Establishing AM symbiosis: Letting friends stay only when you need their gifts

Symbiotic mycorrhizal associations between land plants and fungi can be traced back 400 million years in the fossil record. Arbuscular mycorrhiza (AM) in the phylum Glomeromycota facilitates the acquisition of nutrients such as phosphorus (in the form of orthophosphate, P_i), nitrogen, and other minerals from the soil by plant roots. AM symbiosis also promotes plant fitness under abiotic stresses and against pathogen attack (MacLean et al., 2017). Notably, plants can suppress development of AM symbiosis under P_i-replete growth conditions, indicating that the establishment of the symbiosis is regulated by the plant. Understanding how plants regulate the establishment of AM symbiosis has been an important goal of researchers, as it may enable the development of crops with less dependence on synthetic fertilizers.

Because P_i was known to suppress AM symbiosis, recent research has focused on the SYG1/Pho81/XPR1 (SPX)—PHOSPHATE STARVATION RESPONSE (PHR) module, which plays crucial roles in P_i sensing, transport, and remobilization. PHRs are a family of R2R3 MYB transcription factors that are required for root colonization and AM function. SPXs are a group of sensors for internal P_i status that negatively regulate PHR activity, and hence, AM symbiosis under P_i-replete conditions. Three recent independent studies highlighted the role of the SPX-PHR module in determining AM symbiosis in rice (Oryza sativa L. ssp. japonica; Shi et al., 2021; Das et al., 2022) and in the legume (Medicago truncatula; Wang et al., 2021). In new work, Dehua Liao, Chao Sun and colleagues (Liao et al., 2022) extended the investigation in tomato (Solanum lycopersicum), a complex system consisting of 17 putative SlPHR homologs and five SlSPX proteins. By systematically analyzing the phenotype of mutants, overexpressors, complementation lines, and mutants coupled with virus-induced gene silencing (to overcome functional redundancy), the authors confirmed the role of SlSPX1 and SlPHR1/4 in modulating AM symbiosis in tomato (see Figure).

Figure.

Model for the inhibition of AM symbiosis under Pi-replete conditions in tomato. A, Under Pi-deplete conditions, SlPHR1/4 binds to the promoter region (P1BS) of genes required for AM symbiosis to promote functional interaction. B, Under Pi-replete conditions, SlSPX1 interacts with SlPHR1/4, inhibits transcription initiation, and hence AM symbiosis. C, In Slspx1 mutants, total colonization is enhanced under moderate (0.25 mM) external Pi supply. Modified from Liao et al. (2022), Figure 4 and S21.

SlSPX1 stood out by showing the strongest transcript induction in AM colonized roots and under P_i-deficiency. Interestingly, mutation of SlSPX1 alone was sufficient to alter P_i accumulation, phosphate starvation response gene expression, and to promote AM colonization under moderate external P_i supply (see Figure), indicating that SlSPX1 is the major player for P_i sensing and is a negative regulator of AM symbiosis in tomato. On the other hand, five SlPHR homologs were found to be capable of binding PHR1-binding site (P1BS) and activating promoters with the P1BS motif. All five SlPHR homologs interacted with SlSPX1, but AM colonization was reduced only when SlPHR1 and SlPHR4 were simultaneously knocked out/down. Therefore, SlPHRs, principally SlPHR1 and SlPHR4, function redundantly to positively regulate AM symbiosis. The roles of SlSPX1 and SlPHR1/4 are, in general, consistent with the corresponding function in rice (Shi et al., 2021), highlighting an evolutionarily conserved mechanism that determines AM symbiosis. The case in legumes, however, seems different from rice and tomato. Wang et al. (2021) showed that MtSPX1 and MtSPX3 act as positive regulators for AM colonization by regulating strigolactones biosynthesis, leaving more questions for SPX functional diversity. For instance, the interaction between SPX and PHR proteins is known to depend on inositol pyrophosphate as a ligand (Wild et al., 2016; Ried et al., 2021). Apart from transcriptional control, understanding the protein dynamics between components of the SPX-PHR complex in relation to AM symbiosis might enable improvements in phosphorus use efficiency, and thus improvements in plant growth and yields.