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.