Desiccation Tolerance Research Articles

Functional synergy between disordered proteins and sugars in desiccation protection.

Organisms across all biological kingdoms have evolved to survive near complete desiccation. Desiccation tolerance relies on the intracellular accumulation of high levels of specific intrinsically disordered proteins such as late embryogenesis abundant (LEA) proteins as well as non-reducing disaccharides, such as trehalose and sucrose. IDPs have few intramolecular bonds and a large solvent-accessible surface area, making their ensemble more sensitive to the solution environment than their well-folded counterparts. This implies that the ensemble and functions of protective IDPs are likely to be influenced by changes in metabolome induced by desiccation. Here we show that cosolutes enriched during desiccation, augment the protective function of full length IDPs during drying. We found that trehalose, a key molecule enriched in tardigrades, confers a synergistic protective effect when mixed with a model tardigrade IDP, CAHS D, at biological relevant ratios, and this synergy persists in vivo. Interestingly, a non-tardigrade sugar, sucrose, exerts less synergy. Extending these experiments, we found that LEA proteins from an organism synergizes best with the major non-reducing disaccharide (trehalose or sucrose) enriched in that organism during desiccation to promote protection. LEA proteins are made of 11-mer motif repeats; and interestingly, LEA-sugar synergy is not consistent for 11-, 22-, or 44-mer LEA motifs. Our results demonstrate that desiccation tolerant organisms may have evolved to create a specific cosolute environment to precisely tune the function of constituent IDPs. Beyond extending our knowledge of desiccation tolerance, our finding that cosolutes can tune the protective capacity of IDPs provides evidence that changing solution chemistry can modulate IDP function. We further seek to understand the mechanistic basis of IDP-cosolute synergy using biophysical approaches where we speculate that cosolutes modulate the local and global ensemble of IDPs resulting differences in IDP function.

Uncovering the molecular grammar of IDPs in desiccation tolerance.

Tardigrades, aka water bears, are remarkable for their ability to survive many environmental stresses, including desiccation (extreme drying). Desiccation tolerance in tardigrades depends on the accumulation of several families of intrinsically disordered proteins (IDPs), of which Cytosolic Abundant Heat Soluble (CAHS) proteins are essential to survive desiccation. Beyond tardigrades, CAHS proteins can also improve desiccation tolerance in heterologous systems and prevent desiccation-induced protein damage in vitro. However, what sequence features drive CAHS protein function is unknown. Understanding the CAHS sequence-ensemble-function relationship will shed light on the molecular mechanisms by which tardigrades survive extreme stresses. Using a model CAHS protein, CAHS D, we show that helix formation is important for its protective capacity. Utilizing a rational mutagenesis approach, we find that an internal linker region is the protective portion of CAHS D. We find that within this linker region specific sequence features such as charge identity, hydrophobicity, and amino acid organization dictate specific biophysical properties, such as helix formation, and are correlated to the desiccation protection in vitro. However, small helical peptides by themselves cannot confer the same levels of protection as CAHS D. This indicates that along with helicity, other features likely play a role in determining the protective capacity of CAHS D. These findings support the existing theory of helicity provided protection by different stress-tolerant LEA proteins. Understanding CAHS D's sequence-structure-function relationship will not only provide insights into how IDP sequences dictate their conformational dynamics and functional properties, but can also be useful for real-world applications like designing stress-tolerant crops or helping increase the shelf-life of sensitive biomedical materials in a dry state.

The fragility of vitrified glasses correlates with their protective capacity during desiccation.

