The effect of drying rate on viability retention of recalcitrant propagules of Avicennia marina

Recalcitrant propagules of Avicennia marina were stored under different relative humidities to achieve both rapid and slow drying. Irrespective of conditions, short-term (4–8 days) storage was accompanied by increased rates of protein synthesis and respiratory activity, the initiation of vacuolation and cell division and also by enhanced rates of germination. These data indicate that the germination process is initiated upon shedding. Storage for longer periods resulted in reduced rates of germination and ultimately, in loss of viability. However, propagules dried rapidly retained viability to a lower moisture content than those dried slowly. It is suggested that as germination changes occur during storage, the propagules become increasingly sensitive to desiccation, which might coincide with the degree of vacuolation. Rapidly dried propagules have not proceeded as far along the germination pathway and, at a given moisture content, are not as desiccation sensitive as those dried slowly. Thus viability loss is dependent upon rates of drying rather than on absolute moisture content or storage time, considered independently. S. Air. J. Bot. 1985, 51: 432–438Weerspannige propagule van Avicennia marina is teen verskillende relatiewe vogtigheidswaardes geberg om vinnige sowel as stadige uitdroging teweeg te bring. Ongeag omstandighede, is korttermyn-berging (4–8 dae) gekenmerk deur ‘n verhoogde tempo van proteïensintese en respiratoriese aktiwiteit, aanvang van selholtevorming en seldeling, asook ‘n verhoogde ont-kiemingstempo. Hierdie gegewens dui daarop dat die proses van ontkieming ingelei word deur propaguulverlies. Berging vir langer tydperke het gelei tot verlaagde ontkiemingstempo, en uiteindelik tot verminderde kiemkrag. Propagule wat vinnig uitgedroog is, het egter hul kiemkrag tot op ‘n laer voggehalte behou as die wat stadig uitgedroog is. Daar word voorgestel dat die propagule toenemend sensitief word vir uitdroging, soos ontkiemingsveranderinge gedurende berging plaasvind, en dat dit moontlik saamval met die graad van selholtevorming. Vinnig-gedroogde propagule het nog nie so ver gevorder tot ontkieming nie, en by ‘n spesifieke voggehalte is hulle nie so droogte-sensitief soos die wat stadig uitgedroog het nie. Verlies aan kiemkragtigheid is gevolglik eerder afhanklik van uitdro-gingstempo as van absolute voggehalte of bergingstyd. S.-Afr. Tydskr. Plantk. 1985, 51: 432–43

Sucrose phosphate synthase activity and the co-ordination of carbon partitioning during sucrose and amino acid accumulation in desiccation-tolerant leaf material of the C4 resurrection plant Sporobolus stapfianus during dehydration.

Both sucrose and amino acids accumulate in desiccation-tolerant leaf material of the C(4) resurrection plant, Sporobolus stapfianus Gandoger (Poaceae). The present investigation was aimed at examining sucrose phosphate synthase (SPS) activity and various metabolic checkpoints involved in the co-ordination of carbon partitioning between these competing pathways during dehydration. In the initial phase of dehydration, photosynthesis and starch content declined to immeasurable levels, whilst significant increases in hexose sugars, sucrose, and amino acids were associated with concomitant significant increases in SPS and pyruvate kinase (PK) activities, and maximal activity levels of phosphoenolpyruvate carboxylase (PEPCase), NADP-dependent isocitrate dehydrogenase (NADP-ICDH), and NADH-dependent glutamate synthase (NADH-GOGAT). The next phase of dehydration was characterized by changes in metabolism coinciding with net hexose sugar phosphorylation. This phase was characterized by a further significant increase in sucrose accumulation, with increased rates of net sucrose accumulation and maximum rates of SPS activity measured under both saturating and limiting (inhibitory) conditions. SPS protein was also increased. The stronger competitive edge of SPS for carbon entering glycolysis during hexose phosphorylation was also demonstrated by the further decrease in respiration and the simultaneous, significant decline in both PEPCase and PK activities. A decreased anabolic demand for 2-oxoglutarate (2OG), which remained constant, was shown by the co-ordinated decrease in GOGAT. It is proposed that the further increase in amino acids in this phase of dehydration may be in part attributable to the breakdown of insoluble proteins

