Unexplored dimensions of variability in vegetative desiccation tolerance

Desiccation tolerance has evolved recurrently across diverse land plant lineages as an adaptation for survival in regions where seasonal rainfall drives periodic drying of vegetative tissues. Growing interest in this phenomenon has fueled recent physiological, biochemical, and genomic insights into the mechanistic basis of desiccation tolerance. Although, desiccation tolerance is often viewed as binary and monolithic, substantial variation exists in the phenotype and underlying mechanisms across diverse lineages, heterogeneous populations, and throughout the development of individual plants. Most studies have focused on conserved responses in a subset desiccation-tolerant plants under laboratory conditions. Consequently, the variability and natural diversity of desiccation-tolerant phenotypes remains largely uncharacterized. Here, we discuss the natural variation in desiccation tolerance and argue that leveraging this diversity can improve our mechanistic understanding of desiccation tolerance. We summarize information collected from ~600 desiccation-tolerant land plants and discuss the taxonomic distribution and physiology of desiccation responses. We point out the need to quantify natural diversity of desiccation tolerance on three scales: variation across divergent lineages, intraspecific variation across populations, and variation across tissues and life stages of an individual plant. We conclude that this variability should be accounted for in experimental designs and can be leveraged for deeper insights into the intricacies of desiccation tolerance.     

The signature of seeds in resurrection plants: a molecular and physiological comparison of desiccation tolerance in seeds and vegetative tissues

Desiccation-tolerance in vegetative tissues of angiosperms hasa polyphyletic origin and could be due to 1) appropriation ofthe seed-specific program of gene expression that protects orthodoxseeds against desiccation, and/or 2) a sustainable version ofthe abiotic stress response. We tested these hypotheses by comparingmolecular and physiological data from the development of orthodoxseeds, the response of desiccation-sensitive plants to abioticstress, and the response of desiccation-tolerant plants to extremewater loss. Analysis of publicly-available gene expression dataof 35 LEA proteins and 68 anti-oxidant enzymes in the desiccation-sensitiveArabidopsis thaliana identified 13 LEAs and 4 anti-oxidantsexclusively expressed in seeds. Two (a LEA6 and 1-cys-peroxiredoxin)are not expressed in vegetative tissues in A. thaliana, buthave orthologues that are specifically activated in desiccatingleaves of Xerophyta humilis. A comparison of antioxidant enzymeactivity in two desiccation-sensitive species of Eragrostiswith the desiccation-tolerant E. nindensis showed equivalentresponses upon initial dehydration, but activity was retainedat low water content in E. nindensis only. We propose that theseantioxidants are housekeeping enzymes and that they are protectedfrom damage in the desiccation-tolerant species. Sucrose isconsidered an important protectant against desiccation in orthodoxseeds, and we show that sucrose accumulates in drying leavesof E. nindensis, but not in the desiccation-sensitive Eragrostisspecies. The activation of "seed-specific" desiccation protectionmechanisms (sucrose accumulation and expression of LEA6 and1-cys-peroxiredoxin genes) in the vegetative tissues of desiccation-tolerantplants points towards acquisition of desiccation tolerance fromseeds.     

The discovery,scope, and puzzle of desiccation tolerance in plants

The modern scientific study of desiccation tolerance began in 1702 when Anthony von Leeuwenhoek discovered that rotifers could survive without water for months. By 1860, the controversy over whether organisms could dry up without dying had reached such a pitch that a special French commission was convened to adjudicate the dispute. In 2000, we know that a few groups of animals and a wide variety of plants can tolerate desiccation in the active, adult stages of their life cycles. Among plants, this includes many lichens and bryophytes, a few ferns, and a very few flowering plants, but no gymnosperms nor trees. Some desiccation-tolerant species can survive without water for over ten years, recover from desiccation to unmeasurably low water potentials, and, when plants are desiccated, endure temperature extremes from ?272 to 100 °C. Desiccation-tolerant plants occur on all continents but mainly in xeric habitats or microhabitats where the cover of desiccation-sensitive species is low. Two main puzzles arise from these patterns: What are the mechanisms by which plants tolerate desiccation? and Why are desiccation-tolerant plants not more ecologically widespread? Recent molecular and biochemical studies suggest that there are multiple mechanisms of tolerance, many of which involve protection from oxidants and from the loss of configuration of macromolecules during dehydration. Hypotheses to explain the restricted ecological range of desiccation-tolerance plants include inability to maintain a cumulative positive carbon balance during repeated cycles of wetting and drying and inherent trade offs between desiccation tolerance and growth rate.

     

Chloroplast evolution in algae and land plants

Eukaryotes contain a chimeric assembly of genomes, each localized in a specialized subcellular compartment. The successful survival of an organism requires that these sequestered genomes be viewed as dependent variables in a coevolutionary complex. This discussion focuses on chloroplast evolution. A selected review of information available on chloroplast diversity is presented, followed by an analysis of the genetic modifications which may have occurred in the conversion of a free-living ancestral photosynthetic prokaryote into an organelle that has an obligately dependent and highly efficient interplay with the nuclear genome.     

Phylogenetic distribution and evolution of mycorrhizas in land plants

A survey of 659 papers mostly published since 1987 was conducted to compile a checklist of mycorrhizal occurrence among 3,617 species (263 families) of land plants. A plant phylogeny was then used to map the mycorrhizal information to examine evolutionary patterns. Several findings from this survey enhance our understanding of the roles of mycorrhizas in the origin and subsequent diversification of land plants. First, 80 and 92% of surveyed land plant species and families are mycorrhizal. Second, arbuscular mycorrhiza (AM) is the predominant and ancestral type of mycorrhiza in land plants. Its occurrence in a vast majority of land plants and early-diverging lineages of liverworts suggests that the origin of AM probably coincided with the origin of land plants. Third, ectomycorrhiza (ECM) and its derived types independently evolved from AM many times through parallel evolution. Coevolution between plant and fungal partners in ECM and its derived types has probably contributed to diversification of both plant hosts and fungal symbionts. Fourth, mycoheterotrophy and loss of the mycorrhizal condition also evolved many times independently in land plants through parallel evolution.     

