The evolution of vegetative desiccation tolerance in land plants

Vegetative desiccation tolerance is a widespread but uncommon occurrence in the plant kingdom generally. The majority of vegetative desiccation-tolerant plants are found in the less complex clades that constitute the algae, lichens and bryophytes. However, within the larger and more complex groups of vascular land plants there are some 60 to 70 species of ferns and fern allies, and approximately 60 species of angiosperms that exhibit some degree of vegetative desiccation tolerance. In this report we analyze the evidence for the differing mechanisms of desiccation tolerance in different plants, including differences in cellular protection and cellular repair, and couple this evidence with a phylogenetic framework to generate a working hypothesis as to the evolution of desiccation tolerance in land plants. We hypothesize that the initial evolution of vegetative desiccation tolerance was a crucial step in the colonization of the land by primitive plants from an origin in fresh water. The primitive mechanism of tolerance probably involved constitutive cellular protection coupled with active cellular repair, similar to that described for modern-day desiccation-tolerant bryophytes. As plant species evolved, vegetative desiccation tolerance was lost as increased growth rates, structural and morphological complexity, and mechanisms that conserve water within the plant and maintain efficient carbon fixation were selected for. Genes that had evolved for cellular protection and repair were, in all likelihood, recruited for different but related processes such as response to water stress and the desiccation tolerance of reproductive propagules. We thus hypothesize that the mechanism of desiccation tolerance exhibited in seeds, a developmentally induced cellular protection system, evolved from the primitive form of vegetative desiccation tolerance. Once established in seeds, this system became available for induction in vegetative tissues by environmental cues related to drying. The more recent, modified vegetative desiccation tolerance mechanism in angiosperms evolved from that programmed into seed development as species spread into very arid environments. Most recently, certain desiccation-tolerant monocots evolved the strategy of poikilochlorophylly to survive and compete in marginal habitats with variability in water availability.     

Insights into the cellular mechanisms of desiccation tolerance among angiosperm resurrection plant species

Water is a major limiting factor in growth and reproduction in plants. The ability of tissues to survive desiccation is commonly found in seeds or pollen but rarely present in vegetative tissues. Resurrection plants are remarkable as they can tolerate almost complete water loss from their vegetative tissues such as leaves and roots. Metabolism is shut down as they dehydrate and the plants become apparently lifeless. Upon rehydration these plants recover full metabolic competence and ‘resurrect’. In order to cope with desiccation, resurrection plants have to overcome a number of stresses as water is lost from the cells, among them oxidative stress, destabilization or loss of membrane integrity and mechanical stress. This review will mainly focus on the effect of dehydration in angiosperm resurrection plants and some of the strategies developed by these plants to tolerate desiccation. Resurrection plants are important experimental models and understanding the physiological and molecular aspects of their desiccation tolerance is of great interest for developing drought‐tolerant crop species adapted to semi‐arid areas.     

Resurrection Plants and the Secrets of Eternal Leaf

Most higher plants possess a phase in their life cycle in whichtissues can survive desiccation. However, this is restrictedto specialized tissues such as seeds and pollen. Resurrectionplants are remarkable in that they can tolerate almost completewater loss in their vegetative tissues. The desiccated plantcan remain alive in the dried state for several years. However,upon watering the plants rehydrate and are fully functionalwithin 48 h. Underpinning this amazing ability is the capacityto accumulate large amounts of sucrose in the tissues. Thissugar has the property of stabilizing enzymes and cellular structuresin the absence of water. The sources of carbon that fuel sucrosesynthesis are not known, but temporary carbohydrate stores andphotosynthesis are the most likely candidates. On rewatering,the sucrose is metabolized rapidly as the tissues rehydrate.Increased expression of a number of genes in response to droughtstress have been noted. A number of these are associated withmetabolic pathways linked with primary carbohydrate metabolism.However, some genes related to LEA (Late Embryogenic Abundant)proteins have been isolated which suggests they too may playa role in maintaining tissue integrity during desiccation. Howthese mechanisms are integrated to enable resurrection plantsto survive desiccation is discussed. Copyright 2000 Annals ofBotany Company ABA, Craterostigma, desiccation tolerance, poikilohydric, resurrection.     

