Desiccation Tolerance In Bryophytes Research Articles

Proteomic and Transcriptomic Responses of the Desiccation-Tolerant Moss Racomitrium canescens in the Rapid Rehydration Processes.

The moss Racomitrium canescens (R. canescens) has strong desiccation tolerance. It can remain desiccated for years and yet recover within minutes of rehydration. Understanding the responses and mechanisms underlying this rapid rehydration capacity in bryophytes could identify candidate genes that improve crop drought tolerance. We explored these responses using physiology, proteomics, and transcriptomics. Label-free quantitative proteomics comparing desiccated plants and samples rehydrated for 1 min or 6 h suggesting that damage to chromatin and the cytoskeleton had occurred during desiccation, and pointing to the large-scale degradation of proteins, the production of mannose and xylose, and the degradation of trehalose immediately after rehydration. The assembly and quantification of transcriptomes from R. canescens across different stages of rehydration established that desiccation was physiologically stressful for the plants; however, the plants recovered rapidly once rehydrated. According to the transcriptomics data, vacuoles appear to play a crucial role in the early stages of R. canescens recovery. Mitochondria and cell reproduction might recover before photosynthesis; most biological functions potentially restarted after ~6 h. Furthermore, we identified novel genes and proteins related to desiccation tolerance in bryophytes. Overall, this study provides new strategies for analyzing desiccation-tolerant bryophytes and identifying candidate genes for improving plant drought tolerance.

Desiccation tolerance in bryophytes relates to elasticity but is independent of cell wall thickness and photosynthesis.

Mosses have been found outliers of the trade‐off between photosynthesis and bulk elastic modulus described for vascular plants. Hence, potential trade‐offs among physical features of cell walls and desiccation tolerance, water relations, and photosynthesis were assessed in bryophytes and other poikilohydric species. Long‐term desiccation tolerance was quantified after variable periods of desiccation/rehydration cycles. Water relations were analyzed by pressure–volume curves. Mesophyll conductance was estimated using both CO2 curve‐fitting and anatomical methods. Cell wall elasticity was the parameter that better correlated with the desiccation tolerance index for desiccation tolerant species and was antagonistic to higher absolute values of osmotic potential. Although high values of cell wall effective porosity were estimated compared with the values assumed for vascular plants, the desiccation tolerance index negatively correlated with the porosity in desiccation tolerant bryophytes. Neither cell wall thickness nor photosynthetic capacity were correlated with the desiccation tolerance index of the studied species. The existence of a potential evolutionary trade‐off between cell wall thickness and desiccation tolerance is rejected. The photosynthetic capacity reported for bryophytes is independent of elasticity and desiccation tolerance. Furthermore, the role of cell wall thickness in limiting CO2 conductance would be overestimated under a scenario of high cell wall porosity for most bryophytes.

Archetypal Roles of an Abscisic Acid Receptor in Drought and Sugar Responses in Liverworts.

Abscisic acid (ABA) controls seed dormancy and stomatal closure through binding to the intracellular receptor Pyrabactin resistance1 (Pyr1)/Pyr1-like/regulatory components of ABA receptors (PYR/PYL/RCAR) in angiosperms. Genes encoding PYR/PYL/RCAR are thought to have arisen in the ancestor of embryophytes, but the roles of the genes in nonvascular plants have not been determined. In the liverwort Marchantia polymorpha, ABA reduces growth and enhances desiccation tolerance through increasing accumulation of intracellular sugars and various transcripts such as those of Late Embryogenesis Abundant (LEA)-like genes. In this study, we analyzed a gene designated MpPYL1, which is closely related to PYR/PYL/RCAR of angiosperms, in transgenic liverworts. Transgenic lines overexpressing MpPYL1-GFP showed ABA-hypersensitive growth with enhanced desiccation tolerance, whereas Mppyl1 generated by CRISPR-Cas9-mediated genome editing showed ABA-insensitive growth with reduced desiccation tolerance. Transcriptome analysis indicated that MpPYL1 is a major regulator of abiotic stress-associated genes, including all 35 ABA-induced LEA-like genes. Furthermore, these transgenic plants showed altered responses to extracellular Suc, suggesting that ABA and PYR/PYL/RCAR function in sugar responses. The results presented here reveal an important role of PYR/PYL/RCAR in the ABA response, which was likely acquired in the common ancestor of land plants. The results also indicate the archetypal role of ABA and its receptor in sugar response and accumulation processes for vegetative desiccation tolerance in bryophytes.

