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.
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High‐resolution computed tomography reveals dynamics of desiccation and rehydration in fern petioles of a desiccation‐tolerant fern
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.
- Award ID(s):
- 1258186
- NSF-PAR ID:
- 10460038
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- New Phytologist
- Volume:
- 224
- Issue:
- 1
- ISSN:
- 0028-646X
- Page Range / eLocation ID:
- p. 97-105
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Summary Different methods of measuring cavitation resistance in fern petioles lead to variable results, particularly with respect to the P50metric. We hypothesised that the fern dictyostele structure affects air entry into the xylem, and therefore impacts the shape of the vulnerability curve.
Our study examined this variation by comparing vulnerability curves constructed on petioles collected from evergreen and deciduous ferns in the field, with curves generated using the standard centrifuge, air‐injection and bench‐top dehydration methods. Additional experiments complemented the vulnerability curves to better understand how anatomy shapes estimates of cavitation resistance.
Centrifugation and radial air injection generated acceptable vulnerability curves for the deciduous species, but overestimated drought resistance in the two evergreen ferns. In these hardy plants, axial air injection and bench‐top dehydration produced results that most closely aligned with observations in nature. Additional experiments revealed that the dictyostele anatomy impedes air entry into the xylem during spinning and radial air injection.
Each method produced acceptable vulnerability curves, depending on the species being tested. Therefore, we stress the importance of validating the curves with
in situ measures of water potential and, if possible, hydraulic data to generate realistic results with any of the methods currently available. -
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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 plant
Craterostigma (C. plantagineum ), and surveyed spatial and temporal expression dynamics to identify genetic elements underlying desiccation tolerance. Homeologous genes within theCraterostigma genome have divergent expression profiles, suggesting the subgenomes contribute differently to desiccation tolerance traits. TheCraterostigma genome 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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Summary The hydraulic system of vascular plants and its integrity is essential for plant survival. To transport water under tension, the walls of xylem conduits must approximate rigid pipes. Against this expectation, conduit deformation has been reported in the leaves of a few species and hypothesized to function as a ‘circuit breaker’ against embolism. Experimental evidence is lacking, and its generality is unknown.
We demonstrated the role of conduit deformation in protecting the upstream xylem from embolism through experiments on three species and surveyed a diverse selection of vascular plants for conduit deformation in leaves.
Conduit deformation in minor veins occurred before embolism during slow dehydration. When leaves were exposed to transient increases in transpiration, conduit deformation was accompanied by large water potential differences from leaf to stem and minimal embolism in the upstream xylem. In the three species tested, collapsible vein endings provided clear protection of upstream xylem from embolism during transient increases in transpiration.
We found conduit deformation in diverse vascular plants, including 11 eudicots, ginkgo, a cycad, a fern, a bamboo, and a grass species, but not in two bamboo and a palm species, demonstrating that the potential for ‘circuit breaker’ functionality may be widespread across vascular plants.
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PREMISE Desiccation tolerance (DT) is a widespread phenomenon among land plants, and variable ecological strategies for DT are likely to exist. Using
Syntrichia caninervis , a dryland moss and model system used in DT studies, we hypothesized that DT is lowest in juvenile (protonemal) tissues, highest in asexual reproductive propagules (gemmae), and intermediate in adults (shoots). We tested the long‐standing hypothesis of an inherent constitutive strategy of DT in this species.METHODS Plants were rapidly dried to levels of equilibrating relative humidity (
RHeq ) ranging from 0 to 93%. Postrehydration recovery was assessed using chlorophyll fluorescence, regeneration rates, and visual tissue damage. For each life phase, we estimated the minimum rate of drying (RoDmin ) atRHeq = 42% that did not elicit damage 24 h postrehydration.RESULTS DT strategy varied with life phase, with adult shoots having the lowest
RoDmin (10‒25 min), followed by gemmae (3‒10 h) and protonema (14‒20 h). Adult shoots exhibited no detectable damage 24 h postrehydration following a rapid‐dry only at the highestRHeq used (93%), but when dried to lower RHs the response declined to <50% of control fluorescence values. Notably, immediately following rehydration (0 h postrehydration), shoots were damaged below control levels of fluorescence regardless of theRHeq , thus implicating damage.CONCLUSIONS Life phases of the moss
S. caninervis had a range of strategies from near constitutive (adult shoots) to demonstrably inducible (protonema). A new response variable for assessing degree of DT is introduced as the minimum rate of drying from which full recovery occurs.
