Medicago SPX1 and SPX3 regulate phosphate homeostasis, mycorrhizal colonization and arbuscule degradation

Abstract

To acquire sufficient mineral nutrients such as phosphate (Pi) from the soil, most plants engage in a symbiosis with arbuscular mycorrhizal (AM) fungi. Attracted by plant-secreted strigolactones, the fungi colonize the roots and form highly-branched hyphal structures called arbuscules inside inner cortex cells. It is essential that the host plant controls the different steps of this interaction to maintain its symbiotic nature. However, how plants sense the amount of Pi obtained from the fungus and how this determines the arbuscule lifetime is far from understood. Here, we show that Medicago truncatula SPX-domain containing proteins SPX1 and SPX3 regulate root phosphate starvation responses as well as fungal colonization and arbuscule degradation. SPX1 and SPX3 are induced upon phosphate starvation but become restricted to arbuscule-containing cells upon establishment of the symbiosis. Under Pi-limiting conditions they facilitate the expression of the strigolactone biosynthesis gene DWARF27, which correlates with increased fungal branching by root exudates and increased root colonization. Later, in the arbuscule-containing cells SPX1 and SPX3 redundantly control the timely degradation of arbuscules. This regulation does not seem to involve direct interactions with known transcriptional regulators of arbuscule degradation. We propose a model where SPX1 and SPX3 control arbuscule degeneration in a Pi-dependent manner via a yet-to-identify negative regulator.