Genome-Wide Analysis of Nutrient Signaling Pathways Conserved in Arbuscular Mycorrhizal Fungi

Abstract

Arbuscular mycorrhizal (AM) fungi form a mutualistic symbiosis with a majority of terrestrial vascular plants. To achieve an efficient nutrient trade with their hosts, AM fungi sense external and internal nutrients, and integrate different hierarchic regulations to optimize nutrient acquisition and homeostasis during mycorrhization. However, the underlying molecular networks in AM fungi orchestrating the nutrient sensing and signaling remain elusive. Based on homology search, we here found that at least 72 gene components involved in four nutrient sensing and signaling pathways, including cAMP-dependent protein kinase A (cAMP-PKA), sucrose non-fermenting 1 (SNF1) protein kinase, target of rapamycin kinase (TOR) and phosphate (PHO) signaling cascades, are well conserved in AM fungi. Based on the knowledge known in model yeast and filamentous fungi, we outlined the possible gene networks functioning in AM fungi. These pathways may regulate the expression of downstream genes involved in nutrient transport, lipid metabolism, trehalase activity, stress resistance and autophagy. The RNA-seq analysis and qRT-PCR results of some core genes further indicate that these pathways may play important roles in spore germination, appressorium formation, arbuscule longevity and sporulation of AM fungi. We hope to inspire further studies on the roles of these candidate genes involved in these nutrient sensing and signaling pathways in AM fungi and AM symbiosis.

A SPX domain‐containing phosphate transporter from Rhizophagus irregularis handles phosphate homeostasis at symbiotic interface of arbuscular mycorrhizas

“…The processes of Pi delivery from the arbuscules (or intraradical hyphae) to the periarbuscular space (PAS) (or apoplast) via the specialized transport systems occur in the endomembranes and plasma membranes (PMs) of arbuscules and intraradical hyphae (Ezawa & Saito, 2018; Zhou et al ., 2021). However, the underlying mechanism by which Pi is transported from the fungus to the plant is largely unknown.…”

“…These AM fungal PTs are responsible for absorbing Pi from soil, after which Pi is polymerized into polyphosphate (polyP) through the vacuolar transporter chaperone (VTC) complex in the ERM and transported by the vacuoles (Uetake et al ., 2002; Kikuchi et al ., 2014). Within the IRM, AM fungal exopolyphosphatases Ppx1 and Ppn1 can hydrolyze polyP into inorganic Pi, which is effluxed from the vacuole into the cytoplasm by the unidentified Pi exporter (Aono et al ., 2004; Ohtomo & Saito, 2005; Ezawa & Saito, 2018; Zhou et al ., 2021).…”

A transcriptional activator from Rhizophagus irregularis regulates phosphate uptake and homeostasis in AM symbiosis during phosphorous starvation

“…The Pi transport systems in AMF is very similar to that of Saccharomyces cerevisiae, which is well-known to contain the high-affinity system Pho84p and Pho89p and the low-affinity system Pho87p, Pho90p, and Pho91p (Auesukaree et al, 2003). This suggests that there exists a conserved PHOSPHATE (PHO) signaling pathway between AMF and yeasts (Aono et al, 2004;Olsson et al, 2006;Kikuchi et al, 2014;Zhou et al, 2021).…”

“…It has been shown that there is a specialized Pi export system in the arbuscules, where free Pi is transported and unloaded into the periarbuscular space (PAS) (Ezawa and Saito, 2018;Zhou et al, 2021;Xie et al, 2022). After the Poly-P hydrolyzation in the IRM and arbuscules, the Pi transporters containing SPX (SYG1/Pho81/XPR1) domains participate in the Pi export process at the symbiotic interface, releasing Pi into the PAS (Ezawa and Saito, 2018;Plassard et al, 2019;Xie et al, 2022).…”

“…In two previous studies, only a few TFs, such as RiMsn2 from R. irregularis and GintSTE from Glomus intraradices (currently R. irregularis) are preliminarily investigated (Tollot et al, 2009;Sun et al, 2018), while the key transcriptional regulators engaged in Pi absorption and homeostasis have not been explored in AMF. Some recent studies have shown that there exists the bHLH domain-containing transcription factors encoding genes involved in the PHO pathway in response to low Pi conditions in G. margarita, Gigaspora rosea and R. irregularis (Tang et al, 2016;Xie et al, 2016Xie et al, , 2022Zhou et al, 2021). It is well-known that in S. cerevisiae, the AMF bHLH ortholog ScPho4 is the transcription factor regulating the PHO pathway to control Pi absorption and homeostasis (Lenburg and O'Shea, 1996;Auesukaree et al, 2004;Wykoff et al, 2007).…”