Abstract

Plants being sessile organisms are well equipped genomically to respond to environmental stressors peculiar to their habitat. Evolution of plants onto land was enabled by the ability to tolerate extreme water loss (desiccation), a feature that has been retained within genomes but not universally expressed in most land plants today. In the majority of higher plants, desiccation tolerance (DT) is expressed only in reproductive tissues (seeds and pollen), but some 135 angiosperms display vegetative DT. Here, we review genome-level responses associated with DT, pointing out common and yet sometimes discrepant features, the latter relating to evolutionary adaptations to particular niches. Understanding DT can lead to the ultimate production of crops with greater tolerance of drought than is currently realized.

Introduction

All organisms possess a dynamic genome that is subject to continuous changes, among which gene transposition, -mutation, and -duplication, whole-genome duplication and polyploidization, as well as epigenetic modification all play a role. Such changes are profoundly influenced by the environment and constitute the basis of adaptation by selection which is expressed in the organism's phenotype. In addition, genomes respond on an immediate time scale to prevailing conditions by way of their transcriptomes, proteomes and metabolomes, as well as through epigenetic responses.

Plants are sessile organisms and therefore are particularly well equipped to respond to adverse environments in order to ensure survival. These responses are receiving increasing attention in the light of climate change and the necessity of crop production under shifting climatic conditions and in more marginal environments. Our current grain crops, in general, lack a robust resistance to drought, salt and sub-optimal temperatures primarily because of the trade-off between stress tolerance and yield that was inadvertently neglected during domestication, with loss of tolerance to various stresses as an important consequence. In addition, the accompanying loss of genetic variability prevents correction, i.e. the genetic resources required for (re)adaptation to increasingly stressful environments are lacking and need to be reintroduced from wild forbearers. Thus, exploiting the genetic structures of wild extremophytes, such as plant halophytes and anhydrobiotes, may contribute to the reintroduction of stress tolerance in some of the major crops.

In this review, we summarize and discuss the recent developments in genomic and post-genomic research on the extremophyte resurrection plants which can tolerate drying down to water levels below 0.1 g/g dry weight. This means that these plants are desiccation-tolerant, like most seeds, and may survive prolonged periods of severe drought in a completely dry state without losing viability. Several extremophytes have been subject to genomic studies and may eventually reveal a genetic ‘blueprint’ of desiccation tolerance (DT).

Plant desiccation tolerance

DT was a key trait in the evolution of life in terrestrial environments and has been reported to occur, albeit discretely, across life forms [1]. Indeed, it has been argued that many of the pathways associated with DT are ancestral and conserved [2], although there are clear accompanying differences, mostly niche-related, that have subsequently evolved among species. There are approximately 300 plant species that display vegetative DT, this being more common in bryophytes, lichens and gametophytes of pteridophytes, where DT is mostly constitutively expressed. It is rare in tracheophytes, being displayed in only 135 angiosperm species [3,4]. Here, DT is largely induced during dehydration. The evolution of vascular systems, waxy cuticles and stomatal regulation in aerial tissues of sporophytes enabled resistance to water loss and enhanced the survival of such plants during drought, resulting in an evolutionary thrust to lose DT in vegetative tissues and this becoming confined to spores, pollen grains and seeds. During the later evolution of angiosperms, DT was required in the vegetative tissues in at least nine separate lineages (Figure 1) [25]. There is strong evidence that in several of these lineages, the mechanisms associated with the acquisition of vegetative DT bear a strong resemblance to those enabling DT in seeds [1,69] and it is likely that vegetative DT in angiosperms is derived from a modified seed-based programme of gene expression [7,10].

A diagrammatic phylogeny of the major groups of angiosperms.

Figure 1.
A diagrammatic phylogeny of the major groups of angiosperms.

Bold lines represent clades with desiccation-tolerant members. Numbers in brackets represent the number of genera with a desiccation-tolerant phenotype followed by the total number of genera within the taxa. Images of hydrated (top panel) and desiccated (lower panel) Xerophyta schlechteri (previously called X. viscosa), Sporobolus stapfianus and Craterostigma pumilum — three representatives of the species discussed in this review. The former two species are poikilochlorophyllous, the last one is homoiochlorophyllous. Based on work published in refs. [2,3].

Figure 1.
A diagrammatic phylogeny of the major groups of angiosperms.

