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

To acquire sufficient mineral nutrients such as phosphate (Pi) from the soil, most plants engage in symbiosis with arbuscular mycorrhizal (AM) fungi. Attracted by plant-secreted strigolactones (SLs), the fungi colonize the roots and form highly branched hyphal structures called arbuscules inside inner cortex cells. The host plant must control 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 lifespan, are far from understood. Here, we show that Medicago truncatula SPX-domain containing proteins SPX1 and SPX3 regulate root Pi starvation responses, in part by interacting with PHOSPHATE RESPONSE REGULATOR2, as well as fungal colonization and arbuscule degradation. SPX1 and SPX3 are induced upon Pi starvation but become more restricted to arbuscule-containing cells upon the establishment of symbiosis. This induction in arbuscule-containing cells is associated with the presence of cis-regulatory AW-boxes and transcriptional regulation by the WRINKLED1-like transcription factor WRI5a. Under Pi-limiting conditions, SPX1 and SPX3 facilitate the expression of the SL biosynthesis gene DWARF27, which could help explain the increased fungal branching in response to root exudates. Later, in arbuscule-containing cells, SPX1 and SPX3 redundantly control arbuscule degradation. Thus, SPX proteins play important roles as phosphate sensors to maintain a beneficial AM symbiosis.

The THO/TREX Complex Component RAE2/TEX1 Is Involved in the Regulation of Aluminum Resistance and Low Phosphate Response in Arabidopsis

The C2H2-type zinc finger transcription factor SENSITIVE TO PROTON RHIZOTOXICITY 1 (STOP1) plays a critical role in aluminum (Al) resistance and low phosphate (Pi) response mainly through promoting the expression of the malate transporter-encoding gene ARABIDOPSIS THALIANA ALUMINUM ACTIVATED MALATE TRANSPORTER 1 (AtALMT1). We previously showed that REGULATION OF ATALMT1 EXPRESSION 3 (RAE3/HPR1), a core component of the THO/TREX complex, is involved in the regulation of nucleocytoplasmic STOP1 mRNA export to modulate Al resistance and low Pi response. Here, we report that RAE2/TEX1, another core component of the THO complex, is also involved in the regulation of Al resistance and low Pi response. Mutation of RAE2 reduced the expression of STOP1-downstream genes, including AtALMT1. rae2 was less sensitive to Al than rae3, which was consistent with less amount of malate secreted from rae3 roots than from rae2 roots. Nevertheless, low Pi response was impaired more in rae2 than in rae3, suggesting that RAE2 also regulates AtALMT1-independent pathway to modulate low Pi response. Furthermore, unlike RAE3 that regulates STOP1 mRNA export, mutating RAE2 did not affect STOP1 mRNA accumulation in the nucleus, although STOP1 protein level was reduced in rae2. Introduction of rae1 mutation into rae2 mutant background could partially recover the deficient phenotypes of rae2. Together, our results demonstrate that RAE2 and RAE3 play overlapping but distinct roles in the modulation of Al resistance and low Pi response.