Soil development stage shapes shoot-to-soil carbon flow and organo-mineral association under variable phosphorus supply

Understanding plant–soil–microbe interactions is key to increasing nutrient use efficiency and soil carbon (C) storage. Root exudates play a central role in nutrient acquisition, structure microbial communities and influence organo-mineral association. Yet, how soil development stage and resulting soil chemical properties regulate root exudation and the fate of C in the rhizosphere remain poorly understood.We used a soil–plant–microbe–mineral approach to assess how soil development stage influences plant stoichiometry, rhizosphere C release, microbial activity, and organo-mineral associations. In a growth chamber, we grew Lupinus albus, a model species for phosphorus (P) acquisition, for 30 days under three P levels (5, 15, and 40 mg P kg⁻¹) in three podzolic horizons representing contrasting soil development stages: an organic matter- and quartz-rich Ae, an iron (Fe) and aluminum (Al) oxide-rich Bh, and a primary silicate-dominated BC. Plant-derived C transfer to the rhizosphere, microbes, and reactive iron oxides was traced using a 13C-CO₂ pulse-labeling experiment, with Fe-oxide mesh bags used to assess newly stabilized organo-mineral C. We measured plant biomass, shoot stoichiometry, rhizosphere metabolites, microbial biomass, and enzyme activities.Soil development stage strongly influenced shoot response to P supply and the fate of root-derived C. Shoot biomass was highest and insensitive to P supply in the primary mineral-rich BC, while it was lowest and responding to P supply in the Bh horizon, due to P sorption onto Fe and Al oxides. While dissolved rhizosphere organic C was similar, the metabolomic profile of rhizosphere solutions and microbial parameters varied markedly among soil horizons. 13C recovery in the rhizosphere varied strongly between soil horizons and P levels, reflecting interactions between mineral sorption capacity, metabolomic profiles and microbial activity. In the Ae horizon, high microbial biomass likely enhanced microbial processing of root-derived ¹³C, whereas in the Bh horizon, lower microbial biomass combined with high Fe and Al oxide content likely favored greater adsorption of 13C onto reactive minerals. Iron oxides in mesh bags showed pronounced, horizon-specific capacity to stabilize C, peaking in Bh, followed by Ae and BC.Overall, soil development stage and resulting chemical and mineralogical properties tightly control plant P responses and the fate of C in the rhizosphere. These results highlight the tight coupling of plants, microbes, and minerals, and underscore the importance of soil genesis and integrative approaches for tracing the fate of photosynthates in soil–plant systems. Extending these findings to agroecosystems will require further validation though field trials.