Chromatin reprogramming and transcriptional regulation orchestrate embryogenesis in hexaploid wheat

Embryogenesis represents the beginning of life cycle, but our understanding of the regulatory circuitry in plants is far lagged to animals. Here, we draw a transcriptome trajectory and chromatin landscape profile during embryogenesis of most cultivated crop hexaploid wheat, highlighting large-scale chromatin reconfiguration and distinct proximal and distal transcriptional regulation in defining cell fate transition. Upon fertilization, H3K27ac and H3K4me3 resetting were correlated with maternal genome silence, while de novo building of chromatin accessibility activated zygotic genome. Global depletion of H3K27me3 in pre-embryo results in a permissive chromatin environment with gain-of-chromatin accessibility, allowing subsequent hierarchical cis- and trans-regulation network mediated by key factors, such as LEC1, MYB, ZHD, LEC2, governing embryo pattern formation. By contrast, H3K27me3 restoration coordinating with chromatin compaction in developmental genes attenuated totipotency and prohibited extensive organogenesis during embryo maturation. In addition, dynamic biased expression of homeolog triads and diverse expression profiles after polyploidization were observed. This is correlated with asymmetric transposon elements insertion in accessible proximal and distal regions. Thus, our study revealed a plant-specific chromatin reprogramming process in facilitating the hierarchical transcription regulation circuits mediated "inverse hourglass model" and unveiled epigenetic regulation of evolutionary divergence among different sub-genome in shaping embryogenesis in polyploidy wheat.