Protection of the photosynthetic apparatus during desiccation in resurrection plants (original) (raw)
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Protection of photosynthesis in desiccation-tolerant resurrection plants
Journal of Plant Physiology, 2018
Inhibition of photosynthesis is a central, primary response that is observed in both desiccation-tolerant and desiccation-sensitive plants affected by drought stress. Decreased photosynthesis during drought stress can either be due to the limitation of carbon dioxide entry through the stomata and the mesophyll cells, due to increased oxidative stress or due to decreased activity of photosynthetic enzymes. Although the photosynthetic rates decrease in both desiccation-tolerant and sensitive plants during drought, the remarkable difference lies in the complete recovery of photosynthesis after rehydration in desiccation-tolerant plants. Desiccation of sensitive plants leads to irreparable damages of the photosynthetic membranes, in contrast the photosynthetic apparatus is deactivated during desiccation in desiccation-tolerant plants. Desiccation-tolerant plants employ different strategies to protect and/or maintain the structural integrity of the photosynthetic apparatus to reactivate photosynthesis upon water availability. Two major mechanisms are distinguished. Homoiochlorophyllous desiccation-tolerant plants preserve chlorophyll and thylakoid membranes and require active protection mechanisms, while poikilochlorophyllous plants degrade chlorophyll in a regulated manner but then require de novo synthesis during rehydration. Desiccation-tolerant plants, particularly homoiochlorophyllous plants, employ conserved and novel antioxidant enzymes/metabolites to minimize the oxidative damage and to protect the photosynthetic machinery. De novo synthesized, stress-induced proteins in combination with antioxidants are localized in chloroplasts and are important components of the protective network. Genome sequence informations provide some clues on selection of genes involved in protecting photosynthetic structures; e.g. ELIP genes (early light inducible 2 proteins) are enriched in the genomes and more abundantly expressed in homoiochlorophyllous desiccation-tolerant plants. This review focuses on the mechanisms that operate in the desiccation-tolerant plants to protect the photosynthetic apparatus during desiccation.
Surviving metabolic arrest: photosynthesis during desiccation and rehydration in resurrection plants
Annals of the New York Academy of Sciences, 2015
Photosynthesis is the key process that is affected by dehydration in plants. Desiccation‐tolerant resurrection plants can survive conditions of very low relative water content. During desiccation, photosynthesis is not operational, but is recovered within a short period after rehydration. While homoiochlorophyllous resurrection plants retain their photosynthetic apparatus during desiccation, poikilochlorophyllous resurrection species dismantle chloroplasts and degrade chlorophyll but resynthesize them again during rehydration. Dismantling the chloroplasts avoids the photooxidative stress in poikilochlorophyllous resurrection plants, whereas it is minimized in homoiochlorophyllous plants through the synthesis of antioxidant enzymes and protective proteins or metabolites. Although the cellular protection mechanisms in both of these species vary, these mechanisms protect cells from desiccation‐induced damage and restore photosynthesis upon rehydration. Several of the proteins synthesiz...
An investigation into the role of light during desiccation of three angiosperm resurrection plants
Plant, Cell and Environment, 2003
Under water-limiting conditions excitation energy harnessed by chlorophyll can lead to the formation of reactive oxygen species (ROS). Resurrection plants minimize their formation by preventing the opportunity for light-chlorophyll interaction but also quench them via antioxidants. Poikilochlorohyllous species such as X erophyta humilis break down chlorophyll to avoid ROS formation. Homoiochlorophyllous types retain chlorophyll. We proposed that leaf folding during drying of Craterostigma wilmsii and Myrothamnus flabellifolius shades chlorophyll to avoid ROS (Farrant, Plant Ecology 151, 29-39, 2000). This was tested by preventing leaf folding during drying in light. As controls, plants were dried without light, and X. humilis was included. Craterostigma wilmsii did not survive drying in light if the leaves were prevented from folding, despite protection from increased anthocyanin and sucrose and elevated antioxidant enzyme activity. Membranes were damaged, electrolyte leakage was elevated and plastoglobuli (evidence of light stress) accumulated in chloroplasts. Restrained leaves of M. flabellifolius survived drying in light. Leaf folding allows less shading, but the extent of chemical protection (anthocyanin content and antioxidant activity) is considerably higher in this species compared with C. wilmsii . Chemical protection appears to be light regulated in M. flabellifolius but not in C. wilmsii . Drying in the dark resulted in loss of viability in the homoiochlorophyllous but not the poikilochlorophyllous species. It is hypothesized that some of the genes required for protection are light regulated in the former.