Protection mechanisms in the resurrection plant Xerophyta viscosa (Baker): both sucrose and raffinose family oligosaccharides (RFOs) accumulate in leaves in response to water deficit

Changes in water-soluble carbohydrates were examined in the leaves of the resurrection plant Xerophyta viscosa under conditions of water deficit. Sucrose and raffinose family oligosaccharides (RFOs), particularly raffinose, increased under these conditions, with the highest concentrations evident at 5% relative water content [RWC; 23.5 mg g−1 dry weight (DW) and 17.7 mg g−1 DW, respectively]. Importantly, these effects were reversible, with concentrations returning to levels comparable with that of the full turgor state 7 d after water deficit conditions were alleviated, providing evidence that both sucrose and RFOs may play a protective role in desiccated leaf tissue of X. viscosa. Further, because the sucrose-to-raffinose mass ratio of 1.3:1 observed in the dehydrated state was very low, compared with published data for other resurrection plants (always >5), it is suggested that, in X. viscosa leaves, RFOs serve the dual purpose of stress protection and carbon storage. XvGolS, a gene encoding a galactinol synthase enzyme responsible for the first catalytic step in RFO biosynthesis, was cloned and functionally expressed. In leaf tissue exposed to water deficit, XvGolS transcript levels were shown to increase at 19% RWC. GolS activity in planta could not be correlated with RFO accumulation, but a negative correlation was observed between RFO accumulation and myo-inositol depletion, during water deficit stress. This correlation was reversed after rehydration, suggesting that during water deficit myo-inositol is channelled into RFO synthesis, but during the rehydration process it is channelled to metabolic pathways related to the repair of desiccation-induced damag

Two Decades of Desiccation Biology: A Systematic Review of the Best Studied Angiosperm Resurrection Plants

Resurrection plants have an extraordinary ability to survive extreme water loss but still revive full metabolic activity when rehydrated. These plants are useful models to understand the complex biology of vegetative desiccation tolerance. Despite extensive studies of resurrection plants, many details underlying the mechanisms of desiccation tolerance remain unexplored. To summarize the progress in resurrection plant research and identify unexplored questions, we conducted a systematic review of 15 model angiosperm resurrection plants. This systematic review provides an overview of publication trends on resurrection plants, the geographical distribution of species and studies, and the methodology used. Using the Preferred Reporting Items for Systematic reviews and Meta–Analyses protocol we surveyed all publications on resurrection plants from 2000 and 2020. This yielded 185 empirical articles that matched our selection criteria. The most investigated plants were Craterostigma plantagineum (17.5%), Haberlea rhodopensis (13.7%), Xerophyta viscosa (reclassified as X. schlechteri) (11.9%), Myrothamnus flabellifolia (8.5%), and Boea hygrometrica (8.1%), with all other species accounting for less than 8% of publications. The majority of studies have been conducted in South Africa, Bulgaria, Germany, and China, but there are contributions from across the globe. Most studies were led by researchers working within the native range of the focal species, but some international and collaborative studies were also identified. The number of annual publications fluctuated, with a large but temporary increase in 2008. Many studies have employed physiological and transcriptomic methodologies to investigate the leaves of resurrection plants, but there was a paucity of studies on roots and only one metagenomic study was recovered. Based on these findings we suggest that future research focuses on resurrection plant roots and microbiome interactions to explore microbial communities associated with these plants, and their role in vegetative desiccation tolerance

A Label-Free Proteomic and Complementary Metabolomic Analysis of Leaves of the Resurrection Plant Xerophyta schlechteri during Dehydration

Vegetative desiccation tolerance, or the ability to survive the loss of ~95% relative water content (RWC), is rare in angiosperms, with these being commonly called resurrection plants. It is a complex multigenic and multi-factorial trait, with its understanding requiring a comprehensive systems biology approach. The aim of the current study was to conduct a label-free proteomic analysis of leaves of the resurrection plant Xerophyta schlechteri in response to desiccation. A targeted metabolomics approach was validated and correlated to the proteomics, contributing the missing link in studies on this species. Three physiological stages were identified: an early response to drying, during which the leaf tissues declined from full turgor to a RWC of ~80–70%, a mid-response in which the RWC declined to 40% and a late response where the tissues declined to 10% RWC. We identified 517 distinct proteins that were differentially expressed, of which 253 proteins were upregulated and 264 were downregulated in response to the three drying stages. Metabolomics analyses, which included monitoring the levels of a selection of phytohormones, amino acids, sugars, sugar alcohols, fatty acids and organic acids in response to dehydration, correlated with some of the proteomic differences, giving insight into the biological processes apparently involved in desiccation tolerance in this species

