Especially under nutrient-limiting conditions, most land plants form mutually beneficial interactions with soil-borne fungi in a symbiosis called arbuscular mycorrhiza. The vast network of the fungal hypha absorbs micronutrients – e.g. phosphate – from the soil and transports them to the plant roots in exchange for carbon. In response to variation in nutrient status, the host plant is able to control the intensity of the symbiosis, a process that requires intercellular signaling between colonized root cells and other tissues of the plant. We identified several genes encoding secreted peptides of the CLV3/ESR-related (CLE) family – members of which have previously been identified to act as nutrient or developmental signals in other plant systems – that are up-regulated during mycorrhizal symbiosis in roots of the legume Medicago truncatula. We focused on one mycorrhiza-induced gene (MtCLE53); as well as on MtCLE33, which is not regulated by arbuscular mycorrhizal symbiosis but its expression is induced by external phosphate application. The promoter of both genes is active in the vascular tissues, thus making those genes excellent candidates for long-range (nutrient) signals. In line with this hypothesis, overexpression of MtCLE33 and MtCLE53 in Medicago transgenic roots reduces colonization by mycorrhizal fungi, a phenotype that depends on the presence of a close homolog of the leucine-rich-repeat receptor-like kinase AtCLAVATA1, SUNN. Roots overexpressing MtCLE53 or MtCLE33 showed reduced expression of several key enzymes producing strigolactones – the cues emitted to the rhizosphere by nutrient-starved plants in order to attract beneficial symbionts. A lower strigolactone content in MtCLE-overexpressing roots was also confirmed using mass-spectrometry analysis. Taken together, we identified two CLE-SUNN pathways that integrate signals of plant mycorrhizal colonization and nutrient status to control the extent of the symbiosis and ensure an optimal cost-benefit balance for the host plant.
Coauthors: Kristyna Flokova – Laboratory of Growth Regulators, Palacký University, Czech Republic;Elise Schnabel – Clemson University, Clemson, SC, USA;Xuepeng Sun – Boyce Thompson Institute, Ithaca, NY, USA;Zhangjun Fei – Boyce Thompson Institute, Ithaca, NY, USA;Julia Frugoli – Clemson University, Clemson, SC, USA;Harro Bouwmeester – 2Swammerdam Institute for Life Sciences, University of Amsterdam, The Netherlands;Maria Harrison – Boyce Thompson Institute, Ithaca, NY, USA