Water is essential for active life processes and metabolism. Despite this, a number of diverse organisms distributed across the kingdoms of life are able to survive near-complete desiccation. How organisms survive extreme water loss is one of the enduring mysteries of organismal physiology. Increases in intracellular viscosity, leading to the formation of a vitrified (glassy) state has been implicated as being necessary, but not sufficient, for conferring desiccation tolerance. What properties of a vitrified system make it desiccation-tolerant or -sensitive are unknown. Here we examine the property of ‘glass fragility.’ Specifically, we look at the glass fragility of different mixtures made from two well-characterized mediators of desiccation tolerance, the non-reducing disaccharide trehalose, and the polyol glycerol. We find that different weight-by-weight mixtures of these two desiccation protective molecules result in glasses with distinct glass fragilities. We test the capacity of these mixtures to preserve the function of a desiccation-sensitive enzyme, lactate dehydrogenase, during drying and find that strong glass formation correlates with increased protective capacity. We also rule out two other competing hypotheses, plasticization/anti-plasticization and water retention as possible mechanisms driving protection of dry trehalose-glycerol mixtures. These data suggest that the strength/fragility of a glass is a property influencing its ability to preserve biological material during drying. Understanding the underpinnings of desiccation tolerance not only advances our understanding of organismal physiology but provides avenues for the development of technologies to reduce our dependence on the cold-chain as well as for increasing food security.

Developing Wolbachia-based disease interventions for an extreme environment.

Aedes aegypti mosquitoes carrying self-spreading, virus-blocking Wolbachia bacteria are being deployed to suppress dengue transmission. However, there are challenges in applying this technology in extreme environments. We introduced two Wolbachia strains into Ae. aegypti from Saudi Arabia for a release program in the hot coastal city of Jeddah. Wolbachia reduced infection and dissemination of dengue virus (DENV2) in Saudi Arabian mosquitoes and showed complete maternal transmission and cytoplasmic incompatibility. Wolbachia reduced egg hatch under a range of environmental conditions, with the Wolbachia strains showing differential thermal stability. Wolbachia effects were similar across mosquito genetic backgrounds but we found evidence of local adaptation, with Saudi Arabian mosquitoes having lower egg viability but higher adult desiccation tolerance than Australian mosquitoes. Genetic background effects will influence Wolbachia invasion dynamics, reinforcing the need to use local genotypes for mosquito release programs, particularly in extreme environments like Jeddah. Our comprehensive characterization of Wolbachia strains provides a foundation for Wolbachia-based disease interventions in harsh climates.

Tardigrade small heat shock proteins can limit desiccation-induced protein aggregation

Small heat shock proteins (sHSPs) are chaperones with well-characterized roles in heat stress, but potential roles for sHSPs in desiccation tolerance have not been as thoroughly explored. We identified nine sHSPs from the tardigrade Hypsibius exemplaris, each containing a conserved alpha-crystallin domain flanked by disordered regions. Many of these sHSPs are highly expressed. Multiple tardigrade and human sHSPs could improve desiccation tolerance of E. coli, suggesting that the capacity to contribute to desicco-protection is a conserved property of some sHSPs. Purification and subsequent analysis of two tardigrade sHSPs, HSP21 and HSP24.6, revealed that these proteins can oligomerize in vitro. These proteins limited heat-induced aggregation of the model enzyme citrate synthase. Heterologous expression of HSP24.6 improved bacterial heat shock survival, and the protein significantly reduced heat-induced aggregation of soluble bacterial protein. Thus, HSP24.6 likely chaperones against protein aggregation to promote heat tolerance. Furthermore, HSP21 and HSP24.6 limited desiccation-induced aggregation and loss of function of citrate synthase. This suggests a mechanism by which tardigrade sHSPs promote desiccation tolerance, by limiting desiccation-induced protein aggregation, thereby maintaining proteostasis and supporting survival. These results suggest that sHSPs provide a mechanism of general stress resistance that can also be deployed to support survival during anhydrobiosis.

Differential Effects of Desiccation on Hornworts with Contrasting Life Histories in Tropical Montane Forests: A Functional Trait—Based Perspective

Desiccation tolerance (DT) is the ability of an organism or structure to dry completely and subsequently survive in that air-dry state. Hornworts are excellent plant models to study desiccation effects as they have contrasting life histories which are likely associated with DT. We tested whether (1) epiphytic species had more efficient DT responses to drying and postrehydration than non-epiphytic species and whether (2) “green” spores were more sensitive than non-green spores to extreme drying. Hornwort species were collected from the Atlantic Forest of Rio de Janeiro, Brazil. We studied five species (gametophytes and spores: Dendroceros crispus, D. crispatus, Nothoceros vincentianus, Phaeoceros carolinianus; and only spores of Anthoceros lamellatus), using different relative humidity values, drying durations, and postrehydration conditions. All DT treatments affected the chlorophyll fluorescence (Fv/Fm) of gametophytes, with species-specific responses. D. crispatus and D. crispus (epiphytes) performed better than P. carolinianus and N. vincentianus, with fast recovery of Fv/Fm values postrehydration. The ability of non-green spores of P. carolinianus and A. lamellatus and green spores of D. crispus to support desiccation led us to reject our second hypothesis. The DT strategies of hornworts highlighted the trade-offs that are important in spore dispersal and plant establishment, such as fast colonization in Dendroceros spp. and potential spore soil banks in Phaeoceros and Anthoceros species.

