Plants establish beneficial symbiotic associations with arbuscular mycorrhizal fungi, which colonize the root cortex, building specialized structures called arbuscules that facilitate nutrient exchange. The association occurs following plant recognition of lipochitooligosaccharides (LCOs) from mycorrhizal fungi, which activates the symbiosis signaling pathway prior to mycorrhizal colonization. Here we show that SLR1/DELLA, a repressor of gibberellic acid (GA) signaling, and its interacting partner protein are required for the mycorrhizal symbiosis. GA treatment inhibits mycorrhizal colonization and leads to the degradation of DELLAs. Consistently, rice lines mutated in DELLA are unable to be colonized by mycorrhizal fungi. DELLAs are members of the GRAS family of transcription factors. We further show that rice DELLA interacts with a second GRAS protein, DIP1 (DELLA Interacting Protein 1). DIP1 is also required for mycorrhizal colonization and in turn interacts with a previously characterized mycorrhizal GRAS protein, RAM1, that has been shown to directly regulate mycorrhizal-associated gene expression. We conclude that a complex of GRAS proteins, including DELLAs, is necessary for regulation of mycorrhizal-associated gene expression and thus colonization.

It has previously been shown by whole genome transcriptomic analysis that GA biosynthetic genes are induced during mycorrhizal colonization in rice1. Furthermore, GA has been shown to inhibit mycorrhizal colonization in Pisum sativum2. To understand the role of GA in this regulation, we sought to assess the function of GA during mycorrhizal colonization. Oryzae sativa ssp. japonica cv. Zhonghua11 plants were infected with the arbuscular mycorrhizas (AM) fungus Rhizophagus irregularis and treated with 0.1 μM, 1 μM, 10 μM and 100 μM GA3. Consistent with previous studies, GA treatment greatly promoted the elongation of the shoot and root (Supplementary information, Figure S1). Interestingly, mycorrhizal colonization was severely impaired at 0.1 μM, 1 μM GA3, and was completely blocked at 10 μM and 100 μM GA3, suggesting that GA negatively regulates AM colonization (Supplementary information, Figure S2A). AM1, AM3, AM10, AM14, AM15, AM34 and PT11 were previously shown to be induced during mycorrhizal colonization of rice3. Consistent with the changes that we observed in mycorrhizal colonization, the expression of these AM-specific marker genes was repressed by GA treatment (Supplementary information, Figure S2B and S2C). To explore whether the effect of GA was limited to rice, we also tested the effect of GA treatment on the AM symbiosis in Medicago truncatula. Consistent with the results in rice, colonization levels were greatly reduced by 10 μM GA3 treatment in M. truncatula (Supplementary information, Figure S2E). These results suggest that GA negatively regulates the AM symbiosis in both monocotyledonous and dicotyledonous plants.

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