Phosphate Suppression of Arbuscular Mycorrhizal Symbiosis Involves Gibberellic Acid Signaling

Most land plants entertain a mutualistic symbiosis known as arbuscular mycorrhiza with fungi (Glomeromycota) that provide them with essential mineral nutrients, in particular phosphate (P-i), and protect them from biotic and abiotic stress. Arbuscular mycorrhizal (AM) symbiosis increases plant productivity and biodiversity and is therefore relevant for both natural plant communities and crop production. However, AM fungal populations suffer from intense farming practices in agricultural soils, in particular P-i fertilization. The dilemma between natural fertilization from AM symbiosis and chemical fertilization has raised major concern and emphasizes the need to better understand the mechanisms by which P-i suppresses AM symbiosis. Here, we test the hypothesis that P-i may interfere with AM symbiosis via the phytohormone gibberellic acid (GA) in the Solanaceous model systems Petunia hybrida and Nicotiana tabacum. Indeed, we find that GA is inhibitory to AM symbiosis and that P-i may cause GA levels to increase in mycorrhizal roots. Consistent with a role of endogenous GA as an inhibitor of AM development, GA-defective N. tabacum lines expressing a GA-metabolizing enzyme (GA methyltransferase-GAMT) are colonized more quickly by the AM fungus Rhizoglomus irregulare, and exogenous P-i is less effective in inhibiting AM colonization in these lines. Systematic gene expression analysis of GA-related genes reveals a complex picture, in which GA degradation by GA2 oxidase playsa prominent role. These findings reveal potential targets for crop breeding that could reduce P, suppression of AM symbiosis, thereby reconciling the advantages of P-i fertilization with the diverse benefits of AM symbiosis.

Automated summary

This study explores the impact of phosphate (P-i) on the symbiotic relationship between plants and fungi, revealing that P-i may interfere with AM symbiosis via the phytohormone gibberellic acid (GA). Using Solanaceous model plants, it was found that GA-defective plants significantly affected the colonization of AM fungi, and exogenous phosphate had less inhibitory effect on these plants. The findings provide insights into potential targets for crop breeding to reduce P suppression of AM symbiosis and reconcile the benefits of P-i fertilization with AM symbiosis.