Convergent innovation of (crypto)vivipary via asymmetric dismantling of seed desiccation and dormancy machinery.
Cryptovivipary and vivipary, referred to as (crypto)vivipary, occur across multiple angiosperm lineages and enable embryos to continue developing before dispersal. Yet, this trait raises a fundamental question: how are seed-specific abscisic acid (ABA) responses modulated to support continuous embryonic growth without compromising ABA-dependent vegetative stress tolerance? Here, integrating phylogenomic analyses of independently evolved (crypto)viviparous lineages with spatiotemporal transcripto
Cryptovivipary and vivipary, referred to as (crypto)vivipary, occur across multiple angiosperm lineages and enable embryos to continue developing before dispersal. Yet, this trait raises a fundamental question: how are seed-specific abscisic acid (ABA) responses modulated to support continuous embryonic growth without compromising ABA-dependent vegetative stress tolerance? Here, integrating phylogenomic analyses of independently evolved (crypto)viviparous lineages with spatiotemporal transcriptomics and functional validation, we show that (crypto)vivipary evolved via a convergent "less-is-more" strategy rather than through novel genes or single master loci (e.g., DOG1 ). While upstream hormonal cores (e.g., ABA/GA signaling) are largely conserved, downstream seed desiccation and dormancy effectors are asymmetrically dismantled across cryptoviviparous and viviparous lineages. This remodeling, encompassing 38 shared contracted orthogroups and hundreds of lineage-specific losses, converges on eliminating the execution machinery for seed desiccation tolerance and dormancy maintenance. Consistently, orthologs of the contracted genes are enriched for dry-seed-specific expression and ABA responsiveness in non-(crypto)viviparous species. Furthermore, disrupting representative Arabidopsis orthologs (e.g., SESA1 , TIP3.2 , LEA25 , ECP63 ) recapitulates (crypto)viviparous-like phenotypes, including precocious germination, elevated seed moisture, and in most mutants, compromised storage longevity. Together, our findings demonstrate how structured contraction of terminal seed-specific modules uncouples seed developmental fate from systemic stress signaling, illuminating the molecular architecture of (crypto)vivipary.
