Role of Cell Wall Polyphosphates in Phosphorus Transfer at the Arbuscular Interface in Mycorrhizas

Abstract

Arbuscular mycorrhizal fungi provide plants with soil mineral nutrients, particularly phosphorus. In this symbiotic association, the arbuscular interface is the main site for nutrient exchange. To understand phosphorus transfer at the interface, we analyzed the subcellular localization of polyphosphate (polyP) in mature arbuscules of Rhizophagus irregularis colonizing roots of Lotus japonicus wild-type (WT) and H⁺-ATPase ha1-1 mutant, which is defective in phosphorus acquisition through the mycorrhizal pathway. In both, the WT and the ha1-1 mutant, polyP accumulated in the cell walls of trunk hyphae and inside fine branch modules close to the trunk hyphae. However, many fine branches lacked polyP. In the mutant, most fine branch modules showed polyP signals compared to the WT. Notably, polyP was also observed in the cell walls of some fine branches formed in the ha1-1 mutant, indicating phosphorus release from fungal cells to the apoplastic regions. Intense acid phosphatase (ACP) activity was detected in the periarbuscular spaces around the fine branches. Furthermore, double staining of ACP activity and polyP revealed that these had contrasting distribution patterns in arbuscules. These observations suggest that polyP in fungal cell walls and apoplastic phosphatases may play an important role in phosphorus transfer at the symbiotic interface in arbuscules.

Keywords: H+-ATPase; acid phosphatase; arbuscular mycorrhizal fungi; arbuscule; cell wall; periarbuscular space; polyphosphate; two-compartment system.