The role of prehydration in rescuing shoots of mosses damaged by extreme desiccation events: Syntrichia norvegica (Pottiaceae)

While regarded as a principal factor of desiccation tolerance in bryophytes (along with rate of drying, water content and duration dry), the rate of rehydration has been broadly neglected or inadequately assessed. Prior to receiving liquid water from a rain event, desiccated bryophytes are able to partially rehydrate their tissues by absorbing water vapor when ambient relative humidity is high, a process known as prehydration. A single clone of Syntrichia norvegica was cultured for 4–6 months in a suprasaturated condition. Shoot apices were used in experimental prehydrating (1–48 h), drying (5 min–300 h, equilibrating at ∼0% relative humidity), and duration dry (0–42 d continuously dry at 54% RH) series. Shoots were subsequently prehydrated 24 h prior to exposure to liquid water or directly immersed in liquid water and assessed for desiccation associated damage. Prehydration occurs over a 4-h period, after which shoot water content levels out. Shoots that normally die when equilibrated at low water contents were rescued with a prehydration treatment. At extremely rapid rates of drying (<20 min) prehydration effects were limited. However, at gradual rates of drying the prehydration treatment restored chlorophyll fluorescence and regeneration capacity to near control levels. Prehydration also improved the capacity of a shoot to recover following continuously dry episodes of several weeks. Without a prehydration treatment, shoot apices of the moss Syntrichia norvegica were killed by desiccation to equilibrium with 0% RH, and severely damaged upon rehydration from a 42-d dry period. With a prehydration treatment, both of these scenarios were mitigated. For the prehydration treatment to be effective, a rate of drying only of 30 or more minutes from full turgor without external free water to leaf curling achieves a significant lessening of damage.

Desiccation tolerance in bryophytes: the rehydration proteomes of Bryum argenteum provide insights into the resuscitation mechanism

Bryum argenteum Hedw. is a desiccation tolerant bryophyte and belongs to one of the most important components of the biological soil crusts (BSCs) found in the deserts of Central Asia. Limited information is available on rehydration-responsive proteins in desiccation tolerant plants. As a complement to our previous research analyzing the rehydration transcriptome, we present a parallel quantitative proteomic effort to study rehydration-responsive proteins. Bryophyte gametophores were desiccated (Dry) and rehydrated for 2 h (R2) and 24 h (R24). Proteins from Dry, R2 and R24 gametophores were labeled by isobaric tags for relative and absolute quantitation (iTRAQ) to determine the relative abundance of rehydration-responsive proteins. A total of 5503 non-redundant protein sequences were identified and 4772 (86.7%) protein sequences were annotated using Gene Ontology (GO) terms and Pfam classifications. Upon rehydration 239 proteins were elevated and 461 proteins were reduced as compared to the desiccated protein sample. Differentially up-regulated proteins were classified into a number of categories including reactive oxygen species scavenging enzymes, detoxifying enzymes, Late Embryogenesis Abundant (LEA) proteins, heat shock proteins, proteasome components and proteases, and photosynthesis and translation related proteins. Furthermore, the results of the correlation between transcriptome and proteome revealed the discordant changes in the expression between protein and mRNA.

Mechanisms Underlying Freezing and Desiccation Tolerance in Bryophytes.

Bryophytes are small land plants that have many morphological and physiological features different from vascular plants. With distinct water relations of bryophytes, many bryophyte species exhibit high degrees of tolerance to freezing and desiccation. The tolerance is sustained by the constitutive repair mechanism and the inducible mechanism regulated by environmental signals that provoke specific responses within the cells. Bryophyte cells sense changes in environmental conditions such as decreases in osmotic potential and temperature and that some responses are likely to be mediated by the stress hormone, abscisic acid. Due to their simple structures and high degrees of dehydration tolerance, bryophytes are useful for physiological studies on abiotic stress response and also for analysis of signal sensing and transduction of environmental signals. Furthermore, the basal phylogenetic position of bryophytes in land plants provides many insights into the evolutionary events for conquest of land by the ancestors of plants and subsequent diversification of species as well as their survival strategies in the terrestrial environment.