Acquisition of desiccation tolerance in soybeans

The entry into a desiccation-tolerant state is a major developmental component of seed maturation. Development of desiccation tolerance of embryonic axes of soybean [Glycine max (L.) Merrill cv. Chippewa 64] was studied by measuring changes in electrolyte leakage. germination and relative growth rate after axes were rapidly air-dried to various water contents. Axes acquired the full capacity for germination at 34 days after flowering (DAF). and reached physiological maturity (maximum dry weight) at 48 DAF. When dried to water content h = 0. 08 (g water g⁻¹ dry weight). few axes germinated before 42 DAF. but more than 90% germinated after 48 DAF. However, electrolyte leakage of rehydrated axes showed a linear decline from 30 to 55 DAF. For developing axes there was a critical water content or desiccation threshold. which could be estimated by using the electrolyte leakage method. The threshold of desiccation tolerance decreased gradually from h = 1. 10 to 0. 18 as axes matured from 28 to 55 DAF. The development of desiccation tolerance continued after physiological maturity at 48 DAF. We conclude that the acquisition of desiccation tolerance of soybean axes is a gradual event, rather than an abrupt transition.     

Chlorophyll fluorometry sheds light on the role of desiccation resistance for vegetative overland dispersal of aquatic plants

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Postgenomic analysis of desiccation tolerance

Desiccation tolerance is the capacity to survive complete drying. It is an ancient trait that can be found in prokaryotes, fungi, primitive animals (often at the larval stages), whole plants, pollens and seeds. In the dry state, metabolism is suspended and the duration that anhydrobiotes can survive ranges from years to centuries. Whereas genes induced by drought stress have been successfully enumerated in tissues that are sensitive to cellular desiccation, we have little knowledge as to the adaptive role of these genes in establishing desiccation tolerance at the cellular level. This paper reviews postgenomic approaches in a variety of desiccation tolerant organisms in which the genetic responses have been investigated when they acquire the capacity of tolerating extremes of dehydration or when they are dry. Accumulation of non-reducing sugars, LEA proteins and a coordinated repression of metabolism appear to be the essential and universal attributes that can confer desiccation tolerance. The protective mechanisms of these attributes are described. Furthermore, it is most likely that other mechanisms have evolved since the function of about 30% of the genes involved in desiccation tolerance remains to be elucidated. The question of the overlap between desiccation tolerance and drought tolerance is briefly addressed.     

Engineering desiccation tolerance in Escherichia coli

Recombinant sucrose-6-phosphate synthase (SpsA) was synthesized in Escherichia coli BL21DE3 by using the spsA gene of the cyanobacterium Synechocystis sp. strain PCC 6803. Transformants exhibited a 10,000-fold increase in survival compared to wild-type cells following either freeze-drying, air drying, or desiccation over phosphorus pentoxide. The phase transition temperatures and vibration frequencies (P==O stretch) in phospholipids suggested that sucrose maintained membrane fluidity during cell dehydration.     

Sugars and desiccation tolerance in seeds

Soluble sugars have been shown to protect liposomes and lobster microsomes from desiccation damage, and a protective role has been proposed for them in several anhydrous systems. We have studied the relationship between soluble sugar content and the loss of desiccation tolerance in the axes of germinating soybean (Glycine max L. Merr. cv Williams), pea (Pisum sativum L. cv Alaska), and corn (Zea mays L. cv Merit) axes. The loss of desiccation tolerance during imbibition was monitored by following the ability of seeds to germinate after desiccation following various periods of preimbibition and by following the rates of electrolyte leakage from dried, then rehydrated axes. Finally, we analyzed the soluble sugar contents of the axes throughout the transition from desiccation tolerance to intolerance. These analyses show that sucrose and larger oligosaccharides were consistently present during the tolerant stage, and that desiccation tolerance disappeared as the oligosaccharides were lost. The results support the idea that sucrose may serve as the principal agent of desiccation tolerance in these seeds, with the larger oligosaccharides serving to keep the sucrose from crystallizing.     

Inactivation of two homologues of proteins presumed to be involved in the desiccation tolerance of plants sensitizes Deinococcus radiodurans R1 to desiccation

Mutational inactivation of the genes designated DR1172 and DRB0118 in Deinococcus radiodurans R1 greatly sensitizes this species to desiccation, but not to ionizing radiation. These genes encode proteins that share features with the desiccation-induced LEA76 proteins of many plants and the PCC13-62 protein of Craterostigma plantagineum, suggesting that D. radiodurans may serve as a useful model for the study of desiccation tolerance in higher organisms.     

How plants conquered land: evolution of terrestrial adaptation

The transition of plants from water to land is considered one of the most significant events in the evolution of life on Earth. The colonization of land by plants, accompanied by their morphological, physiological and developmental changes, resulted in plant biodiversity. Besides significantly influencing oxygen levels in the air and on land, plants manufacture organic matter from CO₂ and water with the help of sunlight, paving the way for the diversification of nonplant lineages ranging from microscopic organisms to animals. Land plants regulate the climate by adjusting total biomass and energy flow. At the genetic level, these innovations are achieved through the rearrangement of pre-existing genetic information. Advances in genome sequencing technology are revamping our understanding of plant evolution. This study highlights the morphological and genomic innovations that allow plants to integrate life on Earth.