The hologenomic stress legacy: A framework for soil as a transgenerational memory bank of plant immunity

Plants pass transgenerational inheritance through genetic and epigenetic information; however, the soil's role as the host environment in this memory transfer remains largely unexplored. Research within this field has largely been domain-specific, with only 117 publications in 24 years integrating fields of soil persistent metabolites (soil chemistry), stress-induced microbial consortia (soil microbiology), and plant molecular science (plant epigenetics). In this perspective article, we synthesize evidence and propose a testable hypothesis, the Hologenomic Stress Legacy (HSL) hypothesis. It states that the soil is an active information-storing center containing biochemical and microbial vectors, persistent metabolites and microbiota, that mediate the transfer of immunity information between plant generations. This hypothesis is supported by a scientometric analysis and critical synthesis of literature related to induced priming, transgenerational inheritance, root exudates, microbial-induced priming, and stress-induced microbiota recruitment (published between January 2000-December 2024). The critical synthesis reveals that abiotically/biotically challenged plants send chemical signals to their roots. This alters root exudation, modifies the rhizosphere, and recruits beneficial microorganisms. Accordingly, the HSL framework proposes that this metabolic and microbial "memory" persists in the soil long after the plant's lifecycle, forming a basis for transgenerational priming. We argue that resilience is not just encoded in the plant's genome; it extends to the host environment (the soil) and could potentially be deciphered or engineered for agricultural benefit. Finally, we propose an experimental roadmap to validate this hypothesis, which includes a computational chemistry component (Computational Chemistry Framework for HSL-CCF4H) to help optimize the transfer of this "soil memory" and begin moving from correlational observations to mechanistic causality.