Optimal resource allocation to seeds and vegetative propagules under density-dependent regulation in Syneilesis palmata (Compositae)

Syneilesis palmata reproduces by both seeds and vegetative propagules (short rhizomes). The latter result in the production of new plants that are larger in size and hence have a higher survival probability and a higher growth rate than seeds. A previous study predicted that the optimal reproductive strategy, in terms of maximizing population growth rate (a fitness measure under no density regulations), was pure vegetative reproduction. However, high resource investment to vegetative propagules can cause local crowding resulting in reduced demographic performances of the plants, because the vegetative propagules of Syneilesis are produced close to one another. We examined, in this situation, the impact of allocating a certain proportion of reproductive resource to seeds with relatively greater capacity for dispersal. We simulated dynamics of hypothetical Syneilesis populations with various reproductive resource allocation balances (from pure seed to pure vegetative reproduction), using a density-dependent matrix model. In the model, it was assumed that plants from vegetative propagules experienced density-dependent reduction in their survival probabilities, but this was not the case for plants originating from seeds. Each allocation strategy was evaluated based on an equilibrium population density, a fitness measure under density-dependent regulations. The optimal reproductive strategy predicted was pure vegetative reproduction. Unrealistic conditions were required for seed reproduction to be favoured, such as the production of seeds one hundred times the normal number per unit resource investment. However, the conditions were fairly relaxed compared with those required in the model where no density effects were incorporated. This indicates that escape from local crowding is likely to be one of the roles of seed production in Syneilesis.     

Bayesian reconstruction of ancestral expression of the LEA gene families reveals propagule-derived desiccation tolerance in resurrection plants

Desiccation tolerance is a complex trait that is broadly but infrequently present throughout the evolutionary tree of life. Desiccation tolerance has played a significant role in land plant evolution, in both the vegetative and reproductive life history stages. In the land plants, the late embryogenesis abundant (LEA) gene families are involved in both abiotic stress tolerance and the development of reproductive propagules. They are also a major component of vegetative desiccation tolerance. Phylogenies were estimated for four families of LEA genes from Arabidopsis, Physcomitrella, and the desiccation tolerant plants Tortula ruralis, Craterostigma plantagineum, and Xerophyta humilis. Microarray expression data from Arabidopsis and a subset of the Physcomitrella LEAs were used to estimate ancestral expression patterns in the LEA families and to evaluate alternative hypotheses for the origins of vegetative desiccation tolerance in the flowering plants. The results contradict the idea that vegetative desiccation tolerance in the resurrection angiosperms Craterostigma and Xerophyta arose through the co-option of genes exclusively related to stress tolerance, and support the propagule-derived origin of vegetative desiccation tolerance in the resurrection plants.     

Constitutive expression of small heat shock proteins in vegetative tissues of the resurrection plant Craterostigma plantagineum

Using antibodies raised against two sunflower small heat shock proteins (sHSPs), we have detected immunologically related proteins in unstressed vegetative tissues from the resurrection plant Craterostigma plantagineum. In whole plants, further accumulation of these polypeptides was induced by heat-shock or water-stress. In desiccation-intolerant Craterostigma callus tissue, we failed to detect sHSP-related polypeptides, but their expression, and the concurrent acquisition of desiccation tolerance was induced by exogenous abscisic acid (ABA) treatment. In untressed plants, the cross-reacting polypeptides were abundant in the roots and lower part of the shoots, where they showed homogeneous tissue-distributions. This constitutive expression is novel for vegetative tissues of higher plants, and resembles the expression patterns of sHSPs in desiccation-tolerant zygotic embryos and germinating seeds.J.A. and C.A. contributed equally to this work and are both considered to be first author     