Bold lines represent clades with desiccation-tolerant members. Numbers in brackets represent the number of genera with a desiccation-tolerant phenotype followed by the total number of genera within the taxa. Images of hydrated (top panel) and desiccated (lower panel) Xerophyta schlechteri (previously called X. viscosa), Sporobolus stapfianus and Craterostigma pumilum — three representatives of the species discussed in this review. The former two species are poikilochlorophyllous, the last one is homoiochlorophyllous. Based on work published in refs. [2,3].

Interestingly, ∼10% of angiosperms produce desiccation-sensitive (DS) seeds (termed recalcitrant). It is postulated that DT has been lost, repressed and/or mutated in such seeds and that seed desiccation sensitivity is a derived trait that evolved independently in non-related clades [11]. This has been demonstrated by Marques et al. [12] who sequenced the genome of the DS-seeded species Castanospermum australe and furthermore reported that while several protein-coding genes were lost in genomes of all DS-seeded species sequenced, few (≤1%) were present in DS species only, supporting the hypothesis that independent evolutionary events gave rise to DS-seeded species. It is only in the genomic comparison of desiccation-tolerant and -sensitive systems that a true understanding of DT is achieved.

Photosynthesis is essential for plant growth and productivity, but this metabolism is highly sensitive to water deficit. Even mild dehydration can result in electron leakage and the formation of reactive oxygen species (ROS), which under more severe dehydration results in the induction of apoptosis and plant death in most species [1315]. Resurrection plants have evolved two major mechanisms, poikilochlorophylly and homoiochlorophylly, to prevent such damage and enable photosynthesis to resume very rapidly upon rehydration.

Poikilochlorophyllous species, mainly monocots, break down chlorophyll and dismantle thylakoid membranes during dehydration, a strategy similar to that of desiccation-tolerant seeds. These ‘xeroplasts’ are functionally reassembled on rehydration via co-ordinated transcription and de novo translation processes with striking similarity to those associated with etioplast–chloroplast transition during photomorphogenesis [1618]. This robust mechanism of avoiding photosynthetic ROS production enables greater longevity of such species in the desiccated state [19].

Homoiochlorophyllous species, mostly dicots, maintain the photosynthetic machinery and retain chlorophyll during dehydration, relying on pigment production and morphological changes, such as leaf folding, to minimize photosynthetic ROS production [20]. Furthermore, there is ordered shut down of linear electron transfer (thus bypassing PSII, where most of the damaging ROS reactions occur), with a parallel increase in cyclic electron transfer to maintain ATP production [21]. Induction of cyclic electron transfer is a relatively well-documented response to abiotic stresses such as high light, drought and extreme temperatures in DS plants [22], and this response is not unique. It is the nature of preservation of the photosystems at low water contents (≤40% relative water content [RWC]) that enables survival of desiccation. In the resurrection plant Craterostigma pumilum, supramolecular reorganization of photosystem II into paracrystalline arrays occurs, accompanied by significant accumulation of sucrose and the functional detachment of light-harvesting complexes [21,23]. Homoiochlorophyllous species furthermore up-regulate early light-induced proteins (ELIPs) (discussed below), thought inter alia to bind chlorophyll and prevent photo-oxidative damage [8].

Another common feature of DT, which is differently achieved in various resurrection plants, is the accumulation during dehydration of sucrose and raffinose family oligosaccharides (RFOs). Collectively, these are thought to contribute to osmotic adjustment during early dehydration and antioxidant potential, sugar signalling and prevention of membrane appression and stabilization (by contribution, in combination with late embryogenesis-abundant (LEA) proteins, to intracellular glass formation) of subcellular structures in their native form upon further desiccation [2429]. While oligosaccharide accumulation is a universal observation, the mechanisms whereby this is implemented, from substrates used and enzymes involved in their production, differ among taxa (reviewed in refs. [26,30]) among species, suggesting subtle evolutionary differences among them.

Genomic responses to dehydration in angiosperms

The majority of (DS) angiosperms produce desiccation-tolerant seeds. This is a complicating factor in the quest for a genomic ‘blueprint’ of DT as it implies that the genetic information for DT is present in the genome but exclusively expressed in the seeds (and pollen). Therefore, comparing the genomes of tolerant and sensitive species is only meaningful when supplemented by genome-wide expression studies. However, this poses extra complications as expression of genes, proteins and metabolites must ideally be monitored during dehydration and rehydration. Obviously, the sensitive plant will not survive below a critical water content. Thus, to avoid comparing living with dead (or dying) tissues, it necessitates comparison above the critical water content of the sensitive tissues at 50–60% RWC. Yet, this will only reflect a drought-, or early dehydration response, and not desiccation response, which occurs between 40 and 20% RWC [19,3134]. Thus, a sister lineage approach may have only limited value in this context.

