Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi

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Abstract
The discovery of a previously unknown mechanism of nitrogen transfer from the arbuscular mycorrhizal fungi found on the roots of most land plants, to the host plants suggests that this symbiotic relationship may be a much more important factor in the global nitrogen cycle than was thought. The mechanism involves uptake of inorganic nitrogen by the fungus outside the roots, conversion to amino acids within the fungus, then transfer as ammonium ions from the fungal mycelium into the plant. The first event in host recognition by arbuscular mycorrhizal fungi is thought to be hyphal branching. A strigolactone, 5-deoxy-strigol, isolated from Lotus japonicus has now been identified as an inducer of branching. Strigolactones are root metabolites, previously isolated as seed germination stimulants for root parasitic weeds. This finding highlights the close relationship between plant and fungus, and may provide a new strategy for the control of both beneficial fungal symbionts and destructive parasitic weeds in agriculture and natural ecosystems. Arbuscular mycorrhizal (AM) fungi form mutualistic, symbiotic associations with the roots of more than 80% of land plants1. The fungi are incapable of completing their life cycle in the absence of a host root. Their spores can germinate and grow in the absence of a host, but their hyphal growth is very limited. Little is known about the molecular mechanisms that govern signalling and recognition between AM fungi and their host plants. In one of the first stages of host recognition, the hyphae of AM fungi show extensive branching in the vicinity of host roots before formation of the appressorium2,3,4, the structure used to penetrate the plant root. Host roots are known to release signalling molecules that trigger hyphal branching5,6,7, but these branching factors have not been isolated. Here we have isolated a branching factor from the root exudates of Lotus japonicus and used spectroscopic analysis and chemical synthesis to identify it as a strigolactone, 5-deoxy-strigol. Strigolactones are a group of sesquiterpene lactones, previously isolated as seed-germination stimulants for the parasitic weeds Striga and Orobanche8. The natural strigolactones 5-deoxy-strigol, sorgolactone and strigol, and a synthetic analogue, GR24, induced extensive hyphal branching in germinating spores of the AM fungus Gigaspora margarita at very low concentrations.