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Abstract Desiccation tolerance has evolved recurrently in grasses using two unique strategies of either protecting or dismantling the photosynthetic apparatus to minimize photooxidative damage under life without water (anhydrobiosis). Here, we surveyed chromatin architecture and gene expression during desiccation in two closely related grasses with distinguishing desiccation tolerance strategies to identify regulatory dynamics underlying these unique adaptations. 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. This includes many genes with binding sites for the core seed development transcription factor ABI5, supporting the long‐standing hypothesis that vegetative desiccation tolerance evolved from rewiring seed pathways.Oropetium thomaeumhas a unique set of desiccation induced genes and regulatory elements associated with photoprotection, pigment biosynthesis, and response to high light, reflecting its adaptation of protecting the photosynthetic apparatus under desiccation (homoiochlorophyly). By contrast,Eragrostis nindensishas unique accessible and expressed genes related to chlorophyll catabolism, scavenging of amino acids, and hypoxia, highlighting its poikilochlorophyllous adaptations of dismantling the photosynthetic apparatus and degrading chlorophyll under desiccation. Together, our results highlight the complex regulatory and expression dynamics underlying desiccation tolerance in grasses.
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Core cellular and tissue‐specific mechanisms enable desiccation tolerance in Craterostigma
SUMMARY Resurrection plants can survive prolonged life without water (anhydrobiosis) in regions with seasonal drying. This desiccation tolerance requires the coordination of numerous cellular processes across space and time, and individual plant tissues face unique constraints related to their function. Here, we analyzed the complex, octoploid genome of the model resurrection plantCraterostigma(C. plantagineum), and surveyed spatial and temporal expression dynamics to identify genetic elements underlying desiccation tolerance. Homeologous genes within theCraterostigmagenome have divergent expression profiles, suggesting the subgenomes contribute differently to desiccation tolerance traits. TheCraterostigmagenome contains almost 200 tandemly duplicated early light‐induced proteins, a hallmark trait of desiccation tolerance, with massive upregulation under water deficit. We identified a core network of desiccation‐responsive genes across all tissues, but observed almost entirely unique expression dynamics in each tissue during recovery. Roots and leaves have differential responses related to light and photoprotection, autophagy and nutrient transport, reflecting their divergent functions. Our findings highlight a universal set of likely ancestral desiccation tolerance mechanisms to protect cellular macromolecules under anhydrobiosis, with secondary adaptations related to tissue function.
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- PAR ID:
- 10405961
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- The Plant Journal
- Volume:
- 114
- Issue:
- 2
- ISSN:
- 0960-7412
- Page Range / eLocation ID:
- p. 231-245
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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