Regulatory dynamics distinguishing desiccation tolerance strategies within resurrection grasses

Abstract

Desiccation tolerance has evolved recurrently in grasses using two unique strategies to mitigate photooxidative damage under anhydrobiosis. The grass Oropetium thomaeum protects and retains chlorophyll, thylakoids, and the photosynthetic apparatus during desiccation (Homoiochlorophyly), while Eragrostis nindensis degrades and resynthesizes these components under desiccation and rehydration (Poikilochlorophyly). Here, we surveyed chromatin architecture and gene expression during desiccation in these two closely related species to identify regulatory dynamics underlying the distinct desiccation tolerance strategies in grasses. In both grasses, we observed a strong association between nearby chromatin accessibility and gene expression in desiccated tissues compared to well-watered, reflecting an unusual chromatin stability under anhydrobiosis. Integration of chromatin accessibility (ATACseq) and expression data (RNAseq) revealed a core desiccation response across these two grasses including many genes with binding sites for the core seed development transcription factor ABI5. O. thomaeum had a unique set of desiccation induced genes and regulatory elements associated with photoprotection, pigment biosynthesis, and response to high light, reflecting its adaptation of homoiochlorophyly. A tandem array of early light induced proteins (ELIPs) had massive shifts in gene expression and chromatin openness under desiccation in only O. thomaeum, and ELIPs acquired a novel desiccation related cis-regulatory motif, reflecting regulatory neofunctionalization during the evolution of desiccation tolerance. Together, our results highlight the complex regulatory and expression dynamics underlying desiccation tolerance in grasses.