A multi-omics atlas reveals a zf-C2H2-dominated regulatory hub governing embryonic development in Periplaneta...

The embryo of Periplaneta americana L. is a promising yet underexplored medicinal resource compared to adult insects. Here, we present the first integrated multi-omics atlas of embryonic development across its 28-day cycle, combining morphological analysis with lipidomics, metabolomics, peptidomics, and transcriptomics profiling at five key stages (Days 0, 7, 14, 21, and 28). We delineate a tri-phasic metabolic reprogramming trajectory: maternal reserves catabolism (Days 0-7) supports proliferation; metabolic complexification (Days 7-21) underpins organogenesis; and free fatty acids upregulation (e.g., oleic acid increased by 399.44%, FDR < 0.05) fuel eclosion (Days 21-28). Using database searching, de novo sequencing, and maternal filtering, we show that Maternal peptides dominated early development (99.9% at Day 0) and declined to 77.8% by Day 28, whereas embryo-specific peptides increased from 5 to 2959, indicating a dynamically structured embryonic peptidome. The zf C2H2 family (70.16% of detected transcription factors) orchestrates development via an "initiation-maintenance-execution" strategy, integrating metabolism, peptide biosynthesis, and immunity. Multi-omics integration identifies Days 14-21 as the optimal harvesting window, defined by metabolic stability and enriched bioactive lipids/peptides. This study establishes a molecular blueprint for Periplaneta americana embryogenesis and provides a rational framework for its development as a standardized insect-derived medicinal resource.