Michael C. F. Proctor

Desiccation-tolerance in bryophytes: a review

Abstract Desiccation-tolerance (DT), the ability to lose virtually all free intracellular water and then recover normal function upon rehydration, is one of the most remarkable features of bryophytes. The physiology of bryophytes differs in major respects from that of vascular plants by virtue of their smaller size; unlike vascular plants, the leafy shoots of bryophytes equilibrate rapidly with the water potential in their surroundings and tend to be either fully hydrated or desiccated and metabolically inactive. The time required to recover from desiccation increases and degree of recovery decreases with length of desiccation; both also depend upon temperature and intensity of desiccation. Tolerance in at least some species shows phenotypic plasticity. Recovery of respiration, photosynthesis and protein synthesis takes place within minutes or an hour or two; recovery of the cell cycle, food transport and the cytoskeleton may take 24 hours or more. Positive carbon balance is essential to survival of repeated cycles of drying and wetting; significant growth requires continuously wet periods of a few days or more. Male and female gametophytes, and gametophyte and sporophyte, may differ in tolerance. Desiccation-tolerance is essential to dispersal and establishment of spores and vegetative propagules. The mechanisms of DT in bryophytes, including expression of LEA proteins, high content of non-reducing sugars and effective antioxidant and photo-protection, are at least partly constitutive, allowing survival of rapid drying, but changes in gene expression resulting from mRNA sequestration and alterations in translational controls elicited upon rehydration are also important to repair processes following re-wetting. Phylogenetic and ecological considerations suggest that DT is a primitive character of land plants, lost in the course of evolution of the homoiohydric vascular-plant shoot system, but retained in spores, pollen and seeds, and re-evolved in the vegetative tissues of vascular “resurrection plants.” Bryophytes have retained the poikilohydry and DT that are probably the optimal pattern of adaptation at their scale, but modern bryophytes are specialized and diverse, and are removed by the same span of evolutionary time as the flowering plants from their primitive origins.

Photosynthetic responses of a moss, Tortula ruralis, ssp. ruralis, and the lichens Cladonia convoluta and C. furcata to water deficit and short periods of desiccation, and their ecophysiological significance: a baseline study at present-day CO2 concentration

We report the changes in CO2 assimilation, potential photochemical activity (as measured by slow fluorescence), photosynthetic pigment concentrations, and dark respiration of two desiccation-tolerant (DT) lichens (Cladonia convoluta (Lam.) P. Cout. and C. furcata (Huds.) Schrad.), and a DT moss (Tortula ruralis (Hedw.) Gaertn. ssp. ruralis) during slow drying, and on rehydration following a 12 h period of desiccation. Initially there was a two to fourfold increase in net CO., assimilation due to reduction of CO2 -diffusion resistance by elimination of excess water. Optimum water content for photosynthesis was 100-150 % of dry mass (DM) in C. convoluta, c. 100 % DM in C. furcata, and 120-200 % DM in T. ruralis. The intensity of maximum and steady-state slow fluorescence showed little change above water contents of 56%, DM in the lichens and 73 % DM in T. ruralis (corresponding to c. 30-40 % cell relative water content), but fell sharply at lower water content. The variable duorophyll-fluorescence decrease ratio (Rfd) at 690 nm peaked at 56 % DM water content in the two lichens, and at 45% DM in T. ruralis. Photochemical activity ceased at the same point in the experiments as CO, assimilation; dark respiration ceased only when desiccation was complete. In all three species, the photosynthetic apparatus remained in a fully and quickly recoverable state. Chlorophyll and carotenoid concentrations remained substantially unaltered throughout. On rehydration, chlorophyll fluorescence parameters returned within 30 min to pre-desiccation levels, and photosynthesis recovered fully and rapidly (< 1 h). All three species attained a positive carbon balance within 20 min of re-moistening, in spite of high rates of dark respiration. The results confirm the significance of extracellularly-stored water to poikilohydric DT lichens and bryophytes. The measurements, in conjunction with published data on the full-turgor water content of similar mosses and lichens, show that the cell-physiological response of photosynthesis to water deficit is not greatly different from that of either normal or DT vascular plants. Small plant size and small cell volume in DT lichens and mosses, together with rapid recovery of photosynthesis after desiccation, allow the plants to utilize the small amounts of intermittently available water from brief showers or dew.

The ecology of severe moorland fire on the North York Moors: effects of the 1976 fires, and subsequent surface and vegetation development.