Plant Ecology, 2000
The mechanisms of protection against mechanical and oxidative stress were identified and compared in the angiosperm resurrection plants Craterostigma wilmsii, Myrothamnus flabellifolius and Xerophyta humilis. Dryinginduced ultrastructural changes within mesophyll cells were followed to gain an understanding of the mechanisms of mechanical stabilisation. In all three species, water filled vacuoles present in hydrated cells were replaced by several smaller vacuoles filled with non-aqueous substances. In X. humilis, these occupied a large proportion of the cytoplasm, preventing plasmalemma withdrawal and cell wall collapse. In C. wilmsii, vacuoles were small but extensive cell wall folding occurred to prevent plasmalemma withdrawal. In M. flabellifolius, some degree of vacuolation and wall folding occurred, but neither were sufficient to prevent plasmalemma withdrawal. This membrane was not ruptured, possibly due to membrane repair at plasmodesmata junctions where tearing might have occurred. In addition, the extra-cytoplasmic compartment appeared to contain material (possibly similar to that in vacuoles) which could facilitate stabilisation of dry cells. Photosynthesis and respiration are particularly susceptible to oxidative stress during drying. Photosynthesis ceased at high water contents and it is proposed that a controlled shut down of this metabolism occurred in order to minimise the potential for photo-oxidation. The mechanisms whereby this was achieved varied among the species. In X. humilis, chlorophyll was degraded and thylakoid membranes dismantled during drying. In both C. wilmsii and M. flabellifolius, chlorophyll was retained, but photosynthesis was stopped due to chlorophyll shading from leaf folding and anthocyanin accumulation. Furthermore, in M. flabellifolius thylakoid membranes became unstacked during drying. All species continued respiration during drying to 10% relative water content, which is proposed to be necessary for energy to establish protection mechanisms. Activity of antioxidant enzymes increased during drying and remained high at low water contents in all species, ameliorating free radical damage from both photosynthesis and respiration. The nature and extent of antioxidant upregulation varied among the species. In C. wilmsii, only ascorbate peroxidise activity increased, but in M. flabellifolius and X. humilis ascorbate peroxidise, glutathione reductase and superoxide dismutase activity increased, to various extents, during drying. Anthocyanins accumulated in all species but this was more extensive in the homoiochlorophyllous types, possibly for protection against photo-oxidation.
Editorial: Current advances and challenges in understanding plant desiccation tolerance.
One of the most exciting and gratifying privileges of having edited this research topic on plant desiccation tolerance is that we received papers and reviews on resurrection plant species (particularly angiosperms) covering five continents, almost six, although unfortunately we did not quite get there. We were certainly incredibly fortunate for the kind responses of colleagues in Africa (for providing us with papers dealing with their own (favorite) particular resurrection plant species and the recent discoveries that they have made. It is with this in mind that we are moving toward a more global understanding of resurrection plants, and angiosperm species in particular, although often referred to as being particularly rich in diversity in southern Africa . We have noted that more and more studies are being made of resurrection species around the globe, as species are being uncovered in China such as Boea hygrometrica (this research topic, and Paraboea rufescens both in the Gesneriaceae and in South America Also in Brazil specifically, with Barbacenia purpurea (this research topic, in the Velloziaeace. It is with this in mind that we are realizing more and more that plant desiccation tolerance in angiosperms is far less uncommon than previously suspected, and certainly has re-evolved as an adaptive feature on all continents (except for the South Pole, but this may well be provisional). We start off our quest for understanding plant desiccation tolerance with the green algae; here we are grateful for the first comprehensive review on this under-studied area, with a contribution from Holzinger and Karstens (2013). It is clear that algal cells were obviously the first "plants" to experience desiccation during land plant evolution. Far from following a simple single strategy, Holzinger and Karstens show that a variety of strategies appear to be employed to mitigate desiccation in both the Streptophyta and Chlorophyta lineages. We were hoping to include lichens and bryophytes (mosses), but these have been adequately covered in Moore