Abstract

Epigenetic regulation has played a fundamental role in the evolution of plant reproduction. Across more than a billion years, ancestral genome-defense mechanisms in early eukaryotes were progressively expanded, diversified, and repurposed throughout the green lineage. Streptophyte algae assembled the first plant-specific methylation and small RNA systems, providing pre-adaptations for terrestrial reproduction. In bryophytes and early vascular plants, these systems became integrated into gametophyte development, sporogenesis, and meiotic genome protection. Seed plants experienced substantial diversification and expansion of chromatin regulators and small RNA machinery, enabling increasingly sophisticated control of cone, ovule, and embryo development. Angiosperms underwent the most dramatic rewiring of epigenetic pathways, including gene-family diversification, subfunctionalization, and the emergence of genomic imprinting, endosperm-specific demethylation, and lineage-specific reproductive small RNAs such as phasiRNAs. Convergent solutions, including imprinting, meiotic transposable element (TE) silencing, and TE-derived regulatory elements, arose independently across lineages. Rather than reflecting the emergence of entirely new molecular machinery, these innovations illustrate repeated functional co-option and regulatory rewiring of deeply conserved epigenetic modules. Ecological and life-history pressures further shaped epigenetic diversification, linking environmental stress, mating systems, and domestication to reproductive epigenetic plasticity. Recent evidence further demonstrates that epigenetic plasticity underlies the recurrent evolution of alternative reproductive strategies such as apomixis and contributes to reproductive responses to environmental stress. Advances in comparative epigenomics, single-cell technologies, and epigenome editing are now providing unprecedented opportunities to reconstruct the evolutionary history of reproductive epigenetic pathways and to harness them for crop improvement. Together, these findings reveal epigenetic regulation as a dynamic, modular, and deeply evolvable framework that has repeatedly enabled reproductive innovation throughout plant evolution.

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