At the end of the dry summer of 1976, severe fires destroyed the surface vegetation and caused major alterations of the underlying soils and peats of over 600 ha of Calluna-dominated moorland at Rosedale Moor, c. 330-400 m a.s.l. on the central plateau of the North York Moors. The fire burnt deeply into blanket peats, and largely destroyed thinner peats and the organic horizons of neighbouring stagnohumic gley and podzolic soils, reducing them, in the most extreme cases, to a layer of ash. (...)

The bryophyte paradox: tolerance of desiccation, evasion of drought

Vascular plants represent one strategy of adaptation to the uneven and erratic supply of water on land. Desiccation-tolerant (DT) bryophytes represent an alternative, photosynthesising and growing when water is freely available, and suspending metabolism when it is not. By contrast with vascular plants, DT bryophytes are typically ectohydric, carrying external capillary water which can vary widely in quantity without affecting the water status of the cells. External water is important in water conduction, and results in bryophyte leaf cells functioning for most of the time at full turgor; water stress is a relatively brief transient phase before full desiccation. All bryophytes are C3 plants, and their cells are essentially mesophytic in important physiological respects. Their carbohydrate content shows parallels with that of maturing embryos of DT seeds. Initial recovery from moderate periods of desiccation is very rapid, and substantial elements of it appear to be independent of protein synthesis. Desiccation tolerance in effect acts as a device that evades the problems of drought, and in various adaptive features DT bryophytes are more comparable with (mesic) desert ephemerals or temperate winter annuals (but on a shorter time scale, with DT vegetative tissues substituting for DT seeds) than with drought-tolerant vascular plants.

The ecology of severe moorland fire on the North York moors : seed distribution and seedling establishment of Calluna vulgaris

1. Regeneration of Calluna vulgaris following normal heath fires is from surviving stem bases or, where survival is poor, from a seed bank. Severe fires causing ignition of surface organic horizons kill stem bases and cause a serious depletion of the seed bank, most of which (up to 10 6 seeds m −2 ) lies in the litter and upper 2-3 cm of soil or organic material. Germinable seeds were detected in appreciable numbers down to 6 cm beneath the boundary of the F/O soil horizons in soil cores from mature heath vegetation on a blanket peat and peaty stagnopodzol. However, severe fires in which more than 10 cm of peat is ignited will destroy all of the viable seed bank

Patterns of desiccation tolerance and recovery in bryophytes

The study of desiccation tolerance in bryophytes avoids thecomplications of higher-plant vascular systems and complex leaf structures, butremains a multifaceted problem. Some of the pertinent questions have at leastpartial analogues in seed biology – events during a drying-rewettingcyclewith processes in seed maturation and germination, and the gradual loss ofviability on prolonged desiccation, and the relation of this to intensity ofdesiccation and temperature, with parallel questions in seed storage. Pastresearch on bryophyte desiccation tolerance is briefly reviewed. Evidence ispresented from chlorophyll-fluorescence measurements and experiments withmetabolic inhibitors that recovery of photosynthesis in bryophytes followingdesiccation depends mainly on rapid reactivation of pre-existing structures andinvolves only limited de novo protein synthesis. Followinginitial recovery, protein synthesis is demonstrably essential to themaintenanceof photosynthetic function in the light, but the rate of maintenance turnoverinthe dark appears to be slow. Factors leading to long-term desiccation damagearediverse; indications are that desiccation tolerant species often survive bestinthe range −100 to −200 MPa.

Experiments on the effect of different intensities of desiccation on bryophyte survival, using chlorophyll fluorescence as an index of recovery

Abstract Chlorophyll fluorescence provides a non-invasive and non-destructive method to follow various aspects of the photosynthetic function of bryophytes under relatively natural conditions, which is easy to use and can be applied to small amounts of material. Some of its potentialities (and potential pitfalls) for bryophyte desiccation physiology are outlined. Data are presented on the responses of eleven desiccation-tolerant bryophytes to drying at –41, –114, –218 and –412 MPa for periods up to ~240 days. Recovery was assessed from FV/FM after 20 min and 24 h re-wetting, and from the mean FM value after 24 h. For the more desiccation-tolerant species, Grimmia pulvinata, Syntrichia ruralis, Andreaea rothii, Racomitrium lanuginosum, R. aquaticum, Leucodon sciuroides, Pleurochaete squarrosa and Ulota crispa, long-term survival (>30–120 d) was generally best at ~–100 to –200 MPa (20–45% r.h.). The moderately desiccation-tolerant Anomodon viticulosus, Porella platyphylla and P. obtusata survived best at the highest humidity used, –41 MPa (74% r.h.).

