A FUS3-VAL transcriptional negative feedback circuit terminates seed maturation program and safeguards vegetative development

The transition from seed to seedling in plants requires the precise termination of the embryonic program, yet the molecular mechanism ensuring its irreversible silencing remain a fundamental question. Here, we identify a central regulatory module in which the B3-domain transcription factors FUS3 (an activator) and VAL1/VAL2 (repressors) engage in antagonistic control over this developmental switch. We demonstrate that VAL1/VAL2 directly bind to RY elements in the FUS3 promoter, recruiting Polycomb Repressive Complex 2 (PRC2) to deposit H3K27me3 and epigenetically silence FUS3 in seedlings. Loss of FUS3 completely rescues the embryonic seedling and somatic embryogenesis phenotypes of val1 val2 mutants, establishing FUS3 as the key effector. Conversely, ectopic FUS3 expression is sufficient to recapitulate the val1 val2 phenotype, activating the LAFL network and inducing totipotency. Notably, VAL1/VAL2 and FUS3 co-occupy a shared set of genomic targets via identical RY motifs, yet exert opposing transcriptional outcomes, implementing a "shared-site, antagonistic-function" logic. Furthermore, a self-reinforcing negative feedback loop is uncovered: FUS3 activates VAL1 expression during seed development, which in turn primes the repression of FUS3 itself after late seed maturation. This FUS3-VAL regulatory circuit functions as a molecular switch that locks in the vegetative state, providing a robust mechanism for terminating embryonic identity and ensuring unidirectional developmental progression.