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.     

更苏被子植物的光合作用

更苏植物是一类在极度干燥条件下组织会迅速脱水后遇水又能很快复苏的植物.极少数被子植物有这种能力,在双子叶植物中尤其罕见,而且脱水时叶绿素含量和叶绿体完整性变化较少,称为叶绿素保持型(HDT).该类植物的复苏机理简单,研究方便,因而得到更广泛注意.更苏被子植物光合作用的最新研究进展说明,光化学活性是研究更苏植物脱水复苏生理状态的灵敏指标.和普通植物一样,在光下,更苏被子植物的光化学活性随着叶片失水而受到抑制,但奇怪的是在失去95%以上的水分后复水仍可迅速复活.在脱水过程中叶黄素循环和抗氧化系统的上调以及光合膜完整性和稳定性的保持,可能对更苏被子植物的耐脱水性起非常重要的作用.磷酸盐对复苏的影响也表现在复水阶段而且与上述两种保护机理关系不大,因此应该加强更苏被子植物复水阶段的研究.     

更苏被子植物的光合作用

更苏植物是一类在极度干燥条件下组织会迅速脱水后遇水又能很快复苏的植物。极少数被子植物有这种能力,在双子叶植物中尤其罕见,而且脱水时叶绿素含量和叶绿体完整性变化较少,称为叶绿素保持型(HDT)。该类植物的复苏机理简单,研究方便,因而得到更广泛注意。更苏被子植物光合作用的最新研究进展说明,光化学活性是研究更苏植物脱水复苏生理状态的灵敏指标。和普通植物一样,在光下,更苏被子植物的光化学活性随着叶片失水而受到抑制,但奇怪的是在失去95％以上的水分后复水仍可迅速复活。在脱水过程中叶黄素循环和抗氧化系统的上调以及光合膜完整性和稳定性的保持,可能对更苏被子植物的耐脱水性起非常重要的作用。磷酸盐对复苏的影响也表现在复水阶段而且与上述两种保护机理关系不大,因此应该加强更苏被子植物复水阶段的研究。     

Maintenance or Collapse: Responses of Extraplastidic Membrane Lipid Composition to Desiccation in the Resurrection Plant Paraisometrum mileense

Resurrection plants usually grow in specific or extreme habitats and have the capacity to survive almost complete water loss. We characterized the physiological and biochemical responses of Paraisometrum mileense to extreme desiccation and found that it is a resurrection plant. We profiled the changes in lipid molecular species during dehydration and rehydration in P. mileense, and compared these with corresponding changes in the desiccation-sensitive plant Arabidopsis thaliana. One day of desiccation was lethal for A. thaliana but not for P. mileense. After desiccation and subsequent rewatering, A. thaliana showed dramatic lipid degradation accompanied by large increases in levels of phosphatidic acid (PA) and diacylglycerol (DAG). In contrast, desiccation and rewatering of P. mileense significantly decreased the level of monogalactosyldiacylglycerol and increased the unsaturation of membrane lipids, without changing the level of extraplastidic lipids. Lethal desiccation in P. mileense caused massive lipid degradation, whereas the PA content remained at a low level similar to that of fresh leaves. Neither damage nor repair processes, nor increases in PA, occurred during non-lethal desiccation in P. mileense. The activity of phospholipase D, the main source of PA, was much lower in P. mileense than in A. thaliana under control conditions, or after either dehydration or rehydration. It was demonstrated that low rates of phospholipase D-mediated PA formation in P. mileense might limit its ability to degrade lipids to PA, thereby maintaining membrane integrity following desiccation.     

Non-disaccharide-based mechanisms of protection during drying

Few tissues or organisms can survive the removal of nearly all their intra and extracellular water. These few have developed specialized adaptations to protect their cellular components from the damage caused by desiccation and rehydration. One mechanism, common to almost all such organisms, is the accumulation of disaccharides within cells and tissues at the onset of dehydration. This adaptation has been extensively studied and will not be considered in this review. It has become increasingly clear that true desiccation tolerance is likely to involve several mechanisms working in concert; thus, we will highlight several other important and complimentary adaptations found especially in the dehydration-resistant tissues of higher plants. These include the scavenging of reactive oxygen species, the down-regulation of metabolism, and the accumulation of certain amphiphilic solutes, proteins, and polysaccharides.     

Dehydration-responsive features of <Emphasis Type="Italic">Atrichum undulatum</Emphasis>

Drought is an increasingly important limitation on plant productivity worldwide. Understanding the mechanisms of drought tolerance in plants can lead to new strategies for developing drought-tolerant crops. Many moss species are able to survive desiccation—a more severe state of dehydration than drought. Research into the mechanisms and evolution of desiccation tolerance in basal land plants is of particular significance to both biology and agriculture. In this study, we conducted morphological, cytological, and physiological analyses of gametophytes of the highly desiccation-tolerant bryophyte Atrichum undulatum (Hedw.) P. Beauv during dehydration and rehydration. Our results suggested that the mechanisms underlying the dehydration–recovery cycle in A. undulatum gametophytes include maintenance of membrane stability, cellular structure protection, prevention of reactive oxygen species (ROS) generation, elimination of ROS, protection against ROS-induced damage, and repair of ROS-induced damage. Our data also indicate that this dehydration–recovery cycle consists not only of the physical removal and addition of water, but also involves a highly organized series of cytological, physiological, and biochemical changes. These attributes are similar to those reported for other drought- and desiccation-tolerant plant species. Our findings provide major insights into the mechanisms of dehydration-tolerance in the moss A. undulatum.     

