Abstract:Objective To unravel the mechanism underlying the high-yield performance of hybrid pepper (Capsicum annuum L.) progenies and dissect parent-progeny differences across four interconnected dimensions: plant nutrient accumulation, rhizosphere soil physicochemical properties, microbial community composition, and nutrient metabolism-related functional genes.Methods For both parental lines and their hybrid progenies, the yields and the content of nitrogen (N), phosphorus (P), and potassium (K) in roots, fruits, and rhizosphere soil were determined, alongside rhizosphere soil physicochemical properties. High-throughput sequencing was adopted to analyze the structures of root endophytic and rhizosphere microbial communities, while metagenomic sequencing was used to quantify the abundance differences of genes associated with rhizosphere nutrient metabolism.Results Hybrid progenies exhibited a significant yield increase, with the highest yield increase observed in the Z3 line. All hybrids showed elevated K content in fruits, and Z3 specifically achieved transgressive accumulation of N and P in roots. A distinct turnover of the root endophytic microbial community was detected between parents and progenies. In the hybrids, functional genera including Dyella, Burkholderia-Caballeronia-Paraburkholderia, and Trichoderma were enriched, which were significantly correlated with plant nutrient uptake. In terms of rhizosphere soil properties, all hybrids had higher available phosphorus content and lower rhizosphere pH than parental lines. Notably, Z3 possessed unique advantages of high total nitrogen reserve and increased organic matter content in the rhizosphere. Additionally, the abundance of genes related to P and K metabolism was higher in hybrids than in parents, which was particularly prominent in Z3.Conclusion The transgressive yields of pepper hybrids is driven by the synergy among the rhizosphere environment, microbial communities, and the host plant. Specifically, hybrid progenies constructed an efficient microecosystem by enriching functional microbes (e.g., Dyella) and enhanced nutrient metabolism efficiency through increased abundance of P and K metabolism-related genes. These improvements ultimately led to the formation of nutrient utilization advantages, characterized by efficient nutrient absorption in roots and effective nutrient translocation to fruits. This study provides a novel theoretical framework for deciphering the microbial-driven mechanisms underlying parent-progeny differences in nutrient use efficiency of crops and further enriches the theory of plant-microbe-soil interactions.