A molecular physiological review of vegetative desiccation tolerance in the resurrection plant Xerophyta viscosa (Baker)

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

Variability in Functional Traits along an Environmental Gradient in the South African Resurrection Plant Myrothamnus flabellifolia

Many desiccation-tolerant plants are widely distributed and exposed to substantial environmental variation across their native range. These environmental differences generate site-specific selective pressures that could drive natural variation in desiccation tolerance across populations. If identified, such natural variation can be used to target tolerance-enhancing characteristics and identify trait associations within a common genetic background. Here, we tested for natural variation in desiccation tolerance across wild populations of the South African resurrection plant Myrothamnus flabellifolia. We surveyed a suite of functional traits related to desiccation tolerance, leaf economics, and reproductive allocation in M. flabellifolia to test for trait associations and tradeoffs. Despite considerable environmental variation across the study area, M. flabellifolia plants were extremely desiccation tolerant at all sites, suggesting that tolerance is either maintained by selection or fixed in these populations. However, we detected notable associations between environmental variation, population characteristics, and fitness traits. Relative to mesic sites, plants in xeric sites were more abundant and larger, but were slower growing and less reproductive. The negative association between growth and reproduction with plant size and abundance pointed towards a potential growth–abundance tradeoff. The finding that M. flabellifolia is more common in xeric sites despite reductions in growth rate and reproduction suggests that these plants thrive in extreme aridity

Differences in biochemical, gas exchange and hydraulic response to water stress in desiccation tolerant and sensitive fronds of the fern Anemia caffrorum

Desiccation tolerant plants can survive extreme water loss in their vegetative tissues. The fern Anemia caffrorum produces desiccation tolerant (DT) fronds in the dry season and desiccation sensitive (DS) fronds in the wet season, providing a unique opportunity to explore the physiological mechanisms associated with desiccation tolerance. Anemia caffrorum plants with either DT or DS fronds were acclimated in growth chambers. Photosynthesis, frond structure and anatomy, water relations and minimum conductance to water vapour were measured under well-watered conditions. Photosynthesis, hydraulics, frond pigments, antioxidants and abscisic acid contents were monitored under water deficit. A comparison between DT and DS fronds under well-watered conditions showed that the former presented higher leaf mass per area, minimum conductance, tissue elasticity and lower CO2 assimilation. Water deficit resulted in a similar induction of abscisic acid in both frond types, but DT fronds maintained higher stomatal conductance and upregulated more prominently lipophilic antioxidants. The seasonal alternation in production of DT and DS fronds in A. caffrorum represents a mechanism by which carbon gain can be maximized during the rainy season, and a greater investment in protective mechanisms occurs during the hot dry season, enabling the exploitation of episodic water availability.This work was supported by the projects CTM2014-53902-C2-1-P from the Ministerio de Economia y Competitividad (MINECO, Spain) and the European Regional Development Fund (ERDF) and PGC2018-093824-B-C41/PGC2018-093824-B-C44 from the Ministerio de Ciencia, Innovacion y Universidades (MCIU, Spain) and the ERDF; and the Basque Government (grant UPV/EHU IT-1018-16, Spain). MN was supported by the MINECO and the European Social Fund (predoctoral fellowship BES-2015-072578). AVP-C was supported by the Ministerio de Educacion, Cultura y Deporte (MECD; pre-doctoral fellowship FPU-02054). MIA was supported by a pre-doctoral grant from the Basque Government. We thank the technical support for microscopy preparation provided by the Universitat de Valencia (Seccio de Microscopia Electrnica, SCSIE), Dr. Ferran Hierro (UIB, Serveis Cientificotecnics) and Margalida Roig Oliver (UIB). JMF provided funding for work conducted in South Africa from her South African Department of Science and Innovation, National Research Foundation Research Chair, grant no. 9840