Desiccation tolerance of Sphagnum revisited: a puzzle resolved

As ecosystem engineers, Sphagnum mosses control their surroundings through water retention, acidification and peat accumulation. Because water retention avoids desiccation, sphagna are generally intolerant to drought; however, the literature on Sphagnum desiccation tolerance (DT) provides puzzling results, indicating the inducible nature of their DT. To test this, various Sphagnum species and other mesic bryophytes were hardened to drought by (i) slow drying; (ii) ABA application and (iii) chilling or frost. DT tolerance was assessed as recovery of chlorophyll fluorescence parameters after severe desiccation. We monitored the seasonal course of DT in bog bryophytes. Under laboratory conditions, following initial de‐hardening, untreated Sphagnum shoots lacked DT; however, DT was induced by all hardening treatments except chilling, notably by slow drying, and in Sphagnum species of the section Cuspidata. In the field, sphagna in hollows and lawns developed DT several times during the growing season, responding to reduced precipitation and a lowered water table. Hummock and aquatic species developed DT only in late autumn, probably as a response to frost. Sphagnum protonemata failed to develop DT; hence, desiccation may limit Sphagnum establishment in drier habitats with suitable substrate chemistry. Desiccation avoiders among sphagna form compact hummocks or live submerged; thus, they do not develop DT in the field, lacking the initial desiccation experience, which is frequent in hollow and lawn habitats. We confirmed the morpho‐physiological trade‐off: in contrast to typical hollow sphagna, hummock species invest more resources in water retention (desiccation avoidance), while they have a lower ability to develop physiological DT.     

Analysis of the decrease in photosynthesis on desiccation of mosses from xeric and hydric environments

Three moss species [ Tortula ruraliformis (Besch.) Grout. Bryum pseudotriquetrum (Hedw.) Schaegr and Dicranella palustris (Dicks.) Crund. ex. E. F. Warb. ( D. squarrosa (Starke) Schp.] collected from a range of habitats differing in water availability were desiccated in controlled conditions. All species became photosynthetically inactive when dried below a water content of 100–200% dry weight. Only Tortula ruraliformis , a moss from arid sand dunes. was able to recover fully to pre-desiccated rates of photosynthetic electron transport during subsequent rehydration. The rate of recovery was influenced by irradiance during desiccation. Mosses from hydric habitats showed some resumption of photosynthetic electron transport (following rehydration) if dried in the dark. but did not do so if dried even in low light. In these circumstances the mosses showed evidence of lasting photoinhibition of photosynthesis after rehydration. The desiccation-tolerant T. ruraliformis became significantly photoinhibited only when continually exposed to high irradiance (1200 μmol m⁻² s⁻¹) in the hydrated state. If allowed to desiccate whilst exposed to high irradiance this species showed less evidence of photoinhibition after rehydration, and was not at all affected by desiccation in low irradiance. Photon flux absorption in dry moss was 50–60% less than that in hydrated moss as a result of leaf curling. However, the reduction in absorption of photosynthetically active radiation cannot account for the total loss of photosynthetic oxygen evolution and variable chlorophyll fluorescence observed in the desiccated mosses.     

Comparative desiccation tolerance of two Sphagnum mosses

Summary Sphagnum fallax (Klinggr.) Klinggr., a moss growing in hollows close to the water table, is more desiccation tolerant than S. nemoreum Scop., a hummock former distributed high above the hollows. Sphagnum fallax recovered to a greater proportion of its predesiccation photosynthetic rate after one and five days of tissue dryness. Further, a greater percentage of S. fallax plants survived five and ten day periods at low tissue water contents. Longer desiccated periods and lower water contents during these periods decreased both photosynthetic recovery and survival.Water contents measured in Bloomingdale Bog (Adirondack Mountains, NY, USA) showed that S. fallax probably dries more frequently and for longer periods than S. nemoreum. These results support previous findings that the greater ability of S. nemoreum to remain moist in the field is the most important character in its success as a hummock former. Greater tolerance of desiccation helps S. fallax to compensate for its greater tendency to become dry, and is a key physiological feature enabling it to dominate hollows.     