两种不同生境苦苣苔科植物的复苏特性及其对水分的光合和生理响应

复苏植物可以耐受极度干旱的环境,脱水至10％相对水分含量后仍然可以复苏.苦苣苔科植物包含有较多复苏植物,不同类群的复苏机理可能存在差异.该文选择分布在亚热带和温带石灰岩地区的锈色蛛毛苣苔(Paraboea rufescens)和心叶马铃苣苔(Oreocharis cordatula)两种苦苣苔科植物,并对这两个物种的叶...     

植物复苏性状的分子机理研究进展

复苏性状是某些生物应对水分剧烈变化恶劣环境的一种特殊适应能力,在植物界广泛分布于苔藓和蕨类低等植物,一些高等植物也具有这种性状。复苏植物可以在损失体内95％以上的水分后,遇水而复苏,以此度过环境恶劣的时段。复苏性状的分子机制一直让人们着迷,但对其认知还十分有限。近年来的研究表明,一些小分子代谢物和特殊蛋白的大量积累在复苏植物脱水过程中对生物膜和大分子结构起保护作用;复苏性状中的信号转导与基因调控可能包括ABA在内的一系列信号分子和途径。随着“组学”技术的发展,更宽广角度的研究将会极大的促进人们对复苏性状的认知。对于复苏性状的深入研究,可能为农作物和蔬菜的改良提供一个全新的方向,具有很大的潜在应用价值。     

Ultrastructural responses of the desiccation tolerant plants Xerophyta viscosa and X. retinervis to dehydration and rehydration

This paper compares the changes in water content, chlorophyll a fluorescence and leaf ultrastructure during dehydration and rehydration in two desiccation tolerant plants Xerophyta viscosa and X. retinervis. Both species showed decreasing quantum efficiency of photosystem 2 (F_v/F_m) with decreasing water content. Extreme water loss observed after 25 d of dehydration resulted in considerable damage of leaf tissue ultrastructure. After rehydration, both species need several days to reconstitute their photosynthetic machinery.     

Composition and desiccation-induced alterations of the cell wall in the resurrection plant Craterostigma wilmsii

Resurrection plants have the unique capacity to revive from an air-dried state. In order to tolerate desiccation they have to overcome a number of stresses, mechanical stress being one. In leaves of the Craterostigma species, an extensive shrinkage occurs during drying as well as a considerable cell wall folding. Our previous microscopically analysis using immunocytochemistry on the resurrection plant Craterostigma wilmsii , has shown an increase in labelling of xyloglucan and unesterified pectins in the cell wall during drying. In this study, we have undertaken a biochemical approach to separate, quantify and characterize major cell wall polysaccharides in fully hydrated and dry leaves of C. wilmsii . Our results show that the overall cell wall composition of C. wilmsii leaves was similar to that of other dicotyledonous plants with respect to the pectin content. However, the structure of the hemicellulosic polysaccharide xyloglucan was characterized to be XXGG-type. The data also demonstrate marked changes in the hemicellulosic wall fraction from dry plants compared to hydrated ones. The most conspicuous change was a decrease in glucose content in the hemicellulosic fraction of dry plants. In addition, xyloglucan from the cell wall of dry leaves was relatively more substituted with galactose than in hydrated walls. Together these findings show that dehydration induces significant alteration of polysaccharide content and structure in the cell wall of C. wilmsii , which in turn might be involved in the modulation of the mechanical properties of the wall during dehydration.     

Photosynthetic activity of homoiochlorophyllous desiccation tolerant plant <Emphasis Type="Italic">Haberlea rhodopensis</Emphasis> during dehydration and rehydration

The functional state of the photosynthetic apparatus of flowering homoiochlorophyllous desiccation tolerant plant Haberlea rhodopensis during dehydration and subsequent rehydration was investigated in order to characterize some of the mechanisms by which resurrection plants survive drought stress. The changes in the CO₂ assimilation rate, chlorophyll fluorescence parameters, thermoluminescence, fluorescence imaging and electrophoretic characteristics of the chloroplast proteins were measured in control, moderately dehydrated (50% water content), desiccated (5% water content) and rehydrated plants. During the first phase of desiccation the net CO₂ assimilation decline was influenced by stomatal closure. Further lowering of net CO₂ assimilation was caused by both the decrease in stomatal conductance and in the photochemical activity of photosystem II. Severe dehydration caused inhibition of quantum yield of PSII electron transport, disappearance of thermoluminescence B band and mainly charge recombination related to S₂Q_A⁻ takes place. The blue and green fluorescence emission in desiccated leaves strongly increased. It could be suggested that unchanged chlorophyll content and amounts of chlorophyll–proteins, reversible modifications in PSII electron transport and enhanced probability for non-radiative energy dissipation as well as increased polyphenolic synthesis during desiccation of Haberlea contribute to drought resistance and fast recovery after rehydration.     