Since DS seeds seem to possess the majority of protective mechanisms to desiccation damage, we may assume that relatively few regulatory genes are impaired in their function to lead to DS seeds. This is corroborated by the observation that application of exogenous hormones like ABA (abscisic acid) or inhibitors of GA (gibberellin) biosynthesis may re-establish DT in DS seeds [12]. Identification and characterization of these genes may lead to important insights into the regulation of DT.

Whole-genome analysis

The number of sequenced resurrection genomes available (Table 1) is still too low to allow reliable extraction of recurrent genetic information to identify the genomic signature of a common mechanism of (vegetative) DT. Among the core and conserved features of DT are the ability to ameliorate against free radical damage (particularly that associated with photosynthesis), production of protective substances such as sucrose and RFOs, LEAs and heat shock proteins (inter alia) and the ability to form glasses in air dry tissue, which contributes to longevity and tolerance of temperatures from −70°C to above 60°C. Some of the major players of these conserved features of DT have been studied, to some detail, in a genomic context. Among these are the LEA proteins and ELIPs.

Table 1
Resurrection species with a sequenced genome
SpeciesCladeGenome sizePCGReference
Physcomitrella patens Bryophyte ∼500 Mb 35,938 [35
Selaginella lepidophylla Lycopodiophyta ∼109 Mb 27,204 [31
Selaginella tamariscina Lycopodiophyta ∼301 Mb 27,761 [33
Xerophyta viscosa Monocots ∼295.5 Mb 25,425 [19
Oropetium thomaeum Monocots ∼245 Mb 28,466 [9,36
Boea hygrometrica Eudicots ∼1,691 Mb 49,374 [37
Lindernia brevidens Eudicots ∼270 Mb 27,204 [32
SpeciesCladeGenome sizePCGReference
Physcomitrella patens Bryophyte ∼500 Mb 35,938 [35
Selaginella lepidophylla Lycopodiophyta ∼109 Mb 27,204 [31
Selaginella tamariscina Lycopodiophyta ∼301 Mb 27,761 [33
Xerophyta viscosa Monocots ∼295.5 Mb 25,425 [19
Oropetium thomaeum Monocots ∼245 Mb 28,466 [9,36
Boea hygrometrica Eudicots ∼1,691 Mb 49,374 [37
Lindernia brevidens Eudicots ∼270 Mb 27,204 [32

Abbreviation: PCG, predicted protein-coding genes.

LEA proteins

Genome and transcriptome analysis of basal resurrection plants has revealed loss of genes associated with the aquatic lifestyle, the development of hormonal signalling pathways (such as auxin and ABA), and acquisition of genes and expansion of gene families necessary for osmotic- and thermo-regulation in the terrestrial lifestyle, such as LEA protein gene families [31,33,35,38].

LEAs were first discovered as accumulating in the later stages of embryo development in cotton seeds and have been associated with the acquisition of DT in orthodox seeds [3941]. Since then, LEA proteins have been detected in other parts of the plant, such as seedlings, stems, leaves and roots as a response to abiotic stresses including drought, salinity, heat and cold. We hypothesize that these non-DT-related LEAs are remnants of ancient DT that were subject to neofunctionalization in abiotic stress response. Interestingly, the accumulation of LEA (or LEA-like) proteins under desiccation is also commonly observed in kingdoms other than Plantae such as in anhydrobiotic bacteria and invertebrates [42]. These observations might suggest that LEAs are indispensable for DT establishment in living organisms. However, observations of the occurrence of LEAs in DS seeds strongly suggest that LEAs may be necessary but not sufficient for the acquisition of DT [39].

The majority of these proteins are hydrophilic and small, and display heat stability, anti-aggregation and protein stabilizing properties [4348]. Under low water availability, sugars and LEA proteins can form intracellular glasses that help to stabilize membranes, avoid solute leakage, control water and ion uptake, and slow down oxidative reactions; conferring long-term stability to the cytoplasm in the dry state [4951]. Moreover, their highly disordered character, ability to fold into an α-helix when subjected to water deficit and/or macromolecular crowding environments, and the presence of RNA-binding domains such as fused in sarcoma, are leading to investigations of their role in liquid–liquid phase separation and formation of membraneless compartments [5254]. Here, it has been proposed that their conformational flexibility may play a role in molecular memory and for sensing perturbations in the physicochemical environment of the cell [54]. We propose that LEAs expressed exclusively during the late stages of dehydration may play a role in continued gene expression and regulation at low water contents.

