Drying without senescence in resurrection plants.

Research into extreme drought tolerance in resurrection plants using species such as Craterostigma plantagineum, C. wilmsii, Xerophyta humilis, Tortula ruralis, and Sporobolus stapfianus has provided some insight into the desiccation tolerance mechanisms utilized by these plants to allow them to persist under extremely adverse environmental conditions. Some of the mechanisms used to ensure cellular preservation during severe dehydration appear to be peculiar to resurrection plants. Apart from the ability to preserve vital cellular components during drying and rehydration, such mechanisms include the ability to down-regulate growth-related metabolism rapidly in response to changes in water availability, and the ability to inhibit dehydration-induced senescence programs enabling reconstitution of photosynthetic capacity quickly following a rainfall event. Extensive research on the molecular mechanism of leaf senescence in non-resurrection plants has revealed a multi-layered regulatory network operates to control programed cell death pathways. However, very little is known about the molecular mechanisms that resurrection plants employ to avoid undergoing drought-related senescence during the desiccation process. To survive desiccation, dehydration in the perennial resurrection grass S. stapfianus must proceed slowly over a period of 7 days or more. Leaves detached from the plant before 60% relative water content (RWC) is attained are desiccation-sensitive indicating that desiccation tolerance is conferred in vegetative tissue of S. stapfianus when the leaf RWC has declined to 60%. Whilst some older leaves remaining attached to the plant during dehydration will senesce, suggesting dehydration-induced senescence may be influenced by leaf age or the rate of dehydration in individual leaves, the majority of leaves do not senesce. Rather these leaves dehydrate to air-dryness and revive fully following rehydration. Hence it seems likely that there are genes expressed in younger leaf tissues of resurrection plants that enable suppression of drought-related senescence pathways. As very few studies have directly addressed this phenomenon, this review aims to discuss current literature surrounding the activation and suppression of senescence pathways and how these pathways may differ in resurrection plants.

Increased biomass, seed yield and stress tolerance is conferred in Arabidopsis by a novel enzyme from the resurrection grass Sporobolus stapfianus that glycosylates the strigolactone analogue GR24.

Isolation of gene transcripts from desiccated leaf tissues of the resurrection grass, Sporobolus stapfianus, resulted in the identification of a gene, SDG8i, encoding a Group 1 glycosyltransferase (UGT). Here, we examine the effects of introducing this gene, under control of the CaMV35S promoter, into the model plant Arabidopsis thaliana. Results show that Arabidopsis plants constitutively over-expressing SDG8i exhibit enhanced growth, reduced senescence, cold tolerance and a substantial improvement in protoplasmic drought tolerance. We hypothesise that expression of SDG8i in Arabidopsis negatively affects the bioactivity of metabolite/s that mediate/s environmentally-induced repression of cell division and expansion, both during normal development and in response to stress. The phenotype of transgenic plants over-expressing SDG8i suggests modulation in activities of both growth- and stress-related hormones. Plants overexpressing the UGT show evidence of elevated auxin levels, with the enzyme acting downstream of ABA to reduce drought-induced senescence. Analysis of the in vitro activity of the UGT recombinant protein product demonstrates that SDG8i can glycosylate the synthetic strigolactone analogue GR24, evoking a link with strigolactone-related processes in vivo. The large improvements observed in survival of transgenic Arabidopsis plants under cold-, salt- and drought-stress, as well as the substantial increases in growth rate and seed yield under non-stress conditions, indicates that overexpression of SDG8i in crop plants may provide a novel means of increasing plant productivity.

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.

Sporobolus stapfianus, a model desiccation-tolerant grass.

Sporobolus stapfianus Gandoger, one of ~40 known 'anabiotic'grass species (i.e. 'able to regain vital activity from a state of latent life'), is the most versatile tool for research into desiccation tolerance in vegetative grass tissue. Current knowledge on this species is presented, including the features that suit it for investigations into the plant's ability to survive dehydration of its leaf protoplasm. The main contributors to desiccation tolerance in S. stapfianus leaves appear to be: accumulation during dehydration of protectants of membranes and proteins; mechanisms limiting oxidative damage; a retention of protein synthetic activity in late stages of drying that is linked with changes in gene expression and in the proteomic array; and an ability to retain net synthesis of ATP during drying. S. stapfianus exemplifies an advanced stage of an evolutionary trend in desiccation tolerant plants towards increased importance of the dehydration phase (for induction of tolerance, for synthesis of protectants and for proteomic changes).

Desiccation-tolerance specific gene expression in leaf tissue of the resurrection plant Sporobolus stapfianus.

The desiccation tolerant grass Sporobolus stapfianus Gandoger can modulate cellular processes to prevent the imposition of irreversible damage to cellular components by water deficit. The cellular processes conferring this ability are rapidly attenuated by increased water availability. This resurrection plant can quickly restore normal metabolism. Even after loss of more than 95% of its total water content, full rehydration and growth resumption can occur within 24 h. To study the molecular mechanisms of desiccation tolerance in S. stapfianus, a cDNA library constructed from dehydration-stressed leaf tissue, was differentially screened in a manner designed to identify genes with an adaptive role in desiccation tolerance. Further characterisation of four of the genes isolated revealed they are strongly up-regulated by severe dehydration stress and only in desiccation-tolerant tissue, with three of these genes not being expressed at detectable levels in hydrated or dehydrating desiccation-sensitive tissue. The nature of the putative proteins encoded by these genes are suggestive of molecular processes associated with protecting the plant against damage caused by desiccation and include a novel LEA-like protein, and a pore-like protein that may play an important role in peroxisome function during drought stress. A third gene product has similarity to a nuclear-localised protein implicated in chromatin remodelling. In addition, a UDPglucose glucosyltransferase gene has been identified that may play a role in controlling the bioactivity of plant hormones or secondary metabolites during drought stress.