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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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Gene family rearrangements and transcriptional priming drive the evolution of vegetative desiccation tolerance in Selaginella
SUMMARY Extreme dryness is lethal for nearly all plants, excluding the so‐called resurrection plants, which evolved vegetative desiccation tolerance (VDT) by recruiting genes common in most plants. To better understand the evolution of VDT, we generated chromosome‐level assemblies and improved genome annotations of twoSelaginellaspecies with contrasting abilities to survive desiccation. We identified genomic features and critical mechanisms associated with VDT through sister‐group comparative genomics integrating multi‐omics data. Our findings indicate thatSelaginellaevolved VDT through the expansion of some stress protection‐related gene families and the contraction of senescence‐related genes. Comparative analyses revealed that desiccation‐tolerantSelaginellaspecies employ a combination of constitutive and inducible protection mechanisms to survive desiccation. We show that transcriptional priming of stress tolerance‐related genes and accumulation of flavonoids in unstressed plants are hallmarks of VDT inSelaginella. During water loss, the resurrectionSelaginellainduces phospholipids and glutathione metabolism, responses that are missing in the desiccation‐sensitive species. Additionally, gene regulatory network analyses indicate the suppression of growth processes as a major component of VDT. This study presents novel perspectives on how gene dosage impacts crucial protective mechanisms and the regulation of central processes to survive extreme dehydration.
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- Award ID(s):
- 2243690
- PAR ID:
- 10566529
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- The Plant Journal
- Volume:
- 121
- Issue:
- 1
- ISSN:
- 0960-7412
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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