Plant embryogenesis from zygotic genome activation to seed maturation: Comparative mechanisms and engineering opportunities.

Abstract

Plant embryogenesis converts a zygote into a patterned, maturation-competent embryo. Since the major syntheses published in 2019 and 2021, allele-resolved transcriptomics, single-cell and spatial profiling, and three-dimensional imaging have revealed substantial variation in zygotic genome activation and cleavage geometry across angiosperms, challenging models derived solely from Arabidopsis. Here, we organize recent advances along a comparative zygote-to-seed trajectory and ask how conserved regulatory modules are redeployed across lineages, how early patterning is coupled to seed maturation, and which developmental transitions can be engineered in crops. We first compare the maternal-to-zygotic transition and associated chromatin-state changes, explicitly distinguishing observations from hypotheses about their evolutionary drivers. We then examine how PIN-FORMED (PIN)-dependent auxin transport, local auxin biosynthesis, membrane and peptide signaling, and WUSCHEL-RELATED HOMEOBOX (WOX)-family transcription factors establish embryonic axes and meristems. Next, we connect these early programs to source-sink relations, nutrient partitioning, proteostasis, and hormone-redox control during seed maturation, while separating maturation from dormancy release and germination. Finally, we assess how spatial multi-omics, live imaging, CRISPR activation, and synthetic apomixis can interrogate or engineer these transitions. This framework identifies conserved modules, lineage-specific solutions, and major evidence gaps that must be resolved before embryogenesis can be predictably manipulated for crop improvement.