The good, the bad, and the phosphate: regulation of beneficial and detrimental plant–microbe interactions by the plant phosphate status

Abstract

Phosphate (P i ) is indispensable for life on this planet. However, for sessile land plants it is poorly accessible. Therefore, plants have developed a variety of strategies for enhanced acquisition and recycling of P i . The mechanisms to cope with P i limitation as well as direct uptake of P i from the substrate via the root epidermis are regulated by a conserved P i starvation response (PSR) system based on a family of key transcription factors (TFs) and their inhibitors. Furthermore, plants obtain P i indirectly through symbiosis with mycorrhiza fungi, which employ their extensive hyphal network to drastically increase the soil volume that can be explored by plants for P i . Besides mycorrhizal symbiosis, there is also a variety of other interactions with epiphytic, endophytic, and rhizospheric microbes that can indirectly or directly influence plant P i uptake. It was recently discovered that the PSR pathway is involved in the regulation of genes that promote formation and maintenance of AM symbiosis. Furthermore, the PSR system influences plant immunity and can also be a target of microbial manipulation. It is known for decades that the nutritional status of plants influences the outcome of plant-microbe interactions. The first molecular explanations for these observations are now emerging.

Testing the trade‐balance model: resource stoichiometry does not sufficiently explain AM effects

“…3a,b). Mycorrhiza establishment has been recently found to be regulated by the plant P starvation response system, namely in rice, which was considered to have closed a major knowledge gap on how AM symbiosis is promoted at low and suppressed at high P conditions (Paries & Gutjahr, 2023). This finding has multiple connections with the present results.…”

Unlocking the Mycorrhizal Nitrogen Pathway Puzzle: Metabolic Modelling and multi-omics unveil Pyrimidines’ Role in Maize Nutrition via Arbuscular Mycorrhizal Fungi Amidst Nitrogen Scarcity

“…The integration of maize and fungal RNAseq and metabolome analyses has allowed us to construct a simplified model depicting the various biological events occurring in the symbiotic association (Figure 10). As fungal arbuscules are known to undergo controlled senescence (Choi et al ., 2018; Paries and Gutjahr, 2023), our data suggest that autophagy is upregulated in both maize genotypes under both HN and LN conditions, with higher expression in Lo3 LN roots. Autophagy likely contributes to the degradation of fungal cellular products, potentially releasing nucleosides.…”

“…Fungal arbuscules are known to undergo controlled senescence (Choi et al, 2018;Paries and Gutjahr, 2023), our data suggest that autophagy is upregulated in maize roots, with higher expression in Lo3 LN roots (Supplementary Table 9). Autophagy likely contributes to the degradation of fungal cellular products, potentially releasing nucleosides.…”

“…It is well established that mycorrhizae play a pivotal role in the improvement of plant P nutrition and uptake (Choi et al ., 2018; Plassard et al ., 2019; Paries and Gutjahr, 2023). To determine if the amount of N supplied to the plant and the presence of R. irregularis modify B73 and Lo3 phosphate content, total P content (TPC) was measured by the molybdate blue method.…”

“…It is well established that phosphorus (P) deficiency is the main driver for the establishment of mycorrhizal symbiotic associations (Breuillin et al ., 2010; Smith et al ., 2011; Balzergue et al ., 2013; Wang et al ., 2017; Paries and Gutjahr, 2023). Phosphorus deficiency triggers exudation from roots of signaling molecules such as strigolactones that stimulate AMF hyphal branching (Lanfranco et al ., 2018; Hull et al ., 2021).…”