Overexpression of Arabidopsis thaliana LTL1, a salt-induced gene encoding a GDSL-motif lipase, increases salt tolerance in yeast and transgenic plants

Genes involved in the mechanisms of plant responses to salt stress may be used as biotechnological tools for the genetic improvement of salt tolerance in crop plants. This would help alleviate the increasing problem of salinization of lands cultivated under irrigation in arid and semi-arid regions. We have isolated a novel halotolerance gene from Arabidopsis thaliana, A. thaliana Li-tolerant lipase 1 (AtLTL1), on the basis of the phenotype of tolerance to LiCl conferred by its expression in yeast. AtLTL1 encodes a putative lipase of the GDSL-motif family, which includes bacterial and a very large number of plant proteins. In Arabidopsis, AtLTL1 expression is rapidly induced by LiCl or NaCl, but not by other abiotic stresses. Overexpression of AtLTL1 increases salt tolerance in transgenic Arabidopsis plants, compared to non-transformed controls, allowing germination of seeds in the presence of toxic concentrations of LiCl and NaCl, and stimulating vegetative growth, flowering and seed set in the presence of NaCl. These results clearly point to a role of AtLTL1 in the mechanisms of salt tolerance. In addition, we show that AtLTL1 expression is also activated, although only transiently, by salicylic acid (SA), suggesting that the lipase could also be involved in defence reactions against pathogens.     

Desiccation tolerant plants as model systems to study redox regulation of protein thiols

While the majority of plants and animals succumb to water loss, desiccation tolerant organisms can lose almost all of their intracellular water and revive upon rehydration. Only about 300 ‘resurrection’ angiosperms and very few animals are desiccation tolerant. By contrast, many bryophytes and most lichens are desiccation tolerant and so are the seeds and pollen grains of most flowering plants. The current literature reveals that the extreme fluctuations in water content experienced by desiccation tolerant organisms are accompanied by equally extreme changes in cellular redox state. Strongly oxidizing conditions upon desiccation can cause irreversible oxidation of free cysteine residues of proteins, which can change protein structure and function, and contribute to protein denaturation. It appears likely that reversible formation of disulphide bonds, in particular through protein glutathionylation, contributes to the set of protection mechanisms that confer desiccation tolerance. Upon rehydration, de-glutathionylation can be catalyzed by glutaredoxins (GRXs) and protein disulphide bonds can be reduced through NADPH-dependent thioredoxins (TRXs). Due to their ability to survive severe oxidative stress, desiccation tolerant plants and seeds are excellent models to study protein redox regulation, which may provide tools for enhancing tolerance to drought and more generally, to oxidative stress, in crops.     

Evolutionarily stable allocation to vegetative and sexual reproduction in plants

I apply the resource allocation approach to construct an ESS model aimed at predicting the rate of vegetative and sexual reproduction in plants. The model provides an integrated explanation of why the mode of reproduction should vary between populations and species, and what factors should affect the trade-off between ramet and seed production. It follows that seed production, usually considered to be less effective and more costly than ramet production, may be maintained in the population. The production of ramets should be favored when their recruitment rate is high or the costs are low. The intensity of vegetative reproduction is also related to conditions which affect seed production directly. The rate of ramet production should be inversely correlated with factors favoring sexual reproduction, such as lower cost of seeds or high opportunity for colonization of new patches, etc. Under such conditions it is beneficial to allocate more resources available for reproduction into seeds, at the expense of ramet production. The model emphasizes the need to consider both modes of plant reproduction whenever one of them is theoretically or empirically studied.     

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.     