Drought survival and recovery in grasses: Stress intensity and plant-plant interactions impact plant dehydration tolerance.

Plant dehydration tolerance confers drought survival in grasses, but the mortality thresholds according to soil water content (SWC),vapour pressure deficit (VPD)and plant-plant interactions are little explored. We compared the dehydration dynamics of leaf meristems, which are the key surviving organs, plant mortality,and recovery of Mediterranean and temperate populations of two perennial grass species, Dactylis glomerata and Festuca arundinacea, grown in monocultures and mixtures under a low-VPD (1.5 kPa) versus a high-VPD drought (2.2 kPa). The lethal drought index (LD50 ), that is, SWC associated with 50% plant mortality, ranged from 2.87% (ψs = -1.68 MPa) to 2.19% (ψs = -4.47 MPa) and reached the lowest values under the low-VPD drought. Populations of D. glomerata were more dehydration-tolerant (lower LD50 ), survivedand recovered better than F. arundinacea populations. Plant-plant interactions modified dehydration tolerance and improved post-drought recovery in mixtures compared with monocultures. Water content as low as 20.7%-36.1% in leaf meristems allowed 50% of plants to survive. We conclude that meristem dehydration causes plant mortality and that drought acclimation can increase dehydration tolerance. Genetic diversity, acclimationand plant-plant interactions are essential sources of dehydration tolerance variability to consider when predicting drought-induced mortality.

Demystifying the convergent ecological specialization of desiccation-tolerant vascular plants for water deficit.

Desiccation-tolerant vascular plants (DT plants) are able to tolerate the desiccation of their vegetative tissues; as a result, two untested paradigms can be found in the literature, despite contradictions to theoretical premises and empirical findings. First, it is widely accepted that DT plants form a convergent group of specialist plants to water deficit conditions. A derived paradigm is that DT plants are placed at the extreme end of stress tolerance. Here, we tested the hypotheses that DT plants (1) are in fact convergent specialists for water deficit conditions and (2) exhibit ecological strategies related to stress tolerance, conservative resource-use and survival. We used biogeographical and functional-traits approaches to address the mentioned paradigms and assess the species' ecological strategies. For this, 27 DT plants were used and compared to 27 phylogenetically related desiccation-sensitive vascular plants (DS plants). We could not confirm either of the two hypotheses. We found that despite converging in desiccation tolerance, DT plants differ in relation to the conditions in which they occur and the ecological strategies they use to deal with water deficit. We found that some DT plants exhibit advantageous responses for higher growth and resource acquisition, which are suitable responses to cope with more productive conditions or with higher disturbance. We discuss that the ability to tolerate desiccation could compensate for a drought vulnerability promoted by higher investment in growth and bring advantages to deal with quick and pronounced variation of water, rather than to drought solely. DT plants are not only selected by drought as an environmental constraint. The alternative functional designs could promote the diversity of ecological strategies, which preclude their convergence to the same resources and conditions. Thus, DT plants are a heterogeneous group of plants in how they deal with drought, despite their desiccation tolerance ability.

Influence of desiccation and water deficit on the initial development of seedlings of Tabebuia aurea (Silva Manso) Beth. Hook. and S. Moore (Bignoniaceae)

Desiccation tolerance mechanisms are one of the main factors related to the ability to survive water deficit conditions imposed by abiotic stress. Thus, the objective of this work was to evaluate the desiccation tolerance and the influence of water deficit on the initial development of Tabebuia aurea (Silva Manso) Benth. & Hook.f. ex S. Moore. The seedlings were divided into two treatments the control and those that were submitted to 50% desiccation. The control groups received water daily over a period of 30 days, while the groups that underwent water deficit had water suspension for 14 days, totaling two cycles of water deficit over a period of 30 days. The results of this study indicate that seedlings of T. aurea survive desiccation and present less development, whether of the stem, roots, number of leaves, stem diameter when subjected to desiccation and consequent water deficit. Thus, these results indicate that the reduction in early development is related to the perception and attenuation of stressful conditions imposed by the abiotic environment during development.

