Capturing microbial co-symbiosis to sustain plant productivity

As the world's environment changes it is essential that we produce crop plants adapted to these changes. Within soil, species of bacteria and fungi are involved in symbiotic relationships with the root and at the root-soil interface (so called rhizosphere of crops). The relationship allows each partner to benefit from mutual trading of resources such as critical growth-limiting nutrients. This is important since plants must acquire elemental nutrients such as nitrogen and phosphorus from their surrounding environment and the availability of these nutrients is often a major limitation to plant growth. As well as bringing nutritional enhancement, mutualistic interactions bring additional benefits to improve plant productivity, such as enhanced plant resistance to adverse environmental conditions or pathogen attack. However we cannot gain all of these benefits by simply adding many 'friendly' microbes to soil since the need of one microbe might cancel out the positive effect of another microbe on the plant. How the many rhizosphere microbes compete and combine to affect the plant is a complex question that needs to be studied at a detailed level.

We have discovered that an important mutualistic fungus that helps protect plants against disease and supplies plants with phosphorus can also increase 'nodulation' in Medicago, a plant species that is a close relative of peas and beans. Nodulation is an interaction of nitrogen-fixing bacteria with plant roots that enables plants to gain otherwise unusable nitrogen. We will investigate how this enhancement of nodulation occurs, and determine if it still occurs for plants grown in different soil types. To do this we will use a range of state-of-the-art plant, soil and microbe analytical technologies to assess how microbes, plants and the soil type each contribute to the rhizosphere (microbial communities and soil adjacent to the root), and how this affects crop productivity in a range of soil types. New technologies for the identification of soil microbes mean that we are now at a point where we can study the effects of environments on multilateral interactions at the root rhizosphere - one of the most complex ecosystems on Earth. Together the results will help explain the enhanced-mutualistic effects that we have found. It will also help us to determine the importance of specific factors in the rhizosphere for agriculture, and how they could be enhanced to improve crop productivity in new environments.

In the rhizosphere, plants can affect the competition among soil microbes in any given soil type in order to establish a root-associated microbiota enriched in mutualists. Establishing multiple (co)-symbioses with members of the root microbiota extends the capacity of plants to deal with nutrient depletion and stresses. Our preliminary data suggests that co-symbiosis with the specialist N-fixing microbe Sinorhizobium meliloti and the P-supplying and disease resistance enabling fungus Piriformospora indica enhances rhizobial nodulation, P supply and disease resistance in the legume Medicago truncatula.

In order to determine the extent to which the S. meliloti - P. indica co-symbiosis persists, we will carry out a multifactorial analysis of co-enhancement with S. meliloti and P. indica in representative UK agricultural soils. Using four different UK soil types, we will test the effect of edaphic factors and the root/soil microbiota on the persistency of this co-symbiosis. We will then analyse root growth and nodule number, plant and soil mineral levels, and the numbers and species of microbes, as an output of the plant-soil-microbe system. We will understand the extent to which each organism dominates and affects plant output, and use transcriptomics to identify the plant genes that control enhancement of mutualism, in the context of nitrogen acquisition for the plant. Finally, to develop the potential use of P. indica and related sebacinoid mutualists we will investigate their prevalence across UK soil types, and test if coating M. truncatula seeds with rhizobium and sebacinoid fungi can produce nodulation and sustainable yield enhancements. Together these analyses might identify mechanisms that underlie the establishment of "mutualistic soils" that have beneficial activities in plant nutrition and stress resistance, in analogy to disease suppressive soils that provide stress protection of crops.

Threats originating from soils such as drought, flooding or increased salinity as well as root diseases are devastating in modern agriculture. These threats are increasing as climate changes, both in potency and unpredictability and are difficult, in some cases impossible, to control. If we can enhance root adaptation to environmental cues by generating crops with novel properties such as enhanced stress resistance or the ability to fix nitrogen in roots we could provide food security solutions to forward a new green revolution. Enhancing nutrient availability for plants based on modulating plant-microbial interaction/communication is one key area of impact. To overcome nutrient limitation of soils, farmers must apply fertilisers to their crop plants, the major ingredients of which are phosphates, potassium and nitrates. The production of nitrate fertiliser is a highly energy demanding process and currently accounts for approximately 2% of the world's energy usage while the natural phosphorus deposits will be consumed in the near future.

Plants find a way to improve in soil using recruited generalist or specialist microbes. Mutualistic interactions between plants and microbes thus offer a natural alternative to fertiliser application. If farmers could utilise the natural symbiotic relationships with nitrogen-fixing bacteria and mutualistic fungi that promote growth and stress resistance more successfully, it could significantly reduce or render redundant the need for fertiliser input. This would bring a range of environmental and cost savings to farmers and the public. For example there would be reduced river pollution due to lower nitrate fertiliser use and run-off, sustainable agricultural productivity, and also reduction in food miles to due higher efficiency farming methods. Importantly, our findings could be applied to agriculture in developing countries, bringing the same range of cost and environmental benefits to a large number of people under increasing food and economic poverty.
Our work has identified a novel interaction between plants and two microbes that enhance plant nodulation, enabling plants to gain nitrogen and phosphorus, and also disease resistance. We will use cutting-edge technologies to determine the robustness of this interaction and benefits. As part of this we will analyse how plants, microbes and the soil interact in order to enable the establishment of mutualistic symbioses in the rhizosphere. We will be able to define conditions that can improve plant-soil-microbe performance, in the context of nitrogen and phosphorus acquisition for the plant. This valuable information will help us to understand more about symbiotic relationships and could impact on agriculture by being able to deliver advice to farmers on how to improve plant productivity using mutualistic microbes, that are tailored to the soil type, rhizosphere community and crop.