Increased activities of superoxide dismutase and catalase are not the mechanism of desiccation tolerance induced by hardening in the moss Atrichum androgynum

Abstract

The effects of treatments that increase desiccation tolerance were tested on the activity of the enzymes superoxide dismutase (SOD) and catalase (CAT) in the moss Atrichum androgynum subjected to a drying/wetting cycle. Hardening by both abscisic acid (ABA) pretreatment and partial dehydration significantly increased the rate of recovery of photosynthesis during rehydration following desiccation. Hardening treatments had little effect on SOD activity. In non-hardened plants, SOD activity increased three-fold during desiccation for 32 h at 52% rh, but hardened material tended to display smaller increases in activity. During rehydration, SOD activities rapidly declined to their initial values in all treatments. Hardening by partial dehydration, but not ABA, reduced CAT activity. After desiccation for 32 h, material from all treatments displayed about half the initial CAT activity, and activity did not change during subsequent rehydration. Results show that, while the induction of SOD appears to play a role in desiccation tolerance, a similar induction occurred in both hardened and non-hardened mosses. Induction of greater activities of enzymes that scavenge reactive oxygen species is not responsible for the added tolerance induced by hardening treatments.     

ABA treatment increases both the desiccation tolerance of photosynthesis,and nonphotochemical quenching in the moss Atrichum undulatum

Pulse amplitude modulation fluorescence was used to investigate whether abscisic acid (ABA) pretreatment increases the desiccation tolerance of photosynthesis in the moss Atrichum undulatum. In unstressed plants, ABA pretreatment decreased the F _V/F _m ratio, largely as a result of an increase in F _o. This indicated a reduction in energy transfer between LHCII and PSII, possibly hardening the moss to subsequent stress by reducing the production of the reactive oxygen species near PSII. During desiccation, F ₀, F _m, F _v/F _m, PSII, and NPQ and F ₀ quenching declined in ABA-treated and nontreated mosses. However, during rehydration, F ₀, F _m, F _v/F _m, and PSII recovered faster in ABA-treated plants, suggesting that ABA improved the tolerance of photosystem II to desiccation. NPQ increased upon rehydration in mosses from both treatments, but much more rapidly in ABA-treated plants; during the first hour of rehydration, NPQ was two-fold greater in plants treated with ABA. F ₀quenching followed a similar pattern, indicating that ABA treatment stimulated zeaxanthin-based quenching. The implications of these results for the mechanisms of ABA-induced desiccation tolerance in A. undulatum are discussed.     

Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats?

Bryophytes are a non-monophyletic group of three major lineages (liverworts, hornworts, and mosses) that descend from the earliest branching events in the phylogeny of land plants. We postulate that desiccation tolerance is a primitive trait, thus mechanisms by which the first land plants achieved tolerance may be reflected in how extant desiccation-tolerant bryophytes survive drying. Evidence is consistent with extant bryophytes employing a tolerance strategy of constitutive cellular protection coupled with induction of a recovery/repair mechanism upon rehydration. Cellular structures appear intact in the desiccated state but are disrupted by rapid uptake of water upon rehydration, but cellular integrity is rapidly regained. The photosynthetic machinery appears to be protected such that photosynthetic activity recovers quickly. Gene expression responds following rehydration and not during drying. Gene expression is translationally controlled and results in the synthesis of a number of proteins, collectively called rehydrins. Some prominent rehydrins are similar to Late Embryogenesis Abundant (LEA) proteins, classically ascribed a protection function during desiccation. The role of LEA proteins in a rehydrating system is unknown but data indicates a function in stabilization and reconstitution of membranes. Phylogenetic studies using a Tortula ruralis LEA-like rehydrin led to a re-examination of the evolution of desiccation tolerance. A new phylogenetic analysis suggests that: (i) the basic mechanisms of tolerance seen in modern day bryophytes have changed little from the earliest manifestations of desiccation tolerance in land plants, and (ii) vegetative desiccation tolerance in the early land plants may have evolved from a mechanism present first in spores.     