How long can tardigrades survive in the anhydrobiotic state? A search for tardigrade anhydrobiosis patterns.

Anhydrobiosis is a desiccation tolerance that denotes the ability to survive almost complete dehydration without sustaining damage. The knowledge on the survival capacity of various tardigrade species in anhydrobiosis is still very limited. Our research compares anhydrobiotic capacities of four tardigrade species from different genera, i.e. Echiniscus testudo, Paramacrobiotus experimentalis, Pseudohexapodibius degenerans and Macrobiotus pseudohufelandi, whose feeding behavior and occupied habitats are different. Additionally, in the case of Ech. testudo, we analyzed two populations: one urban and one from a natural habitat. The observed tardigrade species displayed clear differences in their anhydrobiotic capacity, which appear to be determined by the habitat rather than nutritional behavior of species sharing the same habitat type. The results also indicate that the longer the state of anhydrobiosis lasts, the more time the animals need to return to activity.

A quantitative trait locus conferring flood tolerance to deepwater rice regulates the formation of two distinct types of aquatic adventitious roots.

A key trait conferring flood tolerance is the ability to grow adventitious roots as a response to submergence. The genetic traits of deepwater rice determining the development and characteristics of aquatic adventitious roots (AAR) had not been evaluated. We used near-isogenic lines introgressed to test the hypothesis that the impressive shoot elongation ability of deepwater rice linked to quantitative trait loci 1 and 12 also promote the development of AAR. The deepwater rice genotype NIL-12 possessed expanded regions at the stem nodes where numerous AAR developed as a response to submergence. Two types (AR1 and AR2) of roots with distinct timing of emergence and large differences in morphological and anatomical traits formed within 3 (AR1) to 7 (AR2) d of submergence. The mechanical impedance provided by the leaf sheath caused AR2 to emerge later promoting thicker roots, higher elongation capacity and higher desiccation tolerance. Upregulation of key genes suggests a joint contribution in activating the meristem in AAR enhancing the development of these in response to submergence. The morphological and anatomical traits suggested that AR2 is better adapted to long-term flooding than AR1. We therefore propose that AR2 in deepwater rice functions as an evolutionary defence strategy to tackle periodic submergence.

Gesneriads, a Source of Resurrection and Double-Tolerant Species: Proposal of New Desiccation- and Freezing-Tolerant Plants and Their Physiological Adaptations.

Gesneriaceae is a pantropical family of plants that, thanks to their lithophytic and epiphytic growth forms, have developed different strategies for overcoming water scarcity. Desiccation tolerance or "resurrection" ability is one of them: a rare phenomenon among angiosperms that involves surviving with very little relative water content in their tissues until water is again available. Physiological responses of desiccation tolerance are also activated during freezing temperatures, a stress that many of the resurrection gesneriads suffer due to their mountainous habitat. Therefore, research on desiccation- and freezing-tolerant gesneriads is a great opportunity for crop improvement, and some of them have become reference resurrection angiosperms (Dorcoceras hygrometrica, Haberlea rhodopensis and Ramonda myconi). However, their difficult indoor cultivation and outdoor accessibility are major obstacles for their study. Therefore, this review aims to identify phylogenetic, geoclimatic, habitat, and morphological features in order to propose new tentative resurrection gesneriads as a way of making them more reachable to the scientific community. Additionally, shared and species-specific physiological responses to desiccation and freezing stress have been gathered as a stress response metabolic basis of the family.

