Evolution Of Desiccation Tolerance Research Articles

Drying without dying: A genome database for desiccation-tolerant plants and evolution of desiccation tolerance.

Desiccation is typically fatal, but a small number of land plants have evolved vegetative desiccation tolerance (VDT), allowing them to dry without dying through a process called anhydrobiosis. Advances in sequencing technologies have enabled the investigation of genomes for desiccation-tolerant plants over the past decade. However, a dedicated and integrated database for these valuable genomic resources has been lacking. Our prolonged interest in VDT plant genomes motivated us to create the "Drying without Dying" database, which contains a total of 16 VDT-related plant genomes (including 10 mosses) and incorporates 10 genomes that are closely related to VDT plants. The database features bioinformatic tools, such as blast and homologous cluster search, sequence retrieval, Gene Ontology term and metabolic pathway enrichment statistics, expression profiling, co-expression network extraction, and JBrowser exploration for each genome. To demonstrate its utility, we conducted tailored PFAM family statistical analyses, and we discovered that the drought-responsive ABA transporter AWPM-19 family is significantly tandemly duplicated in all bryophytes but rarely so in tracheophytes. Transcriptomic investigations also revealed that response patterns following desiccation diverged between bryophytes and angiosperms. Combined, the analyses provided genomic and transcriptomic evidence supporting a possible divergence and lineage-specific evolution of VDT in plants. The database can be accessed at http://desiccation.novogene.com. We expect this initial release of the "Drying without Dying" plant genome database will facilitate future discovery of VDT genetic resources.

Tracing the serendipitous genesis of radiation resistance.

Free-living organisms frequently encounter unfavorable abiotic environmental factors. Those who adapt and cope with sudden changes in the external environment survive. Desiccation is one of the most common and frequently encountered stresses in nature. On the contrary, ionizing radiations are limited to high local concentrations of naturally occurring radioactive materials and related anthropogenic activities. Yet, resistance to high doses of ionizing radiation is evident across the tree of life. The evolution of desiccation resistance has been linked to the evolution of ionizing radiation resistance, although, evidence to support the idea that the evolution of desiccation tolerance is a necessary precursor to ionizing radiation resistance is lacking. Moreover, the presence of radioresistance in hyperthermophiles suggests multiple paths lead to radiation resistance. In this minireview, we focus on the molecular aspects of damage dynamics and damage response pathways comprising protective and restorative functions with a definitive survival advantage, to explore the serendipitous genesis of ionizing radiation resistance.

Desiccation Tolerance Evolved through Gene Duplication and Network Rewiring in Lindernia.

Although several resurrection plant genomes have been sequenced, the lack of suitable dehydration-sensitive outgroups has limited genomic insights into the origin of desiccation tolerance. Here, we utilized a comparative system of closely related desiccation-tolerant (Lindernia brevidens) and -sensitive (Lindernia subracemosa) species to identify gene- and pathway-level changes associated with the evolution of desiccation tolerance. The two high-quality Lindernia genomes we assembled are largely collinear, and over 90% of genes are conserved. L. brevidens and L. subracemosa have evidence of an ancient, shared whole-genome duplication event, and retained genes have neofunctionalized, with desiccation-specific expression in L. brevidens Tandem gene duplicates also are enriched in desiccation-associated functions, including a dramatic expansion of early light-induced proteins from 4 to 26 copies in L. brevidens A comparative differential gene coexpression analysis between L. brevidens and L. subracemosa supports extensive network rewiring across early dehydration, desiccation, and rehydration time courses. Many LATE EMBRYOGENESIS ABUNDANT genes show significantly higher expression in L. brevidens compared with their orthologs in L. subracemosa Coexpression modules uniquely upregulated during desiccation in L. brevidens are enriched with seed-specific and abscisic acid-associated cis-regulatory elements. These modules contain a wide array of seed-associated genes that have no expression in the desiccation-sensitive L. subracemosa Together, these findings suggest that desiccation tolerance evolved through a combination of gene duplications and network-level rewiring of existing seed desiccation pathways.

Dehydration-responsive features of Atrichum undulatum.

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.

The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon.

In a minute proportion of angiosperm species, rehydrating foliage can revive from airdryness or even from equilibration with air of ~0% RH. Such desiccation tolerance is known from vegetative cells of some species of algae and of major groups close to the evolutionary path of the angiosperms. It is also found in the reproductive structures of some algae, moss spores and probably the aerial spores of other terrestrial cryptogamic taxa. The occurrence of desiccation tolerance in the seed plants is overwhelmingly in the aerial reproductive structures; the pollen and seed embryos. Spatially and temporally, pollen and embryos are close ontogenetic derivatives of the angiosperm microspores and megaspores respectively. This suggests that the desiccation tolerance of pollen and embryos derives from the desiccation tolerance of the spores of antecedent taxa and that the basic pollen/embryo mechanism of desiccation tolerance has eventually become expressed also in the vegetative tissue of certain angiosperm species whose drought avoidance is inadequate in micro-habitats that suffer extremely xeric episodes. The protective compounds and processes that contribute to desiccation tolerance in angiosperms are found in the modern groups related to the evolutionary path leading to the angiosperms and are also present in the algae and in the cyanobacteria. The mechanism of desiccation tolerance in the angiosperms thus appears to have its origins in algal ancestors and possibly in the endosymbiotic cyanobacteria-related progenitor of chloroplasts and the bacteria-related progenitor of mitochondria. The mechanism may involve the regulation and timing of the accumulation of protective compounds and of other contributing substances and processes.

CDT retroelement

The resurrection plant Craterostigma plantagineum can tolerate up to 96% loss of its water content and recover from such extreme dehydration within several hours. This property is not shared by callus which has a strict requirement for exogenous abscissic acid (ABA) to survive severe water loss. ABA treatment and dehydration result in the induction of similar drought-responsive genes. Activation tagging led to the isolation of CDT-1 gene which renders callus desiccation tolerant bypassing the ABA requirement. This gene belongs to a retroelement family, members of which are induced by ABA and dehydration in callus, supporting its role in desiccation tolerance. Indeed, CDT genes have been detected in other desiccation tolerant Craterostigma species. CDT-1 RNA of both strands was identified by in situ hybridization and a CDT-1-derived short interfering RNA was detected in desiccation tolerant tissues and was able to induce dehydration genes in transfected protoplasts to the same extent as an ABA treatment. Thus, under environmental stress the induced transposition, over generations, directs the amplification of CDT-copy number in the genome and increases the desiccation tolerance phenomenon.Addendum to: Hilbricht T, Varotto S, Sgaramella V, Bartels D, Salamini F, Furini A. Retrotransposons and siRNA have a role in the evolution of desiccation tolerance leading to resurrection of the plant Craterostigma plantagineum. New Phytol 2008; 179:877-87.

Molecular characterization of two alanine-rich Lea genes abundantly expressed in the resurrection plant C. plantagineum in response to osmotic stress and ABA

Expression of many genes is induced during dehydration in vegetative tissues of the desiccation tolerant resurrection plantCraterostigma plantagineum. The most abundant group of desiccation-related gene products belong to the LEA (= Late Embryogenesis Abundant) proteins. Here we describe structures and expression patterns of members of group 3 and group 4Lea genes fromC. plantagineum. The most intriguing observation is the strong conservation of repeat motifs inLea genes found across divers plant species includingC. plantagineum and non-desiccation tolerant plants. This conservation of structural elements leads to speculations about evolution of desiccation tolerance in the resurrection plant.