Genomic analysis of LEA proteins in several plant species has revealed a dynamic evolutionary history and diversification of genomic context, as well as protein structural and functional diversification [55]. These characteristics may have contributed to the functioning of distinct sets of LEAs under water deficit stress and may be one of the major protective features that were evolutionarily selected for in resurrection plants.

Supporting this is the observation that LEA families are found, in larger numbers in the genomes of the resurrection plants Selaginella lepidophylla, Selaginella tamariscina, Lindernia brevidens and Xerophyta viscosa compared with closely related species [19,32,33,34] (Table 2). LEAs are also highly expressed under desiccation conditions in the majority of the resurrection species for which genomes and transcriptomes have been analysed [9,32,35,37].

Table 2
The number of LEA genes in resurrection plant genomes [19,31–33]
DHNLEA_1LEA_2LEA_3LEA_4LEA_5LEA_6SMPTotal
Physcomitrella patens 27 12 50 
Selaginella lepidophylla 31 14 11 65 
Selaginella tamariscina 14 40 
Xerophyta viscosa 12 57 23 10 126 
Oropetium thomaeum 58 97 
Boea hygrometrica 39 67 
Lindernia brevidens 36 14 77 
DHNLEA_1LEA_2LEA_3LEA_4LEA_5LEA_6SMPTotal
Physcomitrella patens 27 12 50 
Selaginella lepidophylla 31 14 11 65 
Selaginella tamariscina 14 40 
Xerophyta viscosa 12 57 23 10 126 
Oropetium thomaeum 58 97 
Boea hygrometrica 39 67 
Lindernia brevidens 36 14 77 

Abbreviations: DHN, dehydrins; SMP, seed maturation proteins.

LEA gene families have contracted and even disappeared in aquatic (Spirodela polyrhiza) and marine (Zostera marina) [56] monocot species, which is an indication that these specific LEA families are, to a certain extent, related to the establishment of DT. Furthermore, there is a considerably lower expression of LEAs associated with DT in the desiccation-sensitive seeds of C. australe [12], which led the authors to suggest that some LEAs essential for the DT phenotype have been mutated/silenced in this species. In this sense, the ability to synthesize LEA proteins at a right proportion and at the correct moment is demonstrated in both desiccation-tolerant seeds and resurrection plants to achieve DT, and to re-establish normal metabolic activity post-rehydration.

Early light-induced proteins

ELIPs are proposed to protect the photosynthetic complex from photo-oxidative damage by binding photosynthetic pigments and have long been associated with vegetative DT [57,58]. Expansion of the ELIP gene family has been reported for the desiccation-tolerant species Boea hygrometrica (17 members) [37], L. brevidens (26 members, including a tandem array of 19 duplicates, as opposed to sensitive L. subracemosa with only four members) [31] and S. lepidophylla (23 members in three tandem arrays) [32] (Table 3). All of these species display a homoiochlorophyllous phenotype, retaining chlorophyll and thylakoid membranes during desiccation. Interestingly, X. viscosa which degrades most of its chlorophyll and thylakoids during dehydration has only two members [19]. This suggests that expansion of ELIPs in genomes is related to the homoiochlorophyllous phenotype. In this regard, the genomic expansion and co-ordination of ELIP gene expression is a successful strategy to avoid light-induced damages that may accompany desiccation in such species. Furthermore, DS species closely related to resurrection plants display a smaller number of ELIPs in their genomes [31,32], which provides support to the hypothesis that ELIPs expansion has been only recurrent during the evolution of homoiochlorophylly and is strongly associated with DT in those species.

Table 3
The number of ELIP genes in resurrection plant genomes

Data taken from VanBuren et al. [31] and Xu et al. [33].

