. Molecular Cell Biology, 21(11), 661–677. https://doi.org/10.1038/s41580-020-00288-9

About the author
Dr Tim Mauchline is a plant and soil microbiologist at Rothamsted Research, UK. More information on his work is available here
 
Funding sources
The  Bilateral BBSRC-Embrapa grant on “Exploitation of the wheat rhizosphere microbiome for sustainable wheat production” (BB/N016246/1); Achieving Sustainable Agricultural Systems (NE/N018125/1 LTS-M ASSIST); Optimization of nutrients in soil-plant systems: How can we control nitrogen cycling in soil? (BBS/E/C/00005196); S2N – Soil to nutrition – Work package 1 – Optimizing nutrient flows and pools in the soil-plant-biota system (BBS/E/C/000I0310); The UK-Crop Microbiome Cryobank (BB/T019492/1).