BfmRS encodes a regulatory system involved in light signal transduction modulating motility and desiccation tolerance in the human pathogen Acinetobacter baumannii

We have previously shown that Acinetobacter baumannii as well as other relevant clinical bacterial pathogens such as Staphylococcus aureus and Pseudomonas aeruginosa, perceive and respond to light at 37 °C, the normal temperature in mammal hosts. In this work, we present evidence indicating that the two-component system BfmRS transduces a light signal in A. baumannii at this temperature, showing selective involvement of the BfmR and BfmS components depending on the specific cellular process. In fact, both BfmR and BfmS participate in modulation of motility by light, while only BfmR is involved in light regulation of desiccation tolerance in this microorganism. Neither BfmR nor BfmS contain a photoreceptor domain and then most likely, the system is sensing light indirectly. Intriguingly, this system inhibits blsA expression at 37 °C, suggesting antagonistic functioning of both signaling systems. Furthermore, we present evidence indicating that the phosphorylatable form of BfmR represses motility. Overall, we provide experimental evidence on a new biological function of this multifaceted system that broadens our understanding of A. baumannii’s physiology and responses to light.

Expression of tardigrade disordered proteins impacts the tolerance to biofuels in a model cyanobacterium Synechocystis sp. PCC 6803.

Tardigrades, known colloquially as water bears or moss piglets, are diminutive animals capable of surviving many extreme environments, even been exposed to space in low Earth orbit. Recently termed tardigrade disordered proteins (TDPs) include three families as cytoplasmic-(CAHS), secreted-(SAHS), and mitochondrial-abundant heat soluble (MAHS) proteins. How these tiny animals survive these stresses has remained relatively mysterious. Cyanobacteria cast attention as a "microbial factory" to produce biofuels and high-value-added chemicals due to their ability to photosynthesis and CO2 sequestration. We explored a lot about biofuel stress and related mechanisms in Synechocystis sp. PCC 6803. The previous studies show that CAHS protein heterogenous expression in bacteria, yeast, and human cells increases desiccation tolerance in these hosts. In this study, the expression of three CAHS proteins in cyanobacterium was found to affect the tolerance to biofuels, while the tolerance to Cd2+ and Zn2+ were slightly affected in several mutants. A quantitative transcriptomics approach was applied to decipher response mechanisms at the transcriptional level further.

Desiccation tolerance in larvae of Culex quinquefasciatus Say, 1823 and Anopheles stephensi Liston, 1901 (Diptera: Culicidae): implications for mosquito control

A laboratory assessment of desiccation tolerance in larval stages of mosquitoes Anopheles stephensi Liston, 1901 (Diptera: Culicidae) and Culex quinquefasciatus Say, 1823 (Diptera: Culicidae) was carried out using five temperature levels and three levels of exposure duration as explanatory variables. The increase in the duration of exposure to desiccation from 15 min to 60 min was noted to result in a substantial increase in water loss (in mg) in mosquito larvae. Similarly, the increase in temperature levels was observed to cause larval mortality and a substantial decrease in the emergence of adults. Both the temperature and the duration of exposure to desiccation were found to be influential factors in determining survival and subsequent emergence of adults. Desiccation is a primary factor in determining the survival of mosquito larvae, particularly in the conditions where habitat permanence is uncertain, e.g., in temporary pools and containers serving as mosquito larval habitats. The results of the present study provide a glimpse into the effects of desiccation at varied temperatures and exposure durations on the successful emergence of adults in mosquitoes Cx. quinquefasciatus and An. stephensi. Although primary, the obtained results show that desiccation can be a probable way of regulating the development of mosquito larvae in conditions where the permanence of the habitat for mosquito larvae is uncertain. Further studies on desiccation tolerance may be carried out using different mosquito species that are adapted to temporary pools and containers as sources for breeding.

Indigenous and introduced Collembola differ in desiccation resistance but not its plasticity in response to temperature.