ABA-induced tolerance to ion leakage during rehydration following desiccation in the moss Atrichum androgynum

A simple ion leakage assay was used to investigate the effect ofabscisic acid (ABA) pretreatment on desiccation tolerance in the mossAtrichum androgynum. Results from experiments involvingtheapplication of the protein synthesis inhibitor cyclohexamide during desiccationor rehydration suggested that pretreatment with ABA does not facilitate theproduction of protection or repair proteins duringdesiccation or rehydration. Rather, ABA induces the synthesis of these proteinsduring pretreatment. The ABA-induced increase in tolerance was much less ifplants were pretreated in the dark. Exposure to red light could not substitutefor white light, suggesting that ABA action does not require phytochrome.Desiccating intact long stem segments or long segments separated into apicalandbasal parts had no effect on the desiccation tolerance of either plant part.This suggests that no movement of signals or protective molecules occurs fromthe stem bases to the apices during desiccation. Basal stem segments were muchmore sensitive to desiccation than apical regions, suggesting during senescencea breakdown in mechanisms that protect mosses from injury occurs. Theimplications of these findings for the water relations of A.androgynum are discussed.     

Determination of leaf fresh mass after storage between moist paper towels: constraints and reliability of the method

To ensure comparability among leaf fresh mass measurements it is important to handle the leaves in a standardized manner. In the present work constraints of a commonly used method to achieve full turgor, storage between damp paper towels, were investigated. After overnight rehydration in a saturated atmosphere, the fresh mass of leaves of 14 species was measured, and the leaves were stored between paper towels (two treatments: moist and wet) at 4 degrees C. Their mass was measured after 24, 48, and 72 h. Leaf fresh mass increased during the first 24 h of storage between moist paper towels by an average of 1.8%, between wet towels by 3.3%. Among the species, the increase of leaf fresh mass between moist towels correlated with the species' desiccation propensity, indicating that it was rehydration from water loss during initial handling. On the other hand, between wet towels the fresh mass increase was associated with the species' leaf tissue structure, and it continued to increase beyond 24 h, indicating that the increase was a result of water penetration into the leaf air spaces. It is concluded that storage between moist paper towels results in reliable values of leaf fresh mass, and that desiccated leaves rehydrate well between moist towels. However, care has to be taken to avoid too wet conditions as they may lead to erroneously high fresh mass values, especially in species with large air spaces. Furthermore, exposure to unsaturated atmospheric conditions during handling has to be minimized.     

ABA Increases the Desiccation Tolerance of Photosynthesis in the Afromontane Understorey Moss Atrichum androgynum

The effect of pretreatment with abscisic acid (ABA) on the physiologyof the moss Atrichum androgynum during a desiccation–rehydrationcycle was examined. During rehydration following desiccationfor 16 h, net CO₂fixation recovered much more slowly than photosystemII (PSII) activity, conditions conducive to the formation ofreactive oxygen species (ROS) in the photosynthetic apparatus.Pretreatment with ABA increased the rate of recovery of photosynthesisand PSII activity, and also doubled non-photochemical quenching(NPQ). Increased NPQ activity will reduce ROS formation, andmay explain in part how ABA hardens the moss to desiccation.In ABA-pretreated, but not untreated mosses, desiccation significantlyincreased the concentration of soluble sugars. Sugar accumulationmay promote vitrification of the cytoplasm and protect membranesduring desiccation. Starch concentrations in freshly collectedA. androgynum were only approx. 40 mg g^-1dry mass; they roseslightly during desiccation but were only slightly affectedby ABA pretreatment. ABA did not reduce chlorophyll breakdownduring desiccation. Copyright 2001 Annals of Botany Company Moss, desiccation, abscisic acid, photosynthesis, chlorophyll fluorescence     

Declining hydraulic efficiency as transpiring leaves desiccate: two types of response