et al. (2009). Our shift into the angiosperms, starts with an unlikely species, Arabidopsis thaliana (Djafi et al., 2013), however much is inferred, developed, tested using the Arabidopsis genetic model. In this case, an important area of angiosperm desiccation tolerance involves signaling (Moore et al., 2009), and Djafi et al. (2013) in their study focus on the phospoholipase C genes/proteins that are known to be triggered in response to dehydration. Djafi et al. (2013) have performed a thorough transcriptome study in A. thaliana using the presence of inhibitors that identified a set of DREB2 (Dehyration Response Element Binding) regulatory genes involved in dehydration stress responses. Moving into resurrection plants we were fortunate to have received such a comprehensive review by Dinakar and Bartels (2013) of the various-omics Moore and Farrant
Plant physiology, 2015
During desiccation, homoiochlorophyllous resurrection plants retain most of their photosynthetic apparatus, allowing them to resume photosynthetic activity quickly upon water availability. These plants rely on various mechanisms to prevent formation of reactive oxygen species and/or protect their tissues from the damage they inflict. In this work, we addressed the issue of how homoiochlorophyllous resurrection plants deal with the problem of excessive excitation/electron pressures during dehydration using Craterostigma pumilum as a model plant. To investigate the alterations in the supramolecular organization of photosynthetic protein complexes, we examined cryo-immobilized, freeze-fractured leaf tissues using (cryo)-scanning electron microscopy. These examinations revealed rearrangements of photosystem II (PSII) complexes, including a lowered density during moderate dehydration, consistent with a lower level of PSII proteins, as shown by biochemical analyses. The latter also showed...
An Overview of Mechanisms of Desiccation Tolerance in Selected Angiosperm Resurrection Plants
The vegetative tissues of resurrection plants, like seeds, can tolerate desiccation to 5% relative water content (RWC) for extended periods and yet resume full metabolic activity on re-watering. In this review we will illustrate how this is achieved in a variety of angiosperm resurrection plants, our studies ranging from the ecophysiological to the biochemical level. At the whole plant level, leaf folding and other anatomical changes serve to minimise light and mechanical stress associated with drying and rehydration. The mechanisms of cell wall folding are described for Craterostigma wilmsii and Myrothanmus flabellifolia. Free radicals, radical oxygen species (ROS) usually generated under water-deficit stress by photosynthesis, are minimised by either homoiochlorophylly (e.g. C. wilmsii and M. flabellifolia) or poikilochlorophylly (e.g. Xerophyta sp.). The antioxidant systems of these plants effectively deal with ROS generated by other metabolic processes. In addition to antioxidants common to most plants, resurrection plants also accumulate polyphenols such as 3, 4, 5 triO -galloylquinic acid in M. flabellifolia, and seed-associated antioxidants (e.g. 1-cys-peroxiredoxin and metallothionines) as effective ROS scavengers. Sucrose accumulates at low RWC, presumably protecting the sub-cellular milieu against desiccation-induced macromolecular denaturation.
Photosynthesis in desiccation tolerant plants: Energy metabolism and antioxidative stress defense
Plant Science
Resurrection plants are regarded as excellent models to study the mechanisms associated with desiccation tolerance. During the past years tremendous progress has been made in understanding the phenomenon of desiccation tolerance in resurrection plants, but many questions are open concerning the mechanisms enabling these plants to survive desiccation. The photosynthetic apparatus is very sensitive to reactive oxygen species mediated injury during desiccation and must be maintained or quickly repaired upon rehydration. The photosynthetic apparatus is a primary source of generating reactive oxygen species. The unique ability of plants to withstand the oxidative stress imposed by reactive oxygen species during desiccation depends on the production of antioxidants. The present review considers the overall strategies and the mechanisms involved in the desiccation tolerance in the first part and will focus on the effects on photosynthesis, energy metabolism and antioxidative stress defenses in the second part.► Resurrection plants use various strategies to protect cellular integrity during desiccation. ► Photosynthesis is shutdown during desiccation and completely recovered following rehydration. ► Protection against oxidative stress during desiccation is afforded by antioxidant system.
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 planta...