Biological invasions have significant ecological and economic impacts. Much attention is therefore focussed on predicting establishment and invasion success. Trait-based approaches are showing much promise, but are mostly restricted to investigations of plants. Although the application of these approaches to animals is growing rapidly, it is rare for arthropods and restricted mostly to investigations of thermal tolerance. Here we study the extent to which desiccation tolerance and its phenotypic plasticity differ between introduced (nine species) and indigenous (seven species) Collembola, specifically testing predictions of the 'ideal weed' and 'phenotypic plasticity' hypotheses of invasion biology. We do so on the F2 generation of adults in a full factorial design across two temperatures, to elicit desiccation responses, for the phenotypic plasticity trials. We also determine whether basal desiccation resistance responds to thermal laboratory natural selection. We first show experimentally that acclimation to different temperatures elicits changes to cuticular structure and function that are typically associated with water balance, justifying our experimental approach. Our main findings reveal that basal desiccation resistance differs, on average, between the indigenous and introduced species, but that this difference is weaker at higher temperatures, and is driven by particular taxa, as revealed by phylogenetic generalised least squares approaches. By contrast, the extent or form of phenotypic plasticity does not differ between the two groups, with a 'hotter is better' response being most common. Beneficial acclimation is characteristic of only a single species. Laboratory natural selection had little influence on desiccation resistance over 8-12 generations, suggesting that environmental filtering rather than adaptation to new environments may be an important factor influencing Collembola invasions.

Physiological and biochemical changes in desiccation and rehydration cycles of Selaginella convoluta (Selaginellaceae)

Abstract Vegetative desiccation tolerance (VDT) is a biological process that allows resurrection plants to complete desiccation-rehydration cycles and survive without permanent damage. Physiological and biochemical changes related to the VDT were evaluated in the lycophyte Selaginella convoluta from the Caatinga biome, a seasonally dry tropical forest of northeastern Brazil. As representative of the oldest division of extant vascular plants, the investigation of VDT mechanisms in this species serves as an opportunity to provide information for research communities interested in functional traits related to water-limited conditions. The experiments were performed with plants in their natural habitat, in dry and rainy seasons, and in pots under shade house conditions. Relative water content, chlorophyll a fluorescence, gas exchange, activity of antioxidant enzymes, concentration of chlorophylls, proteins, total amino acids, proline, and soluble carbohydrates in leaf tissues were evaluated throughout the process of complete dehydration and subsequent re-watering of intact plants. The overall results reveal the capacity of S. convoluta to tolerate extreme dehydration and rapidly recover upon rehydration. This species minimizes potential damages during the desiccation-rehydration cycle due to the presence of inductive mechanisms (photochemical preventing, sucrose accumulation) and constitutive mechanisms (antioxidant activity of catalase and ascorbate peroxidase), which share similarities with the VDT of both angiosperms and bryophytes.

Climatic stress decreases tick survival but increases rate of host‐seeking behavior

AbstractTicks are vectors of many diseases and are expanding in geographic distribution. However, how ticks will fare in their new environments, where they may experience stressful climatic conditions at the expansion front, remains unclear. Since there is a trade‐off in ticks between behaviors that promote longevity and behaviors that promote reproduction, we hypothesized that extreme climatic stress reduces the survivorship of ticks but increases the frequency of tick host‐seeking behavior, or questing. Here, we used a novel method to simulate climatic stress on individual ticks of three species—Amblyomma americanum, Dermacentor variabilis, and Ixodes scapularis—to evaluate their survival, physiology, and questing behavior. The first experiment involved placing 144 adult ticks of each species in two temperature ranges (15–25°C and 25–35°C) and three relative humidity (RH) treatments (32%, 58%, and 84% RH). We assessed the ticks daily for survivorship and questing, and we measured water loss by comparing the mass of each tick when it died to when it was fully hydrated. In this first experiment, ticks in warmer and less humid conditions generally died faster than those in cooler and more humid conditions. Ticks of all three species were more likely to quest shortly before their death and consistently died after losing approximately 50%–56% of their total body water content, but Ixodes reached that threshold much faster than the other two species. The second experiment involved placing 18 ticks of each species at 35°C and 32% RH. We assessed the ticks every 3 h for survivorship, questing, and water loss. Ticks again were more likely to quest shortly before their death. With frequent checks, we were able to measure the dehydration tolerance more accurately and the rate of water loss. Ticks of all three species consistently died after losing approximately 51% of their total body water content. However, Ixodes lost water approximately 5 times faster than Amblyomma and 11 times faster than Dermacentor. These results demonstrate that severe climatic stress tilts the trade‐off toward higher questing rates but not higher overall questing time because of reduced survival rates.