Why do Polytrichaceae have lamellae

Abstract Light-response curves of chlorophyll-fluorescence parameters from 12 species of Polytrichaceae show photosynthetic electron flow giving a good fit to negative-exponential saturation curves up to high irradiances; 95%-saturation irradiances for the species of unshaded habitats approached or exceeded noon summer sunlight. The species showed little or no indication of the non-saturating electron flow at high irradiances, or the very high values of non-photochemical quenching, seen in many other mosses of dry, sun-exposed habitats. Calculation of CO2 diffusion rates from first principles on a cell-area basis indicates that photosynthesis of mosses with unistratose leaves is likely to be limited by CO2 diffusion resistance at high irradiances. In Polytrichaceae the area for CO2 uptake is often >6 times the projected leaf area. By lowering the whole-leaf resistance to CO2 uptake, the lamellae remove the CO2-diffusion constraint that limits mosses with unistratose leaves and allow Polytrichaceae to utilize efficiently the high irradiance of direct sunlight.

Light and desiccation responses of some Hymenophyllaceae (filmy ferns) from Trinidad, Venezuela and New Zealand: poikilohydry in a light-limited but low evaporation ecological niche

BACKGROUND AND AIMS Hymenophyllaceae (filmy ferns) are typically plants of shady, constantly moist habitats. They attain greatest species diversity and biomass in humid tropical montane forests and temperate hyperoceanic climates. This paper presents ecophysiological data bearing on their worldwide ecological niche space and its limits. METHODS Chlorophyll fluorescence was used to monitor recovery in desiccation experiments, and for measurements of 95 % saturating irradiance [photosynthetic photon flux density (PPFD(95 %))] of photosynthetic electron flow and other parameters, in the New Zealand Hymenophyllum sanguinolentum, and three species each of Hymenophyllum and Trichomanes from forests in Trinidad and Venezuela. KEY RESULTS Hymenophyllum sanguinolentum was comparable in desiccation tolerance and light responses with the European species. The more common species in the two tropical forests showed PPFD(95 %) >100 µmol m(-2) s(-1), and withstood moderate desiccation (-40 MPa) for several days. The four most shade-adapted species had PPFD(95 %) ≤51 µmol m(-2) s(-1), and were sensitive to even mild and brief desiccation (-22 MPa for 3 d). CONCLUSIONS Light and desiccation responses of filmy ferns can be seen as an integrated package. At low light and windspeed in humid forests, net radiation and saturation deficit are low, and diffusion resistance high. Water loss is slow and can be supported by modest conduction from the sub-stratum. With higher irradiance, selection pressure for desiccation tolerance increases progressively. With low light and high humidity, the filmy fern pattern of adaptation is probably optimal, and the vascular plant leaf with mesophyll and stomata offers no advantage in light capture, water economy or CO(2) uptake. Trade-offs between light adaptation and desiccation tolerance, and between stem conduction and water absorption through the leaf surface, underlie adaptive radiation and niche differentiation of species within the family. Hymenophyllaceae are a rare example of an evolutionary shift of adaptive strategy from typical vascular plant adaptation to the poikilohydry most typical of bryophytes.

Desiccation tolerance and recovery of the leafy liverwort Porella platyphylla (L.)Pfeiff.: chlorophyll-fluorescence measurements

AbstractModulated chlorophyll fluorometry demonstrated rapid and complete recovery of maximum and effective quantum yield (Fv/Fm and ΦPSII)on remoistening after 7 days in an air-dry state. Both parameters returned to pre-desiccation values within 2 h in either darkness or light (PPFD 100 μmol m−2 S−l), and the period of desiccation appeared as only a transitory interruption of normal photosynthetic function. In the course of drying both parameters declined as cell water content fell below full turgor, steeply so below RWC = 0.5, but photochemical quenching was little affected. Increase in non-photochemical quenching (NPQ) under water stress was almost all in the slow-relaxing (‘photoinhibitory’) component. During recovery in light, NPQ increased strongly with peaks at 2-3 hand 7-8 h (in both fast and slowrelaxing components), returning to pre-desiccation levels within 24 h. Progressive fall in NPQ during recovery in the dark was mostly due to decline in the slow-relaxing component. The results suggest tha...