CLE signaling in arbuscular mycorrhiza symbiosis
Final Report Abstract
Most land plants, including major crops like soybean or maize, form a mutually beneficial relationship with soil fungi called arbuscular mycorrhiza (AM) symbiosis. For the fungal partner the symbiosis is obligatory, as the plant provides the fungus with fatty acids it is not able to synthesize. In contrast, most plants are able to survive without the symbiosis, however in nutrient-depleted soils the fungal partner provides substantial benefit to the plant by increasing its mineral nutrient uptake. One of the main mineral nutrients provided by AM fungi is phosphate. It has been known for a long time that plants control the extent of fungal colonization in their root systems, possibly in order to prevent overcolonization and over-sequestration of carbon by the fungal symbiont. One such control mechanism, termed “autoregulation of mycorrhizal symbiosis” (AOM), describes a phenomenon in which colonized roots elicit a negative systemic signal that prevents further colonization of other parts of the root system. Hence, AOM would “measure” root colonization and – once a critical level is reached – inhibit further colonization. Until recently, neither the signal nor the mechanism underlying AOM signalling was known. In one part of my postdoctoral project we found that the MtCLE53 gene is induced in roots of the legume plant Medicago truncatula colonized by AM fungi. Overexpression of this gene resulted in a decrease in root colonization, indicating that MtCLE53 could be the negative signal underlying AOM. This is further supported by the fact that CLE genes encode short peptides, which are mobile and thus represent excellent candidates for long- and short-range signalling; and in addition it was previously described that AOM is regulated by a receptor kinase known to be involved in CLE signalling. In line with this, the negative effect of MtCLE53 was not observed in sunn mutants, which are impaired in the function of this receptor kinase. Using next-generation sequencing of root transcripts following overexpression of MtCLE53, we identified several genes involved in the biosynthesis of strigolactones as major targets of MtCLE53 signalling. Strigolactones are phytohormones that are predominantly produced in plant roots starving for phosphate and are secreted into the rhizosphere, where they act as direct communication signal to the AM fungi and promote symbiosis initiation. Thus, the observation that enhanced MtCLE53 signalling decreases the production of these AM-promoting compounds provides an explanation for the reduced fungal colonization in MtCLE53 overexpressing roots. It furthermore provides a mechanistic explanation for previous observations indicating that strigolactone content decreases in roots after they are colonized by AM fungi. Taken together, by identifying and functionally characterizing an AM-induced M. truncatula CLE gene my postdoctoral project has contributed to the understanding of plant control over fungal colonization. In modern-day agriculture, mineral nutrients are provided to the plants by application of synthetic fertilizer. However, over-application of fertilizer leads to run-off into the groundwater and thus increases pollution of lakes and streams. In addition, fertilizer resources are finite and declining. Thus, a future sustainable agriculture will increasingly rely on AM symbiosis, which allows the plants to efficiently acquire mineral nutrients and thus reduces the need for fertilizers. However, understanding the molecular basis of plant control over fungal colonization is critical if we want to employ AM symbiosis in an agricultural setting. Only if we fully understand the environmental conditions under which a symbiosis is beneficial and supported by the plant, we can exploit it to sustainably increase crop yield and plant health. The molecular characterization of the AOM pathway is one first step to understand plant control over fungal colonization, and it is conceivable that manipulation of this pathway could help us to optimize AM symbiosis in the future.
Publications
- A transcriptional program for arbuscule degeneration during AM symbiosis is regulated by MYB1. Current Biology 27 (8), 1206-1212 (2017)
Floss DS, Gomez KS, Park HJ, MacLean AM, Müller LM, Bhattarai KK, Levesque-Tremblay V, Maldonado-Mendoza IE, Harrison MJ
(See online at https://doi.org/10.1016/j.cub.2017.03.003) - Phytohormones, miRNAs, and peptide signals integrate plant phosphorus status with arbuscular mycorrhizal symbiosis. Current Opinion in Plant Biology 50, 132-139 (2019)
Müller LM and Harrison MJ
(See online at https://doi.org/10.1016/j.pbi.2019.05.004)