The conductance of transpiring leaves to liquid water (Kleaf) was measured across a range of steady-state leaf water potentials (Psileaf). Manipulating the transpiration rate in excised leaves enabled us to vary Psileaf in the range -0.1 MPa to less than -1.5 MPa while using a flowmeter to monitor the transpiration stream. Employing this technique to measure how desiccation affects Kleaf in 19 species, including lycophytes, ferns, gymnosperms and angiosperms, we found two characteristic responses. Three of the six angiosperm species sampled maintained a steady maximum Kleaf while Psileaf remained above -1.2 MPa, although desiccation of leaves beyond this point resulted in a rapid decline in Kleaf. In all other species measured, declining Psileaf led to a proportional decrease in Kleaf, such that midday Psileaf of unstressed plants in the field was sufficient to depress Kleaf by an average of 37%. It was found that maximum Kleaf was strongly correlated with maximum CO2 assimilation rate, while Kleaf = 0 occurred at a Psileaf slightly less negative than at leaf turgor loss. A strong linear correlation across species between Psileaf at turgor loss and Psileaf at Kleaf = 0 raises the possibility that declining Kleaf was related to declining cell turgor in the leaf prior to the onset of vein cavitation. The vulnerability of leaves rehydrating after desiccation was compared with vulnerability of leaves during steady-state evaporation, and differences between methods suggest that in many cases vein cavitation occurs only as Kleaf approaches zero.     

Desiccation resistance of two semiterrestrial isopods, Ligia exotica and Ligia taiwanensis (Crustacea) in Taiwan

The ability to resist desiccation stress was examined in two semiterrestrial Ligia species, Ligia exotica Roux and L. taiwanensis Lee, in Taiwan, under a certain desiccation condition. L. exotica exhibited the longer survival time, lower weight-specific rates of water loss, and the slightly higher ability of tolerance to water loss, compared to L. taiwanensis. In each species, the animal size displays a positive correlation to the survival time and total ability to resist desiccation, yet this size effects on the weight-specific water loss rate is negative. Neither water content nor maximum tolerance to water loss shows the association with the animal size in both species. The path ways and magnitudes of the interactions between these traits of desiccation resistance are analyzed and diagrammed using a stepwise regression model. In this model, the body sizes of animal can explain the most part of the variations in the survival time. The body size has a direct effect and an indirect effect, through the effect on water loss rate, on the time that the experimental animals can survival under this desiccated condition. These results suggest that L. exotica attains larger size than does L. taiwanensis, a lower transpiration rate and, consequently, a greater ability in desiccation resistance. The performances of these interactions in the desiccated resistance are more advantageous for L. exotica to migrate and colonize in variable land habitats within a certain limit, and as a result that L. exotica shows a broader distribution pattern than did L. taiwanensis in Taiwan.     

Dry artificial seeds and desiccation tolerance induction in microspore-derived embryos of broccoli

Desiccation tolerance of broccoli microspore-derived embryos was induced by exogenous application of abscisic acid (ABA). Embryos, which were desiccated to about 10% water content, were estimated for viability after rehydration. Survival was dependent on the ABA concentration and the development stage of embryo, but not on the length of exposure period to ABA or genotype. Cotyledonary stage embryos acquired the highest desiccation tolerance when treated with 1×10^-4M ABA. Under this condition, on average 27–48% of the desiccated embryos could convert into plants. Embryos treated with 1×10^-6M ABA or no ABA or earlier development-staged embryos, such as globular and heart stages, lost viability after desiccation. A one day exposure to ABA had the similar effect on the induction of desiccation tolerance as a 7-day treatment. The dried embryos maintained their ability of plant conversion after three months of storage under room conditions. The plants derived from the desiccated embryos were not different in the morphology or ploidy level from those from non-desiccated ones.Abbreviations ABA abscisic acid - RH relative humidity     

The effect of extreme dehydration on photosynthetic activity of Sphagnum denticulatum cultivated genotypes from different habitats

Abstract

The effect of water deficit on drought-sensitive peat mosses’ photosynthetic activities were analyzed in Sphagnum denticulatum genotypes representing two ecotypes–aquatic and terrestrial. All plants, cultivated for a long time in common garden conditions, were desiccated to a water content of less than 2% of controls and subsequently rehydrated for up to 30?days. The aquatic control plants showed shade adaptations as expressed by the F₀, F_v/F₀ and Chl a/b ratios which may reflect the conditions at the parental habitat. The ecotype- and genotype-specific responses to desiccation and rehydration were observed. Under desiccation, the photoinhibition was greater in the terrestrial plants (as demonstrated by lower F_v/F_m and Φ_PSII), in comparison with the aquatic plants. This suggests either severe damage of photo centers or better photoprotection mechanisms. Although there were no consistent differences between ecotypes across treatments, the signs of intraspecific variation in desiccation sensitiveness, which presumably arose from plasticity and local adaptation of plants to their parental environments, were detected. Genotypes and their place of origin should be taken into account in future studies.     

