Main conclusionProvides a first comprehensive review of integrated physiological and molecular aspects of desiccation toleranceXerophyta viscosa. A synopsis of biotechnological studies being undertaken to improve drought tolerance in maize is given.Xerophyta viscosa (Baker) is a monocotyledonous resurrection plant from the family Vellociacea that occurs in summer-rainfall areas of South Africa, Lesotho and Swaziland. It inhabits rocky terrain in exposed grasslands and frequently experiences periods of water deficit. Being a resurrection plant it tolerates the loss of 95 % of total cellular water, regaining full metabolic competency within 3 days of rehydration. In this paper, we review some of the molecular and physiological adaptations that occur during various stages of dehydration of X. viscosa, these being functionally grouped into early and late responses, which might be relevant to the attainment of desiccation tolerance. During early drying (to 55 % RWC) photosynthesis is shut down, there is increased presence and activity of housekeeping antioxidants and a redirection of metabolism to the increased formation of sucrose and raffinose family oligosaccharides. Other metabolic shifts suggest water replacement in vacuoles proposed to facilitate mechanical stabilization. Some regulatory processes observed include increased presence of a linker histone H1 variant, a Type 2C protein phosphatase, a calmodulin- and an ERD15-like protein. During the late stages of drying (to 10 % RWC) there was increased expression of several proteins involved in signal transduction, and retroelements speculated to be instrumental in gene silencing. There was induction of antioxidants not typically found in desiccation-sensitive systems, classical stress-associated proteins (HSP and LEAs), proteins involved in structural stabilization and those associated with changes in various metabolite pools during drying. Metabolites accumulated in this stage are proposed, inter alia, to facilitate subcellular stabilization by vitrification process which can include glass- and ionic liquid formation.
Vegetative desiccation tolerance, the ability to survive loss of over 90% of cellular water, is an extremely rare trait in Angiosperms. Xerophyta schlechteri survives such extreme water deficit by entering prolonged quiescence and suppressing drought-induced senescence in most of the leaf area, except the apical tip. Information on the molecular regulation of senescence in such plants is scarce and this is the first study to investigate such regulation in senescing and non-senescing tissues of the same leaf. Genome-wide RNA sequencing enabled comparison of senescent and non-senescent tissues during desiccation and early rehydration, establishment of the water content range in which senescence is initiated and identification of molecular mechanisms employed to bring about cellular death. Senescence-associated genes (XsSAG) specific to this species were identified and two potential regulatory sites were enriched in regions upstream to these XsSAGs, allowing us to create a model of senescence regulation in X. schlechteri based on homology with known Arabidopsis senescence regulators. We hypothesise that desiccation-driven senescence occurs as a result of a convergence of signals around MAPK6 to trigger WRKY-mediated ethylene synthesis and XsSAG expression, not unlike aging and stress-related senescence in Arabidopsis, but at remarkably lower water contents (<35% RWC).
Vegetative desiccation tolerance (VDT), the ability of such tissues to survive the near complete loss of cellular water, is a rare but polyphyletic phenotype. It is a complex multifactorial trait, typified by some near universal (core) factors but with many and varied adaptations due to plant architecture, biochemistry and biotic/abiotic dynamics of particular ecological niches. The ability to enter into a quiescent biophysically stable state is what ultimately determines desiccation tolerance. Thus, understanding of the metabolomic complement of plants with VDT gives insight into the nature of survival as well as evolutionary aspects of VDT. In this study we measured the soluble carbohydrate profiles and the polar, TMS-derivatisable metabolomes of 7 phylogenetically diverse species with VDT, in contrast with 3 desiccation sensitive (DS) species, under conditions of full hydration, severe water deficit stress, and desiccated. Our study confirmed the existence of core mechanisms of VDT systems relying on either constitutively abundant trehalose, or the accumulation of raffinose family oligosaccharides and sucrose, with threshold ratios conditioned by other features of the metabolome. DS systems did not meet these ratios. Considerable chemical variations among VDT species suggest that similar stresses, e.g. photosynthetic stress, are dealt with using different chemical regimes. Furthermore, differences in timing of metabolic shifts suggest there is not a single desiccation programme, but that subprocesses are coordinated differently at different phases of drying. There is likely to be constraints on the composition of a viable dry state and how different adaptive strategies interact with the biophysical constraints of VDT.
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