Acclimation and adaptive responses of woody plants to environmental stresses

The predominant emphasis on harmful effects of environmental stresses on growth of woody plants has obscured some very beneficial effects of such stresses. Slowly increasing stresses may induce physiological adjustment that protects plants from the growth inhibition and/or injury that follow when environmental stresses are abruptly imposed. In addition, short exposures of woody plants to extreme environmental conditions at critical times in their development often improve growth. Furthermore, maintaining harvested seedlings and plant products at very low temperatures extends their longevity. Drought tolerance: Seedlings previously exposed to water stress often undergo less inhibition of growth and other processes following transplanting than do seedlings not previously exposed to such stress. Controlled wetting and drying cycles often promote early budset, dormancy, and drought tolerance. In many species increased drought tolerance following such cycles is associated with osmotic adjustment that involves accumulation of osmotically active substances. Maintenance of leaf turgor often is linked to osmotic adjustment. A reduction in osmotic volume at full turgor also results in reduced osmotic potential, even in the absence of solute accumulation. Changes in tissue elasticity may be important for turgor maintenance and drought tolerance of plants that do not adjust osmotically. Water deficits and nutrient deficiencies promote greater relative allocation of photosynthate to root growth, ultimately resulting in plants that have higher root:shoot ratios and greater capacity to absorb water and minerals relative to the shoots that must be supported. At the molecular level, plants respond to water stress by synthesis of certain new proteins and increased levels of synthesis of some proteins produced under well-watered conditions. Evidence has been obtained for enhanced synthesis under water stress of water-channel proteins and other proteins that may protect membranes and other important macromolecules from damage and denaturation as cells dehydrate. Flood tolerance: Both artificial and natural flooding sometimes benefit woody plants. Flooding of orchard soils has been an essential management practice for centuries to increase fruit yields and improve fruit quality. Also, annual advances and recessions of floods are crucial for maintaining valuable riparian forests. Intermittent flooding protects bottomland forests by increasing groundwater supplies, transporting sediments necessary for creating favorable seedbeds, and regulating decomposition of organic matter. Major adaptations for flood tolerance of some woody plants include high capacity for producing adventitious roots that compensate physiologically for decay of original roots under soil anaerobiosis, facilitation of oxygen uptake through stomata and newly formed lenticels, and metabolic adjustments. Halophytes can adapt to saline water by salt tolerance, salt avoidance, or both. Cold hardiness: Environmental stresses that inhibit plant growth, including low temperature, drought, short days, and combinations of these, induce cold hardening and hardiness in many species. Cold hardiness develops in two stages: at temperatures between 10° and 20°C in the autumn, when carbohydrates and lipids accumulate; and at subsequent freezing temperatures. The sum of many biochemical processes determines the degree of cold tolerance. Some of these processes are hormone dependent and induced by short days; others that are linked to activity of enzyme systems are temperature dependent. Short days are important for development of cold hardiness in species that set buds or respond strongly to photoperiod. Nursery managers often expose tree seedlings to moderate water stress at or near the end of the growing season. This accelerates budset, induces early dormancy, and increases cold hardiness. Pollution tolerance: Absorption of gaseous air pollutants varies with resistance to flow along the pollutant’s diffusion path. Hence, the amount of pollutant absorbed by leaves depends on stomatal aperture, stomatal size, and stomatal frequency. Pollution tolerance is increased when drought, dry air, or flooding of soil close stomatal pores. Heat tolerance: Exposure to sublethal high temperature can increase the thermotolerance of plants. Potential mechanisms of response include synthesis of heat-shock proteins and isoprene and antioxidant production to protect the photosynthetic apparatus and cellular metabolism. Breaking of dormancy: Seed dormancy can be broken by cold or heat. Embryo dormancy is broken by prolonged exposure of most seeds to temperatures of 1° to 15°C. The efficiency of treatment depends on interactions between temperature and seed moisture content. Germination can be postponed by partially dehydrating seeds or altering the temperature during seed stratification. Seed-coat dormancy can be broken by fires that rupture seed coats or melt seedcoat waxes, hence promoting water uptake. Seeds with both embryo dormancy and seed-coat dormancy may require exposure to both high and low temperatures to break dormancy. Exposure to smoke itself can also serve as a germination cue in breaking seed dormancy in some species. Bud dormancy of temperate-zone trees is broken by winter cold. The specific chilling requirement varies widely with species and genotype, type of bud (e.g., vegetative or floral bud), depth of dormancy, temperature, duration of chilling, stage of plant development, and daylength. Interruption of a cold regime by high temperature may negate the effect of sustained chilling or breaking of bud dormancy. Near-lethal heat stress may release buds from both endodormancy and ecodormancy. Pollen shedding: Dehiscence of anthers and release of pollen result from dehydration of walls of anther sacs. Both seasonal and diurnal pollen shedding are commonly associated with shrinkage and rupture of anther walls by low relative humidity. Pollen shedding typically is maximal near midday (low relative humidity) and low at night (high relative humidity). Pollen shedding is low or negligible during rainy periods. Seed dispersal: Gymnosperm