SpeciesPhenotypeELIPs
Physcomitrella patens Homoiochlorophyllous 17 
Selaginella lepidophylla Homoiochlorophyllous 23 
Selaginella tamariscina Homoiochlorophyllous 
Xerophyta viscosa Poikilochlorophyllous 2–4 
Oropetium thomaeum Poikilochlorophyllous 
Boea hygrometrica Homoiochlorophyllous 17 
Lindernia brevidens Poikilochlorophyllous 26 
Selaginella moellendorffii Desiccation sensitive 
Arabidopsis thaliana Desiccation sensitive 
SpeciesPhenotypeELIPs
Physcomitrella patens Homoiochlorophyllous 17 
Selaginella lepidophylla Homoiochlorophyllous 23 
Selaginella tamariscina Homoiochlorophyllous 
Xerophyta viscosa Poikilochlorophyllous 2–4 
Oropetium thomaeum Poikilochlorophyllous 
Boea hygrometrica Homoiochlorophyllous 17 
Lindernia brevidens Poikilochlorophyllous 26 
Selaginella moellendorffii Desiccation sensitive 
Arabidopsis thaliana Desiccation sensitive 

Genome-wide expression

Comparison of transcriptomes of several resurrection species, including Haberlea rhodopensis, Oropetium thomaeum, Sporobolus stapfianus, S. lepidophylla, S. tamariscina, L. brevidens and X. viscosa largely confirms the consistent expression of a collection of genes and proteins (potentially) important in the regulation of DT [9,19,31,32,59]. Not surprisingly, these include genes coding for LEA proteins, heat shock proteins, antioxidant enzymes, cell wall modification enzymes, enzymes involved in carbohydrate metabolism, and components of signal transduction, such as the ABA signalling pathway. As indicated above, these seem to be common elements in DT across species.

A substantial number of these genes have been assumed to be seed-specific, but it is now clear that they play similar roles in the vegetative DT response. As indicated above, it is likely that seed- and vegetative DT have been co-opted [7,9]. As in resurrection species, the DT mechanism in seeds is engaged by a loss of water. A striking example is the expression of the larger part of the ABI3 regulon in leaves during dehydration of X. viscosa [19]. ABI3 is a B3 domain-containing transcription factor. The ABI3 regulon in Arabidopsis thaliana consists of nearly 100 genes which are thought to be committed to seed maturation [60]. In addition, analysis of cis-elements of differentially expressed DT-related genes provides information about potential higher order regulators of DT, e.g. transcription factors. For example, in X. viscosa these include PIF1, PIF4, ABF1 and ABI5 [19] and in H. rhodopensis MYB, NAC, WRKY and DREB2 [61].

A clue about DT-associated genes that are specific for a species may lead to the identification of a species-specific adaptive strategy. It is particularly useful to explore the genes that underwent duplication and are differentially expressed during de- and rehydration. In the genome of X. viscosa, such clusters of desiccation-associated genes (CoDAGs) were found. CoDAGS host a paralogous set of genes, containing at least one pair of genes and all genes located within CoDAGs are differentially expressed in response to de- and rehydration. The genome of X. viscosa contains 277 CoDAGs with 600 genes involved [19] which are largely composed of genes with declining transcript abundance upon dehydration, including (inter alia) the ABA receptor PYL (pyrabactin resistance-like), ABC transporters, ethylene-responsive transcription factors, intracellular ribonucleases and LEA proteins. The decline in abundance upon dehydration may be related to the suppression of growth or energy metabolism in the vegetative tissues, or that the genes in these CoDAGs suppress the expression of DT in vegetative tissues [19].

The regulation of gene expression upon dehydration of resurrection plants may occur at the epigenetic and transcriptional level. In drying leaves of X. viscosa, the different classes of LEA genes display differential enrichment of promoter elements, indicating differential regulation by (putative) transcription factors [19]. For example, the LEA_1 family is enriched for promoter elements that putatively bind the phytochrome-interacting (transcription) factors PIF1 and PIF2 which are involved in phytochrome-induced repression of photosynthesis and response to temperature, respectively [62]. Thus, such differential enrichment may control the response of the different classes of LEAs to various environmental components, including light, temperature and drought.

