Both in natural and agricultural ecosystems, plants are constantly exposed to numerous abiotic and biotic factors; and plant survival and fitness depends on the continuous assessment and systemic integration of information to adapt to such environmental stimuli. To cope with e.g. nutrient scarcity, most land plant species – including crops like soybean or maize – engage in an intimate relationship with soil fungi of the phylum Glomeromycotina and form a symbiosis called arbuscular mycorrhiza (AM) symbiosis. AM fungi colonize the root cortical cells of their host plant, where they form branched hyphal structures called “arbuscules”. At the same time, AM fungi form a vast hyphal network surrounding the root, which allows them to take up mineral nutrients such as phosphate (Pi) very efficiently and from distant locations in the soil. These mineral nutrients are then transferred to the host plant via specialized transporters at the host-symbiont interface in the arbuscule-harboring cortex cells. In exchange for these benefits, the fungal symbiont receives carbon (C) from the host plant (Figure 1).
The bidirectional nutrient exchange underlying AM symbiosis is basis for a balanced, mutualistic symbiosis, which leads to an increased nutrient uptake of the host plant. However, disturbances in this balance (e.g. when the fungal partner sequestrates carbon from the host plant but does not deliver sufficient Pi) can lead to an imbalanced symbiosis that can lead to detrimental consequences for the plant host.
Why is this important?
AM symbiosis bears tremendous potential for a sustainable agriculture: it is estimated that the human population will reach nine billion by the year 2050, causing global crop demand to increase dramatically. At the same time, present agricultural practices, which include excess application of fertilizers, are not sustainable and often harmful for the environment, and thus will undermine the future generation’s capacities for agricultural food production. Most crop plants, however, are capable of engaging in a symbiosis with AM fungi. Therefore, an efficient use of these microbial symbionts in agriculture could diminish the need for chemical fertilizers. However, a broad application of AM fungi to agricultural fields is problematic for many reasons, including ecological considerations that come with introducing non-native fungi to a field. In addition, not all AM fungal species are equally beneficial to a given plant species under all environmental circumstances, and sometimes AM fungal colonization can even lead to detrimental outcomes for the host plant. One solution to this dilemma is to breed for plants that maximally exploit the benefits of AM symbiosis under various environmental conditions. AM symbiosis initiation and maintenance is largely under the control of the host plant. If AM symbiosis is to be successfully employed in agriculture setting it is crucial to fully understand the regulatory mechanisms underlying plant control over fungal colonization. Only then we can breed for plant genotypes that maximize symbiotic benefits.
Autoregulation of mycorrhizal symbiosis
One regulatory mechanism that allows the plant to control root colonization is called “autoregulation of mycorrhiza symbiosis” (AOM). AOM is a mechanism that allows the plant to assess the current extent of root colonization, and “switch off” further AM fungal root colonization once a critical colonization level is reached.
In Medicago truncatula, the AOM pathway consists of the small, mobile peptide hormone CLE53, which is produced in the vascular tissue of roots colonized by AM fungi as shown by promoter-GUS experiments (Figure 2A, B). From there, CLE53 can move systemically to elicit its function in other roots or plant organs. Genetic over-expression of CLE53 using the ubiquitously active 35S promoter leads to a suppression of AM fungal root colonization, which was found to be dependent on the leucine-rich receptor-like kinase SUNN (Figure 2C). By sequencing the transcriptome of CLE53-overexpressing roots and by direct hormone measurements, we found that overexpression of CLE53 leads to a decrease in the production of certain phytohormones, namely strigolactones. Strigolactones (SL) are produced by phosphate-starving plants and act as direct communication molecules between the host plant and the AM fungus in the rhizosphere, and are important regulators of symbiosis initiation.
Thus, we hypothesize that plants utilize the CLE53-mediated AOM pathway to fine-tune root colonization by AM fungi: If a plant is starving for Pi, it produces and secretes strigolactones, which then lead to initiation and establishment of AM symbiosis. Colonized roots express CLE53. Once a critical root colonization (and CLE53) level is reached, the initiation of further root colonization will be suppressed by slowing down strigolactone production (Figure 2D). This results in a balanced root colonization level and prevents over-colonization of the root system and over-sequestration of carbon by the fungal symbiont.
In the Müller lab, we strive to better understand the molecular signaling pathways underlying plant control over AM symbiosis.
Our research is centered on the interface of molecular genetics, plant physiology, and ecology. We employ targeted mutagenesis, transcriptomics, genetics, genomics, and microscopy in model plant species such as Medicago truncatula to answer questions like “what is the molecular function of symbiotic peptide signals?”, “how are symbiotic peptide signals induced and transduced?”, “how do plants prevent parasitism (over-sequestration of carbon) by AM fungi?”, and “how do plants measure symbiosis success?”.
If we understand the molecular pathways of plant control over AM symbiosis, we can use this knowledge to breed for crop plants with better capacities to exploit the benefits of AM symbiosis. In light of climate change, the imminent decline of phosphorous fertilizer resources and increased environmental pollution through excess fertilizer usage, a targeted application of AM symbiosis in agriculture might be one solution to feed a growing human population in a sustainable way.