cones typically dehydrate before opening. The cones open and shed seeds because of differential shrinkage between the adaxial and abaxial tissues of cone scales. Once opened, cones may close and reopen with changes in relative humidity. Both dehydration and heat are necessary for seed dispersal from serotinous (late-to-open) cones. Seeds are stored in serotinous cones because resinous bonds of scales prevent cone opening. After fire melts the resinous material, the cone scales can open on drying. Fires also stimulate germination of seeds of some species. Some heath plants require fire to open their serotinous follicles and shed seeds. Fire destroys the resin at the valves of follicles, and the valves then reflex to release the seeds. Following fire the follicles of some species require alternate wetting and drying for efficient seed dispersal. Stimulation of reproductive growth: Vegetative and reproductive growth of woody plants are negatively correlated. A heavy crop of fruits, cones, and seeds is associated with reduced vegetative growth in the same or following year (or even years). Subjecting trees to drought during early stages of fruit development to inhibit vegetative growth, followed by normal irrigation, sometimes favors reproductive growth. Short periods of drought at critical times not only induce formation of flower buds but also break dormancy of flower buds in some species. Water deficits may induce flowering directly or by inhibiting shoot flushing, thereby limiting the capacity of young leaves to inhibit floral induction. Postharvest water stress often results in abundant return bloom over that in well-irrigated plants. Fruit yields of some species are not reduced or are increased by withholding irrigation during the period of shoot elongation. In several species, osmotic adjustment occurs during deficit irrigation. In other species, increased fruit growth by imposed drought is not associated largely with osmotic adjustment and maintenance of leaf turgor. Seedling storage: Tree seedlings typically are stored at temperatures just above or below freezing. Growth and survival of cold-stored seedlings depend on such factors as: date of lifting from the nursery; species and genotype; storage temperature, humidity, and illumination; duration of storage; and handling of planting stock after storage. Seedlings to be stored over winter should be lifted from the nursery as late as possible. Dehydration of seedlings before, during, and after storage adversely affects growth of outplanted seedlings. Long-term storage of seedlings may result in depletion of stored carbohydrates by respiration and decrease of root growth potential. Although many seedlings are stored in darkness, a daily photoperiod during cold storage may stimulate subsequent growth and increase survival of outplanted seedlings. For some species, rapid thawing may decrease respiratory consumption of carbohydrates (over slowly thawed seedlings) and decrease development of molds. Pollen storage: Preservation of pollen is necessary for insurance against poor flowering years, for gene conservation, and for physiological and biochemical studies. Storage temperature and pollen moisture content largely determine longevity of stored pollen. Pollen can be stored successfully for many years in deep freezers at temperatures near −15°C or in liquid nitrogen (−196°C). Cryopreservation of pollen with a high moisture content is difficult because ice crystals may destroy the cells. Pollens of many species do not survive at temperatures below −40°C if their moisture contents exceed 20–30%. Pollen generally is air dried, vacuum dried, or freeze dried before it is stored. To preserve the germination capacity of stored pollen, rehydration at high humidity often is necessary. Seed storage: Seeds are routinely stored to provide a seed supply during years of poor seed production, to maintain genetic diversity, and to breed plants. For a long time, seeds were classified as either orthodox (relatively long-lived, with capacity for dehydration to very low moisture contents without losing viability) or recalcitrant (short-lived and requiring a high moisture content for retention of viability). More recently, some seeds have been reclassified as suborthodox or intermediate because they retain viability when carefully dried. True orthodox seeds are preserved much more easily than are nonorthodox seeds. Orthodox seeds can be stored for a long time at temperatures between 2° and −20°C, with temperatures below −5°C preferable. Some orthodox seeds have been stored at superlow temperatures, although temperatures of −40°, −70°, or −196°C have not been appreciably better than −20°C for storage of seeds of a number of species. Only relatively short-term storage protocols have been developed for nonorthodox seeds. These treatments typically extend seed viability to as much as a year. The methods often require cryopreservation of excised embryos. Responses to cryopreservation of nonorthodox seeds or embryos vary with species and genotype, rate of drying, use of cryoprotectants, rates of freezing and thawing, and rate of rehydration. Fruit storage: Storing fruits at low temperatures above freezing, increasing the CO₂ concentration, and lowering the O₂ concentration of fruit storage delays senescence of fruits and prolongs their life. Fruits continue to senesce and decay while in storage and become increasingly susceptible to diseases. Both temperate-zone and tropical fruits may develop chilling injury characterized by lesions, internal discoloration, greater susceptibility to decay, and shortened storage life. Chilling injury can be controlled by chemicals, temperature conditioning, and intermittent warming during storage. Stored fruits may become increasingly susceptible to disease organisms. Fruit diseases can be controlled by cold, which inhibits growth of microorganisms and maintains host resistance. Exposure of fruits to high CO₂ and low O₂ during storage directly suppresses disease-causing fungi. Pathogens also can be controlled by exposing fruits to heat before, during, and after storage. Scald that often develops during low-temperature storage can be controlled by chemicals and by heat treatments.     