Anhydrobiosis in bacteria: from physiology to applications

Anhydrobiosis is a phenomenon related to the partial or total desiccation of living organisms, keeping their vital functions after rehydration. The desiccated state in prokaryotes has been widely studied, mainly due to the broad spectrum of the anhydrobiosis applications. In this review, we present the basic theoretical concepts related to anhydrobiosis, focusing on bacterial species. An update about desiccation tolerance in bacteria is given; and the general mechanisms of desiccation tolerance and desiccation damage are described. In addition, we show how the study of anhydrobiosis in prokaryotes has established the theoretical and practical basis for the development of the drying technologies. With regard to the desiccation tolerance in bacteria, although many mechanisms remain undiscovered at the molecular level, important research about the physiology of the anhydrobiotic state and its applications has been performed, and here we provide the most recent information about this subject. On the other hand, the most widely used drying technologies and their particular applications in several fields are described (e.g. medicine, agriculture and food industry). Finally, topics on the stability of desiccated bacterial cells are treated, concluding with the necessity of focusing the research on the mathematical modelling of the desiccated state in bacteria.     

苔藓植物耐旱机制研究进展

耐旱藓类快速脱水并存活的能力可由快速建立起来的对环境变化的耐受机制来反映,保护细胞完整性的组成型机制与修复细胞损伤的诱导机制协同作用使苔藓植物渡过干旱胁迫。再水化时光合系统原初恢复非常迅速;ABA处理可显著改变PSⅡ的生理特征;基因表达的变化主要由翻译调控引起;脱水组织中贮存mRNPs既保护了mRNAs, 又加快了再水化修复速度。山墙藓(Tortula ruralis)是耐旱研究较多的一个种,已建立了表达序列文库(EST),将会成为耐旱研究的重要模式植物。     

苔藓植物耐旱机制研究进展

耐旱藓类快速脱水并存活的能力可由快速建立起来的对环境变化的耐受机制来反映,保护细胞完整性的组成型机制与修复细胞损伤的诱导机制协同作用使苔藓植物渡过干旱胁迫.再水化时光合系统原初恢复非常迅速;ABA处理可显著改变PSⅡ的生理特征;基因表达的变化主要由翻译调控引起;脱水组织中贮存mRNPs既保护了mRNAs,又加快了再水化修复速度.山墙藓(Tortula ruralis)是耐旱研究较多的一个种,已建立了表达序列文库(EST),将会成为耐旱研究的重要模式植物.     

Element concentrations in mosses and surface waters of western Canadian mires relative to precipitation chemistry and hydrology

Concentrations of N, P, S, Na, K, Mg, Ca, Mn, Fe, Cu, Cd, Zn, Pb, Al, and AIA (acid insoluble ash) m mosses (three Sphagnum species and Tomenthypnum nitens, all hummock species) from a variety of mires, both ombrotrophic and minerotrophic, in the coastal western and central parts of Canada are considered in relation to surface water pH and concentrations of Na⁺, K⁺, Mg²⁺, Ca²⁺, Cl⁻, and SO₄^2- Distinct west-east concentration gradients were present for most elements in both mosses and water, but there were correlations between surface water and moss concentrations only for Ca and Mg
On ombrotrophic sites and sites characterized by poor fen vegetation, wet deposition is the main source of elements in the surface water On rich fen sites, additional Ca and Mg from surrounding soils change the elemental proportions We conclude that hydrochemically the limit between poor and rich fen sites is more decisive than between bog and fen The increase in Ca may give brown mosses a competitive advantage over Sphagnum
Moss concentrations of Na and Mg are the only ones decreasing inland The constancy or inland increase of moss elemental concentrations may depend on either an increasing atmospheric supply (e g Pb), differences in moss growth rates (especially N, P, and K) or site conditions related to the water regime (e g Fe and Al)     

Thermal energy dissipation in reaction centres and in the antenna of photosystem II protects desiccated poikilohydric mosses against photo-oxidation

