Regulatory Divergence Underlying Mangrove Adaptation: Chromatin Accessibility and Transcriptional Resource Allocation in Extreme Environments

Mangroves provide a unique model for understanding plant adaptation to intertidal stressors, yet the regulatory mechanisms underlying their adaptive evolution remain largely unexplored. Here, we generated genome-wide chromatin accessibility landscapes for two mangrove species ( Bruguiera gymnorhiza and Kandelia obovata ) using ATAC-seq and performed comparative analysis with rice ( Oryza sativa ). Mangroves exhibited significantly higher transcription factor binding site (TFBS) densities—particularly for stress-responsive families such as MYB, WRKY , and NAC , indicating enhanced regulatory complexity. Integration with transcriptomic data revealed a mangrove-specific resource allocation strategy: highly accessible and highly expressed (HA-HE) loci were strongly enriched for salt and osmotic stress responses functions, whereas in rice these active regions were prioritized growth-related genes. Furthermore, under salt stress, mangroves predominantly upregulated HA-HE genes (4.3-fold up/down ratio in B. gymnorhiza ), while rice generally downregulated these loci. Convergent evolutionary analysis of 18 species identified conserved non-coding elements (CNEs) gained/retained in mangrove lineages, associated with key stress-related genes ( CYSD1, GLIP1, bZIP53 ). Together, these results demonstrate that mangroves achieve adaptation through: (i) regulatory network expansion via heightened TFBS density, (ii) preferential allocation of accessible chromatin to stress-responsive programs, and (iii) convergent evolution of non-coding regulatory elements. Our study unveils cis -regulatory innovations underlying mangrove resilience and provides a framework for decoding adaptive evolution in extreme environments.