Bi-directional nutrient exchange
The requirement for essential soil nutrients such as nitrogen (N) and phosphate (P), is another major driver for symbiotic associations between plants and beneficial microorganisms including AMFs and nitrogen-fixing rhizobia. AMF establishes root symbiosis with more than 80% of terrestrial plants (Chan, 2022; Dey & Ghosh, 2022). The partnership is mutually beneficial but not exclusive i.e. plants can form associations with multiple microorganisms simultaneously. Such associations assist plants in the acquisition of water and essential minerals, particularly P and N (Wipf, Krajinski, van Tuinen, Recorbet, & Courty, 2019). In return, AMF and other microorganisms receive assimilated carbon. AMF-mediated N/P uptake pathways function alongside the plant nutrient transport systems, providing a greatly expanded network of nutrient uptake from distal regions beyond the normal reach of roots or root hairs.
Plants control the AMF symbioses to the availability of orthophosphate (Pi), the preferred form of P taken up by roots (H. Lu et al., 2022). The plant Pi sensing SYG1/Pho81/XPR1 (SPX)—PHOSPHATE STARVATION RESPONSE (PHR) pathway regulates AMF symbiosis in crops such as rice (Shi et al., 2021), Medicago (J. Li et al., 2021) and tomato (Liao et al., 2022). The SPXs Pi sensing proteins regulate the activity of the PHR family of R2R3 MYB transcription factors (TF). Many genes required for AMF symbiosis have PHR1-binding sites (P1BS) and are activated by PHR binding (Fig. 1B). SPX negatively regulates PHR in rice and tomato, and hence, suppresses AMF symbiosis under moderate-Pi or Pi-replete conditions. In contrast, the Medicago MtSPX1 and MtSPX3 proteins are positive regulators of AMF colonization through the regulation of strigolactone (SLs) biosynthesis. Thus, there appears to be a diversification of SPX functions between cereals and legumes (J. Li et al., 2021).
The activation of a subset of Pi-starvation induced or phosphate-starvation response (PSR) genes, is a functional marker of successful AMF symbiosis (Fig 1B). However, the genetic predisposition of the host plant is a major determinant of the efficiency of AMF symbiosis, as observed in maize accessions (Sawers et al., 2017). PHR2 (Phosphate Starvation Response 2) is a major transcription factor regulating PSR in rice. It promotes AMF colonization by activating pre-contact signaling genes and mediates mycorrhizal Pi uptake (Das et al., 2022). The OsADK1 (Arbuscule Development Kinase 1) receptor-like kinase, which is required for mycorrhizal colonization and arbuscule development, is an OsPHR2 target (Shi et al., 2022). TheRhizophagus irregularis SPX-domain containing PTs regulates arbuscule development and fine-tunes symbiotic Pi transfer -to the plant (Xie et al., 2022). Similarly, the Gigaspora margaritahigh-affinity PT, GigmPT transceptor activates a protein kinase A-mediated signaling cascade leading to Pi transport (Xie et al., 2016). Other AMF-activated genes such as LjPT4 and MtPT4 also serve Pi sensing functions in L. japonicus and M. truncatula , respectively (Volpe, Giovannetti, Sun, Fiorilli, & Bonfante, 2016). The extraradical AMF also transports Pi-solubilizing bacteria (PSB) that enhance organic P mineralization and increase Pi delivery to plants, via AMF-independent pathways (F. Jiang, Zhang, Zhou, George, & Feng, 2021).
N availability regulates plant-AMF symbiosis through proteins such as OsNPF4.5. Knockout lines lacking OsNPF4.5 functions had fewer arbuscules and lower (45%) symbiotic nitrate uptake (S. Wang et al., 2020). The lipids and carbohydrates in root exudates support fungal growth (Kameoka & Gutjahr, 2022; Salmeron-Santiago et al., 2021). Lipid provision involves two lipid biosynthetic enzymes (FatM and RAM2) and two ABC transporters (STR1 and 2; Stunted Arbuscule 1 and 2). FatM (An acyl-ACP thioesterase) increases plastid export of 16:0 fatty acids (Fig. 1A). Thereafter, RAM2 (Required for Arbuscular Mycorrhization 2) produces 16:0 b-monoacylglycerol, which is exported from the root cells across the peri-arbuscular membrane (Bravo, Brands, Wewer, Dormann, & Harrison, 2017). The M. truncatula AP2/ERF family transcription factor MtWRI5a binds to STR and other AMF-specific gene promoters (such as MtPT4 ) to promote lipid and Pi transport from host-to-AMF and AMF-to-host, respectively (Y. Jiang et al., 2018). The CBX1 (CTTC Motif-Binding Transcription Factor 1; a WRI1 homolog), which is enriched in AMF-regulated genes, activates L. japonicus LjPT4and lipid-metabolism genes (Xue et al., 2018). The riceOsadk1 -defective mutants have low expression of RAM1 andWRI5 and produce fewer arbuscules (Shi et al., 2022). These findings suggest that MtWRI5a, LjCBX1, and OsADK1 are master regulators of bidirectional nutrient transport.