GmSPX5 regulates arbuscular mycorrhizal colonization and phosphate acquisition through modifying transcription profile and microbiome in soybean

Symbiosis with arbuscular mycorrhizal (AM) fungi is a crucial strategy for plant adaptation to low phosphorus (P) stress. However, the mechanisms underlying how phosphate (Pi) signaling regulators participate in AM colonization remain largely unknown in soybean (Glycine max). In this study, the expression of GmSPX5, one member of the SPX (SYG1/Pho81/XPR1) family, was induced by AM fungal inoculation in soybean roots. Furthermore, the expression of GmSPX5 seems to overlap with AM infection structures through analyzing GUS activity of transgenic soybean plants harboring Pro_GmSPX5:GUS. Four transgenic lines with GmSPX5 overexpression (OX8 and OX12) and suppression (Ri9 and Ri11) were subsequently used to examine the functions of GmSPX5 on AM symbiosis and Pi acquisition. Despite no difference between Ri and wild-type (WT), the overexpression of GmSPX5 significantly increased AM colonization as reflected by 8.4% in OX8 and 8.7% in OX12, respectively. Consistently, the dry weight and total P content of OX8 and OX12 were higher than WT. Furthermore, a total of 3483 genes were found to exhibit differential expression patterns in roots between OX12 and WT, including genes related to linolenic acid metabolism and flavonoid metabolism. Meanwhile, the composition of the bacterial community in the roots of OX12 was distinct from that in WT through β-diversity analysis. Particularly, an ASV19 (Sphingomonadales) was enriched in OX12 roots, which was positively related to total P content and AM fungi colonization. Taken together, these results highlight that GmSPX5 can regulate AM symbiosis, as well as Pi acquisition in soybean. Our findings advance the understanding of SPX functions in plant–microbe interaction.