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.
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 plant
- Award ID(s):
- 2213983
- 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
More Like this
-
Abstract Oropetium thomaeum has 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 nindensis has 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. -
Summary Desiccation‐tolerant (DT) plants can dry past −100 MPa and subsequently recover function upon rehydration. Vascular DT plants face the unique challenges of desiccating and rehydrating complex tissues without causing structural damage. However, these dynamics have not been studied in intact DT plants.
We used high resolution micro‐computed tomography (microCT), light microscopy, and fluorescence microscopy to characterize the dynamics of tissue desiccation and rehydration in petioles (stipes) of intact DT ferns.
During desiccation, xylem conduits in stipes embolized before cellular dehydration of living tissues within the vascular cylinder. During resurrection, the chlorenchyma and phloem within the stipe vascular cylinder rehydrated before xylem refilling. We identified unique stipe traits that may facilitate desiccation and resurrection of the vascular system, including xylem conduits containing pectin (which may confer flexibility and wettability); chloroplasts within the vascular cylinder; and an endodermal layer impregnated with hydrophobic substances that impede apoplastic leakage while facilitating the upward flow of water within the vascular cylinder.
Resurrection ferns are a novel system for studying extreme dehydration recovery and embolism repair in the petioles of intact plants. The unique anatomical traits identified here may contribute to the spatial and temporal dynamics of water movement observed during desiccation and resurrection.
-
Abstract Desiccation-tolerant (DT) organisms can lose nearly all their water without dying. Desiccation tolerance allows organisms to survive in a nearly completely dehydrated, dormant state. At the cellular level, sugars and proteins stabilize cellular components and protect them from oxidative damage. However, there are few studies of the dynamics and drivers of whole-plant recovery in vascular DT plants. In vascular DT plants, whole-plant desiccation recovery (resurrection) depends not only on cellular rehydration, but also on the recovery of organs with unequal access to water. In this study, in situ natural and artificial irrigation experiments revealed the dynamics of desiccation recovery in two DT fern species. Organ-specific irrigation experiments revealed that the entire plant resurrected when water was supplied to roots, but leaf hydration alone (foliar water uptake) was insufficient to rehydrate the stele and roots. In both species, pressure applied to petioles of excised desiccated fronds resurrected distal leaf tissue, while capillarity alone was insufficient to resurrect distal pinnules. Upon rehydration, sucrose levels in the rhizome and stele dropped dramatically as starch levels rose, consistent with the role of accumulated sucrose as a desiccation protectant. These findings provide insight into traits that facilitate desiccation recovery in dryland ferns associated with chaparral vegetation of southern California.more » « less
-
Abstract Desiccation tolerance evolved recurrently across diverse plant lineages to enable survival in water-limited conditions. Many resurrection plants are polyploid, and several groups have hypothesized that polyploidy contributed to the evolution of desiccation tolerance. However, due to the vast phylogenetic distance between resurrection plant lineages, the rarity of desiccation tolerance, and the prevalence of polyploidy in plants, this hypothesis has been difficult to test. Here, we surveyed natural variation in morphological, reproductive, and desiccation tolerance traits across several cytotypes of a single species to test for links between polyploidy and increased resilience. We sampled multiple natural populations of the resurrection grass Microchloa caffra across an environmental gradient ranging from mesic to xeric in South Africa. We describe two distinct ecotypes of M. caffra that occupy different extremes of the environmental gradient and exhibit consistent differences in ploidy, morphological, reproductive, and desiccation tolerance traits in both field and common growth conditions. Interestingly, plants with more polyploid genomes exhibited consistently higher recovery from desiccation, were less reproductive, and were larger than plants with smaller genomes and lower ploidy. These data indicate that selective pressures in increasingly xeric sites may play a role in maintaining and increasing desiccation tolerance and are mediated by changes in ploidy.
-
Transcriptional divergence of duplicated genes after whole genome duplication (WGD) has been described in many plant lineages and is often associated with subgenome dominance, a genome-wide mechanism. However, it is unknown what underlies the transcriptional divergence of duplicated genes in polyploid species that lack subgenome dominance. Soybean is a paleotetraploid with a WGD that occurred 5 to 13 Mya. Approximately 50% of the duplicated genes retained from this WGD exhibit transcriptional divergence. We developed accessible chromatin region (ACR) datasets from leaf, flower, and seed tissues using MNase-hypersensitivity sequencing. We validated enhancer function of several ACRs associated with known genes using CRISPR/Cas9-mediated genome editing. The ACR datasets were used to examine and correlate the transcriptional patterns of 17,111 pairs of duplicated genes in different tissues. We demonstrate that ACR dynamics are correlated with divergence of both expression level and tissue specificity of individual gene pairs. Gain or loss of flanking ACRs and mutation of
cis -regulatory elements (CREs) within the ACRs can change the balance of the expression level and/or tissue specificity of the duplicated genes. Analysis of DNA sequences associated with ACRs revealed that the extensive sequence rearrangement after the WGD reshaped the CRE landscape, which appears to play a key role in the transcriptional divergence of duplicated genes in soybean. This may represent a general mechanism for transcriptional divergence of duplicated genes in polyploids that lack subgenome dominance.