Beyond phosphate uptake: PT4/PT11 as key functional components linking phosphate acquisition, nutrient exchange, and arbuscule maintenance in arbuscular mycorrhizal symbiosis.

Phosphorus is an essential macronutrient for plant growth and development, yet its availability in many soils is limited by strong chemical fixation and low mobility. Arbuscular mycorrhizal (AM) symbiosis provides an important biological strategy for improving plant phosphate acquisition by establishing specialized arbuscules within root cortical cells, where reciprocal nutrient exchange occurs across the periarbuscular membrane (PAM). Among the phosphate transporter families involved in this process, the mycorrhiza-specific PHT1 transporters PT4 in Medicago truncatula and PT11 in Oryza sativa are major components of the mycorrhizal phosphate uptake pathway and are required for efficient phosphate acquisition and the maintenance of functional arbuscules. Genetic and physiological studies further indicate that disruption of PT4/PT11-mediated phosphate transport is closely associated with premature arbuscule degeneration and impaired symbiotic performance, highlighting a functional link between phosphate uptake, nutrient exchange, and arbuscule maintenance. In this review, we summarize current knowledge of the molecular mechanisms underlying PT4/PT11 function and regulation during AM symbiosis. We first compare mycorrhiza-specific phosphate transporters across plant species and discuss their localization, transport properties, and contributions to the mycorrhizal Pi uptake pathway. We then examine the multilayered regulatory network controlling PT4/PT11 expression, including the common symbiosis signaling pathway, calcium-dependent signaling, CYCLOPS-RAM1-centered transcriptional regulation, AP2/ERF-family regulators, hormone-associated regulation, and systemic phosphate-sensing pathways. Particular attention is given to the functional coupling between PT4/PT11-mediated phosphate uptake and other components of reciprocal nutrient exchange, including carbon and lipid transfer, proton extrusion, and arbuscule maintenance. We further discuss how impairment of phosphate transport through PT4/PT11 affects arbuscule integrity and the physiological conditions of the plant-fungus interface. Based on available genetic and physiological evidence, we propose a working model in which PT4/PT11-mediated phosphate uptake contributes to maintaining a favorable interfacial phosphate environment and efficient nutrient exchange, thereby supporting arbuscule function and longevity. Importantly, current evidence does not demonstrate that PT4/PT11 possess a transport-independent function or directly transmit signals through interactions with downstream signaling components. The mechanisms linking transporter activity, local phosphate status, nutrient exchange, and arbuscule maintenance therefore remain to be experimentally resolved. Finally, we highlight emerging approaches, including single-cell and spatial transcriptomics, proximity labeling, transport-defective mutants, and genome editing, that may distinguish transport-dependent from potential transport-independent functions of PT4/PT11. Understanding these mechanisms may provide a conceptual and practical foundation for exploiting AM symbiosis to improve phosphorus-use efficiency, reduce dependence on mineral phosphate fertilizers, and develop more sustainable crop production systems.