Proteome analysis of leaves from the resurrection plant <Emphasis Type="Italic">Boea hygrometrica</Emphasis> in response to dehydration and rehydration

Resurrection plants differ from other species in their unique ability to survive desiccation. In order to understand the mechanisms of desiccation tolerance, proteome studies were carried out using leaves of the resurrection plant Boea hygrometrica to reveal proteins that were differentially expressed in response to changes in relative water content. This opportunity was afforded by the rare ability of excised B. hygrometrica leaves to survive and resume metabolism following desiccation in a manner similar to intact plants. From a total of 223 proteins that were reproducibly detected and analyzed, 35% showed increased abundance in dehydrated leaves, 5% were induced in rehydrated leaves and 60% showed decreased or unchanged abundance in dehydrated and rehydrated leaves. Since the induction kinetics fall into clearly defined patterns, we suggest that programmed regulation of protein expression triggered by changes of water status. Fourteen dehydration responsive proteins were analyzed by mass spectrometry. Eight proteins were classified as playing a role in reactive oxygen species scavenging, photosynthesis and energy metabolism. In agreement with these findings, glutathione content and polyphenol oxidase activity were found to increase upon dehydration and rapid recovery of photosynthesis was observed.     

Resurrection Plants: The Puzzle of Surviving Extreme Vegetative Desiccation

Tolerance to near complete desiccation of vegetative organs is a widespread capability in bryophytes and is also shared by a small group of vascular plants known as resurrection plants. To date more than 300 species, belonging to pteridophytes and angiosperms, have been identified that possess this kind of desiccation-tolerance. The vegetative desiccation-tolerance of resurrection plants is an inductive process displayed only under environmental stress with or without the involvement of abscisic acid as molecular signal. The different problems associated with desiccation encountered by resurrection plants render the employment of many interacting mechanisms necessary. Preservation of cell order and correct structure of membranes and macromolecules is underpinned by the synthesis of large amounts of sugars, amino acids, and small polypeptides such as late embryogenesis abundant (LEA) proteins and dehydrins. Some of these compatible solutes, such as sucrose and LEA proteins, are also involved in cytoplasm vitrification, which occurs during the last phase of desiccation. Mechanical damage due to vacuole shrinkage in dehydrating cells is avoided by cell wall folding or by replacing the water in vacuoles with nonaqueous substances. Oxidative stress, due to enhanced production of reactive oxygen species (ROS) especially by chloroplasts, is minimized through two different strategies. The homoiochlorophyllous resurrection plants, which conserve chloroplasts with chlorophylls and thylakoids upon drying, fold leaf blades and synthesize anthocyanins, as both sunscreens and free radical scavengers, and additionally increase the activity of antioxidant systems in cells. In contrast, the chloroplasts in poikilochlorophyllous species degrade chlorophylls and thylakoid membranes yielding desiccoplasts that are devoid of any internal structures. These adaptive mechanisms preserve cells from damage by desiccation and allow them to resume vital functions once rehydrated. Even if based mainly on cell protection during drying, the vegetative desiccation-tolerance of resurrection plants also relies on systems of cell recovery and repair upon rehydration. However, most of these systems are prepared during cell dehydration.     

Factors Inducing Successful Anhydrobiosis in the African Chironomid Polypedilum vanderplanki: Significance of the Larval Tubular Nest

The African chironomid Polypedilum vanderplanki exhibits anhydrobiosis,i.e., the larvae can survive complete desiccation. Recoveryrate and trehalose content were investigated in larvae desiccatedslowly or at a rate more than 3 times faster. Upon slow desiccation(evaporation rate 0.22 ml day^–1) larvae synthesized 38µg trehalose/individual before complete desiccation, andall of them recovered after rehydration, whereas larvae thatwere dehydrated quickly (evaporation rate 0.75 ml day^–1)accumulated only 6.8 µg trehalose/individual and noneof them revived after rehydration. In the pools that are theirnatural habitat P. vanderplanki larvae make tubes by incorporatingdetritus or soil with their sticky saliva. This tubular structureis a physical barrier not only to protect the larva from naturalenemies but also induces successful anhydrobiosis by reducingthe dehydration rate. When larvae were dehydrated with 100 µldistilled water (DW) in soil tubes, they accumulated 37 µgtrehalose/individual and more than half of them could reviveafter rehydration, whereas larvae without tubes accumulatedlower level of trehalose and none recovered after rehydration.