Drought- and desiccation-induced modulation of gene expression in plants

Desiccation is the extreme form of dehydration. Tolerance of desiccation is acquired by seeds and in resurrection plants, a small group of angiosperms. Desiccation tolerance is the result of a complex cascade of molecular events, which can be divided into signal perception, signal transduction, gene activation and biochemical alterations leading to acquisition of tolerance. Many of these molecular processes are also observed during the dehydration of non-tolerant plants. Here we try to give an overview of the gene expression programmes that are triggered by dehydration, with particular reference to protective molecules and the regulation of their expression. Potential transgenic approaches to manipulating stress tolerance are discussed.     

Conservation between higher plants and the moss <Emphasis Type="Italic">Physcomitrella patens</Emphasis>in response to the phytohormone abscisic acid: a proteomics analysis

Background  

The plant hormone abscisic acid (ABA) is ubiquitous among land plants where it plays an important role in plant growth and development. In seeds, ABA induces embryogenesis and seed maturation as well as seed dormancy and germination. In vegetative tissues, ABA is a necessary mediator in the triggering of many of the physiological and molecular adaptive responses of the plant to adverse environmental conditions, such as desiccation, salt and cold.     

Quantitative genetics of seed size variation inPhlox

Summary Because seed size is often associated with survival and reproduction in plant populations, genetic variation for seed size may be reduced or eliminated by natural selection. To test this hypothesis we assessed genetic sources of variation in seed size in a population ofPhlox drummondii to determine whether genetic differences among seeds influence the size they attain. A diallel cross among 12 plants from a population at Bastrop, Texas, USA allowed us to partition variance in the mass of seeds among several genetic and parental effects. We found no evidence of additive genetic variance or dominance genetic variance for seed mass in the contribution of plants to their offspring. Extranuclear maternal effects accounted for 56% of the variance in seed mass. A small interaction was observed between seed genotype and maternal plant. Results of this study support theory that predicts little genetic variation for traits associated with fitness.