Plant-derived carbon (C) is a critical constituent of particulate organic carbon (POC) and plays an essential role in soil organic carbon (SOC) sequestration. Yet, how arbuscular mycorrhizal fungi (AMF) control the contribution of plant-derived C to SOC storage through two processes (biosynthesis of plant biopolymers and soil metabolism) remains poorly understood. Here, we utilized transcriptome analysis to examine the effects of AMF on P. communis roots. Under the AM symbiosis, root morphological growth and tolerance to stress were strengthened, and the biosynthetic pathways of key plant biopolymers (long-chain fatty acids, cutin, suberin, and lignin) contributing to the plant-derived C were enhanced. In the subsequent metabolic processes, AMF increased soil metabolites contributing to plant-derived C (such as syringic acid) and altered soil metabolic pathways, including carbohydrate metabolism. Additionally, C-acquiring soil extracellular enzyme activities were enhanced by AMF, which could affect the stabilization of plant-derived C in soil. The contents of POC (21.71 g kg−1 soil), MAOC (10.75 g kg−1 soil), and TOC (32.47 g kg−1 soil) in soil were significantly increased by AMF. The concentrations of plant-derived C and microbial-derived C were quantified based on biomarker analysis. AMF enhanced the content of plant-derived C in both POC and MAOC fractions. What's more, plant-derived C presented the highest level in the POC fraction under the AMF treatment. This research broadens our understanding of the mechanism through which plant-derived C contributes to the accumulation of POC and SOC induced by AM symbiosis, and evidences the benefits of AMF application in SOC sequestration.