Ecology of desiccation tolerance in bryophytes: A conceptual framework and methodology

Bryophytes have long been understood to be desiccation tolerant (capable of reviving from an air-dry state, DT). While mechanistic studies focusing on the expression of this complex trait are numerous over the last 50 years, a firm conceptual framework for the ecology of desiccation tolerance in bryophytes has lagged behind. As a result of this, mechanistic studies have gone ahead without an ecological foundation, and this path can be scientifically risky. The motivating elements for this article include (1) the low visibility and lack of implementation of a conceptual framework for studying the ecology of DT in bryophytes, (2) the lack of a protocol for the step-by-step handling of field-collected or laboratory cultured specimens for study of desiccation tolerance with particular attention to the deacclimation of plants, (3) a recognition that most studies of desiccation tolerance tend to conflate two of the most important factors of desiccation, rate of desiccation and water content, and (4) recognizing that the ecological factors of rehydration, aside from recovery, are nearly always ignored in experiments on desiccation tolerance in bryophytes. Therefore this review postulates a conceptual framework for the ecology of desiccation tolerance, presenting the principal factors of desiccation (rate of drying, water content at equilibration, duration dry, and rate of rehydration) and how they may interact, presenting the principal physiological phases of rehydration (recovery, hardening, dehardening), and highlighting the importance of specimen handling in preparation for an experiment on DT. Useful metrics for assessment are derived that include the minimum rate of drying tolerated at a given water content, the minimum or maximum water content tolerated, the maximum duration dry tolerated, and the minimum dehardening time exhibited.

Ecology of desiccation tolerance in bryophytes: A conceptual framework and methodology

Ecology of desiccation tolerance in bryophytes: A conceptual framework and methodology

Dehydration rate determines the degree of membrane damage and desiccation tolerance in bryophytes.

Desiccation tolerant (DT) organisms are able to withstand an extended loss of body water and rapidly resume metabolism upon rehydration. This ability, however, is strongly dependent on a slow dehydration rate. Fast dehydration affects membrane integrity leading to intracellular solute leakage upon rehydration and thereby impairs metabolism recovery. We test the hypothesis that the increased cell membrane damage and membrane permeability observed under fast dehydration, compared with slow dehydration, is related to an increase in lipid peroxidation. Our results reject this hypothesis because following rehydration lipid peroxidation remains unaltered, a fact that could be due to the high increase of NO upon rehydration. However, in fast-dried samples we found a strong signal of red autofluorescence upon rehydration, which correlates with an increase in ROS production and with membrane leakage, particularly the case of phenolics. This could be used as a bioindicator of oxidative stress and membrane damage.

Integrating Herbicides and Re-seeding to Restore Rangeland Infested by an Invasive Forb-Annual Grass Complex

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Group A PP2Cs evolved in land plants as key regulators of intrinsic desiccation tolerance

Vegetative desiccation tolerance is common in bryophytes, although this character has been lost in most vascular plants. The moss Physcomitrella patens survives complete desiccation if treated with abscisic acid (ABA). Group A protein phosphatases type 2C (PP2C) are negative regulators of abscisic acid signalling. Here we show that the elimination of Group A PP2C is sufficient to ensure P. patens survival to full desiccation, without ABA treatment, although its growth is severely hindered. Microarray analysis shows that the Group A PP2C-regulated genes exclusively overlap with genes exhibiting a high level of ABA induction. Group A PP2C disruption weakly affects ABA-activated kinase activity, indicating Group A PP2C action downstream of these kinases in the moss. We propose that Group A PP2C emerged in land plants to repress desiccation tolerance mechanisms, possibly facilitating plants propagation on land, whereas ABA releases the intrinsic desiccation tolerance from Group A PP2C regulation.

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 repea...

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.

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.