Effects of desiccation rate and inhibition of protein synthesis and the violaxanthin cycle on the rewetting recovery of Porella platyphylla

Following 5 different rates of 1-week desiccation to which Porella platyphylla (a desiccation-tolerant leafy liverwort) was subjected, physiological recovery upon rehydration (after 1 h, 24 h, 48 h) in light was monitored by cytological, photosynthetic (e-transport rate, photoprotective mechanisms), and other metabolic parameters using nuclear- and chloroplast-encoded protein synthesis inhibitors and a violaxanthin cycle inhibitor (DTT: dithiothreitol). Desiccation tolerance is mainly constitutive in P. platyphylla, allowing survival of rapid drying, and employs an active rehydration-induced repair and recovery mechanism. Following 24 hours of rehydration after the one-week dehydration in laboratory air (∼35% relative humidity /RH/), the chloroplasts had an irregular round shape. The recovery within 1 h of the thylakoid-function-related photosynthetic processes was extremely fast and independent of protein synthesis, while the overall recovery (except plants dried up at 76% RH, which depended on protein synthesis only to a limited extent) required de novo protein synthesis during rewetting. During the course of rehydration protein synthesis affects rehydrin expression, osmolite and general carbohydrate metabolism, the main repair and antioxidant mechanisms. Recovery was the best in samples dried up at 76% RH. Membrane permeability increased upon rehydration following 1-week dehydration. Normal membrane function recovered after 24 h (max. 48 h), except in plants that suffered drastic dehydration. Total protein content of plants dried under different conditions and of samples taken during recovery was generally lower than in the control plants at full turgor. The xanthophyll cycle has a great importance during the recovery in light; we confirmed the existence of a greater zeaxanthin-dependent and a smaller zeaxanthin-insensitive NPQ (nonphotochemical quenching). Plants dried under more favorable conditions had better light protection. The highest values of the osmotic potential belonged to the plants subjected to intense dehydration. Total soluble carbohydrate content was well-balanced and seemed to be unchanged following the different treatments. There was a significant increase in proline, while total fructan showed lower values at different degrees of 1-week desiccation. The cytoplasmic protein synthesis is likely to be involved in the change of the fructan content during rehydration.

Phenotypic plasticity in desiccation physiology of closely related, range restricted and broadly distributed fruit fly species

Abstract Variation in geographical range size among closely related species may result from differences in physiological traits, such as desiccation tolerance, that enable these species to interact with their environment or adapt to new surroundings. We tested the hypothesis that insect species with a broader geographical range have either a higher basal desiccation tolerance or mount a more plastic response than more narrowly distributed species by exposing four fruit fly species (Ceratitis capitata, Ceratitis rosa, Ceratitis cosyra and Ceratitis podocarpi) to one of three acclimation treatments (control: standard relative humidity (RH) and temperature; desiccation: standard temperature and low humidity; and temperature: low RH and high temperature) and measuring metabolic rate, activity, water loss rates and survival. The targeted physiological responses differed between species and acclimation treatments. Survival of the widely distributed C. capitata improved by up to 43% after short‐term exposure to high temperature and desiccation (35°C; 0% RH) treatment, while survival in the more narrowly distributed species only improved by 4%–30% after a desiccation treatment (25°C; 0% RH). Less water was lost by broadly distributed C. capitata through excretion after both high temperature and desiccation treatments, but only activity and respiratory water loss (RWL) were reduced after the temperature treatment, and total water loss and cuticular water loss declined after the desiccation treatment. The narrowly distributed C. rosa also lost less water through excretion after both acclimation treatments but showed reduced cuticular and RWL only after desiccation. While basal tolerance in C. cosyra was high, acclimation responses in this species and C. podocarpi were insignificant in that they did not produce a measurable survival benefit. Broadly distributed species successfully employed unique combinations of physiological strategies, with some having highly flexible responses to stressful environmental conditions, which ultimately results in beneficial acclimation to enhance survival during dry conditions. By contrast, range restricted species showed limited responses to desiccation stress. Flexible desiccation responses likely contribute to species geographical ranges in changing climate conditions. Read the free Plain Language Summary for this article on the Journal blog.