Seasonal differences have been observed in the ability of desiccated mosses to dissipate absorbed light energy harmlessly into heat. During the dry summer season desiccation-tolerant mosses were more protected against photo-oxidative damage in the dry state than during the more humid winter season. Investigation of the differences revealed that phototolerance could be acquired or lost even under laboratory conditions. When a desiccated poikilohydric moss such as Rhytidiadelphus squarrosus is in the photosensitive state, the primary quinone, Q(A), in the reaction centre of photosystem II is readily reduced even by low intensity illumination as indicated by reversibly increased chlorophyll fluorescence. No such reduction is observed even under strong illumination in desiccated mosses after phototolerance has been acquired. In this state, reductive charge stabilization is replaced by energy dissipation. As a consequence, chlorophyll fluorescence is quenched. Different mechanisms are responsible for quenching. One is based on the presence of zeaxanthin provided drying occurs in the light. This mechanism is known to be controlled by a protonation reaction which is based on proton-coupled electron transport while the moss is still hydrated. Another mechanism which also requires light for activation, but no protonation, is activated during desiccation. While water is slowly lost, fluorescence is quenched. In this situation, an absorption band formed at 800 nm in the light is stabilized. It loses reversibility on darkening. Comparable kinetics of fluorescence quenching and 800 nm signals as well as the linear relationship between non-photochemical fluorescence quenching (NPQ) and loss of stable charge separation in photosystem II reaction centres suggested that desiccation-induced quenching is a property of photosystem II reaction centres. During desiccation, quenchers accumulate which are stable in the absence of water but revert to non-quenching molecular species on hydration. Together with zeaxanthin-dependent energy dissipation, desiccation-induced thermal energy dissipation protects desiccated poikilohydric mosses against photo-oxidation, ensuring survival during drought periods.     

Effects of dehydration rate on physiological responses and survival after rehydration in larvae of the anhydrobiotic chironomid

Strategies to combat desiccation are critical for organisms living in arid and semi-arid areas. Larvae of the Australian chironomid Paraborniella tonnoiri resist desiccation by reducing water loss. In contrast, larvae of the African species Polypedilum vanderplanki can withstand almost complete dehydration, referred to as anhydrobiosis. For successful anhydrobiosis, the dehydration rate of P. vanderplanki larvae has to be controlled. Here, we desiccated larvae by exposing them to different drying regimes, each progressing from high to low relative humidity, and examined survival after rehydration. In larvae of P. vanderplanki, reactions following desiccation can be categorized as follows: (I) no recovery at all (direct death), (II) dying by unrepairable damages after rehydration (delayed death), and (III) full recovery (successful anhydrobiosis). Initial conditions of desiccation severely affected survival following rehydration, i.e. P. vanderplanki preferred 100% relative humidity where body water content decreased slightly. In subsequent conditions, unfavorable dehydration rate, such as more than 0.7 mg water lost per day, resulted in markedly decreased survival rate of rehydrated larvae. Slow dehydration may be required for the synthesis and distribution of essential molecules for anhydrobiosis. Larvae desiccated at or above maximum tolerable rates sometimes showed temporary recovery but died soon after.     

Tissue elastic properties of eight Hawaiian Dubautia species that differ in habitat and diploid chromosome number

Summary Eight Hawaiian Dubautia species grow in habitats as varied as exposed lava, dry scrub, mesic forest, wet forest, and bog. These species also differ in diploid chromosome number, with four species having 13 pairs of chromosomes and four species having 14 pairs. This ecological and chromosomal variation is paralleled by significant interspecific variation in tissue elastic properties. The four 13-paired species from dry habitats exhibit significantly lower tissue elastic moduli near full hydration (E _i) than the four 14-paired species from mesic to wet habitats. Values of E _i range from 2 to 4 MPa among the former species and from 9 to 18 MPa among the latter species. The turgor dependence of the elastic modulus also differs markedly between the two groups of species. As a result of these differences in tissue elastic properties, the capacity for maintaining high turgor pressures as tissue water content decreases is much greater in the 13-paired species from dry habitats than in the 14-paired species from mesic to wet habitats. These results indicate that the evolutionary diversification of the Dubautia species has been accompanied by a significant degree of change at the physiological level.