Epigenetics

One of the most crucial questions on the topic of genome-level responses to the environment is the control of gene expression through changes in the epigenetic landscape. Despite the importance of epigenetic modifiers in plant responses to environmental stimuli and modulation of gene expression, stress response and adaptation, there are only a few published reports on the identification of epigenetic modifiers from DT plants. In C. plantagineum, the ABA-induced retrotransposon CDT-1 controls the synthesis of a small interfering RNA similar to miR159, which is involved in plant responses to drought and ABA [63]. Moreover, CDT-2, an additional mutant similar to CDT-1, leads to increased expression of desiccation-associated genes and to desiccation-tolerant callus without the application of ABA in C. plantagineum [64]. Transgenic A. thaliana plants carrying a retroelement fragment from B. hygrometrica designated osmotic and alkaline resistance 1 (OAR1) had increased osmotic and alkaline stress tolerance compared with control plants [65]. When stressed, short transcripts originating from OAR1 increased in both B. hygrometrica and transformed A. thaliana [66]. Transcripts involved in chromatin remodelling and gene and RNA silencing increase in abundance in X. viscosa leaves during drying, whereas transcripts of Polycomb-group proteins and interacting components decrease in abundance [19]. A genome-wide profiling of micro-RNAs in the desiccation-tolerant species Tripogon loliiformis identified several predicted transcription factors associated with micro-RNAs decreasing abundance during desiccation [66]. One example is the nuclear factor Y B subunits, which confer drought tolerance and lead to improved maize yields under water-limited conditions [66,67]. Although S. lepidophylla lacks evidence of gene body methylation, intact long terminal repeat retrotransposons have high levels of CpG and CHG methylation with comparatively little CHH methylation [31].

Summarizing conclusion and prospects

Next-generation sequencing has provided the exciting possibility to study whole-genome responses to the environment, both as evolutionary adaptation and as immediate response to a changing environment. Using the case of DT, we have reviewed the progress in elucidating its molecular mechanisms and species specificity, summarized in Figure 2, using whole-genome approaches. We conclude that species displaying DT use similar ‘toolboxes’ in their response to severe drought but have also adopted species- or clade-specific changes in engaging the DT response at the right time. Analysing more genomes of resurrection species will undoubtedly lead to understanding their evolutionary adaptation, and aid to (further) elucidation of (core) molecular mechanisms. Potentially, this knowledge may be very useful to generate crops with tolerance to severe drought, implying a radically different approach from current efforts, which have not been very successful yet, due to the complexity of the drought response [68].

Summary of key regulatory and protective components (and genes) associated with DT in resurrection plants.

Figure 2.
Summary of key regulatory and protective components (and genes) associated with DT in resurrection plants.

Higher order epigenetic regulators co-ordinate the expression of transcription factors that control major downstream processes (such as cellular protection and energy metabolism). Species-specific differences in the latter, arising from niche-related evolutionary pressures, result in phenotypical differences among them, as typified by alternative mechanisms of homoiochlorophylly and poikilochlorophylly.

Figure 2.
Summary of key regulatory and protective components (and genes) associated with DT in resurrection plants.

Higher order epigenetic regulators co-ordinate the expression of transcription factors that control major downstream processes (such as cellular protection and energy metabolism). Species-specific differences in the latter, arising from niche-related evolutionary pressures, result in phenotypical differences among them, as typified by alternative mechanisms of homoiochlorophylly and poikilochlorophylly.

Summary

  • Most land plants have the genetic potential for DT, but this is displayed only in orthodox seeds, some pollen and the vegetative tissues of resurrection plants.

  • There is a core set of conserved features of DT in plant tissues, including the ability to reversibly down-regulate photosynthesis, prevent free radical damage and production of appropriate quantities and ratios of cellular protectants such as oligosaccharides and LEA proteins.

  • Whole-genome and transcriptome analyses show that there are species and clade-specific differences in the orchestration of these components to achieve DT, likely due to different niche-related evolutionary pressures and/or epigenetic modification.

  • Examples of clade-specific differences include the expansion and of ELIP gene families in resurrection plants displaying homoiochlorophylly. A species-specific adaptation in X. viscosa is evident in the presence of CoDAGS, likely ensuring metabolic quiescence and longevity in the desiccated state.

Abbreviations

     
  • ABA

    abscisic acid

  •  
  • CoDAGs

    clusters of desiccation-associated genes

  •  
  • DS

    desiccation-sensitive

  •  
  • DT

    desiccation tolerance

  •  
  • ELIPs

    early light-induced proteins

  •  
  • LEA

    late embryogenesis-abundant

  •  
  • OAR1

    osmotic and alkaline resistance 1

  •  
  • RFOs

    raffinose family oligosaccharides

  •  
  • ROS

    reactive oxygen species

  •  
  • RWC

    relative water content

Funding

J.M.F. contributed towards this work with funding from the National Research Foundation [grant no. 69416] and her DST-NRF South African Research chair [grant no. 98406].

Acknowledgements

We thank Keren Cooper for the design of Figure 1.

Competing Interests

The Authors declare that there are no competing interests associated with the manuscript.

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