Molecular responses to dehydration and desiccation in desiccation-tolerant angiosperm plants

Molecular responses to dehydration and desiccation in desiccation-tolerant angiosperm plants Abstract Due to the ability to tolerate extreme dehydration, desiccation-tolerant plants have been widely investigated to find potential approaches for improving water use efficiency or developing new crop varieties. The studies of desiccation-tolerant plants have identified sugar accumulation, specific protein synthesis, cell structure changes, and increased anti-oxidative reactions as part of the mechanisms of desiccation tolerance. However, plants respond differently according to the severity of water loss, and the process of water loss affects desiccation tolerance. A detailed analysis within the dehydration process is important for understanding the process of desiccation tolerance. This review defines dehydration and desiccation, finds the boundary for the relative water content between dehydration and desiccation, compares the molecular responses to dehydration and desiccation, compares signaling differences between dehydration and desiccation, and finally summarizes the strategies launched in desiccation-tolerant plants for dehydration and desiccation, respectively. The roles of abscisic acid (ABA) and reactive oxygen species (ROS) in sensing and signaling during dehydration are discussed. We outline how this knowledge can be exploited to generate drought-tolerant crop plants. ABA, dehydration, desiccation, desiccation tolerance, molecular responses, ROS, stress signaling Introduction Water stress often affects growth and development of crop plants and leads to substantial loss in food production. How to improve water stress tolerance in plants is a core question in agricultural activities. In nature, there are some plants that can tolerate >90% water loss and resume physiological activities within hours after regaining water supply (Alpert, 2006). These plants are grouped as ‘resurrection plants’ and their ability to tolerate nearly complete drying is called ‘desiccation tolerance’ (Jenks and Wood, 2008; Lüttge et al., 2011). The studies of resurrection plants may provide approaches for developing new crop varieties and designing new water management strategies in crop production. To date, research has demonstrated that the mechanism of plant desiccation tolerance is closely related to the accumulation of sugars (e.g. sucrose), the large-scale synthesis of specific proteins (e.g. late embryogenesis abundant proteins), and the adaptive adjustment of cell structures (e.g. cell wall) (Hoekstra et al., 2001; Moore et al., 2009). A few resurrection plant species including Physcomitrella patens (Cove et al., 2006), Craterostigma plantagineum (Bartels and Salamini, 2001), Boea hygrometrica (Mitra et al., 2013), Xerophyta viscosa (Farrant et al., 2015), and Sporobolus stapfianus (Gaff et al., 2009) have been substantially investigated so that they are becoming potential model plants. In recent years, increasing systematic data from transcriptomes, proteomes, and metabolomes are facilitating our understanding of plant desiccation tolerance (Gechev et al., 2012; Giarola et al., 2017). The availability of genome sequences makes some plants suitable as model plants among resurrection plants, such as P. patens (Rensing et al., 2008) B. hygrometrica (Xiao et al., 2015), Oropetium thomaeum (VanBuren et al., 2015), and X. viscosa (Costa et al., 2017). Most studies focus on comparing well-watered plants with desiccated plants and rehydrated plants to reveal important factors affecting plant desiccation tolerance. A comparison between moderate dehydration and complete dehydration (desiccation) has hardly been addressed. To understand mechanisms underlying desiccation, the recognition of changes in terms of water stress sensing and transition of metabolic reactions during mild to moderate and complete dehydration is necessary. For example, in the transcriptome analysis of Myrothamnus flabellifolia, a total of 8287 differentially transcribed genes (DTGs) were detected during dehydration, but only 204 DTGs were up-regulated and 547 DTGs were down-regulated during all different dehydration stages [90, 75, and 27% relative water contents (RWCs)] (Ma et al., 2015). This raises the question: what are the roles of the DTGs up-regulated or down-regulated from slight to moderate or from moderate to complete dehydration? Another example is the proteome analysis of X. viscosa, which identified a number of dehydration-responsive proteins. These proteins were grouped into three classes based on their expression patterns: early dehydration-responsive (significant change only at 65% RWC), late dehydration-responsive (significant change only at RWC 35%), and full dehydration-responsive (with altered levels of expression at both 65% and 35% RWC) (Ingle et al., 2007). This shows that differential responses exist at early and late stages of dehydration. Similarly, non-resurrection plants, such as Arabidopsis thaliana or Sorghum bicolor, respond with different gene expression programs to mild and severe dehydration (Buchanan et al., 2005; Denby and Gehring, 2005). This difference is also reflected on the metabolite level. Using untargeted global metabolomics analysis, Oliver et al. (2011a) revealed that the levels of glucose, fructose, and galactinol declined in S. stapfianus only at RWCs from 80% to 40%, and the levels of alanine and aspartate only significantly decreased at 50% RWC. Because of the importance of understanding the differences of plant responses between dehydration and desiccation, this review summarizes the advance of studies on model or non-resurrection plants. New hypotheses are proposed on plant response mechanisms to dehydration and desiccation. Drought, dehydration, and desiccation When water stress is mentioned, ‘drought, dehydration, or desiccation’ are used to describe the stressed status of plants. A clear distinction between drought, dehydration, and desiccation is the first step for a comparative analysis in terms of morphological, physiological, and molecular responses. Early in 1973, Hsiao tried to classify the plant water status into ‘hydrated, mild stress, moderate stress, severe stress, and desiccation’ according to the severity of stress (Hsiao, 1973; for details see Table 1). However, this classification of the water status does not describe the differences between drought, dehydration, and desiccation correctly, because not only is the amount of water loss important, but the rate of dehydration and the duration of the stress also determine responses to water deficit (Bray, 1997). As ‘drought’ is closely related to agricultural production, it is often used to describe water deficit, even in some experimental studies regarding resurrection plants, such as the studies by Cui et al., (2012) or Gechev et al. (2013). According to Huang et al., (2010), Levitt (1985), and Talamè et al. (2007), we propose the following definitions: (i) drought is a slow process during which transpiration exceeds water uptake in plants that mainly grow in soil; (ii) dehydration implies that whole plants or detached organs encounter a steady water loss and are often kept in air to lose water; and (iii) desiccation is the final result of dehydration and the water status is equilibrated with the air (desiccated is equal to extremely dehydrated). This review focuses on comparing plant responses to dehydration and desiccation. Table 1. Plant water status under various stress conditions Water status  Water potential (Ψ)  Relative water contents  Hydrated  0 bar  80–100%a  Mild stress  5–10 bars lower  8–10% lower  Moderate stress  12–15 bars lower  10–20% lower  Severe stress  >15 bars lower  >20% lower  Desiccation  >35 bars lowerb  >50% lower  Water status  Water potential (Ψ)  Relative water contents  Hydrated  0 bar  80–100%a  Mild stress  5–10 bars lower  8–10% lower  Moderate stress  12–15 bars lower  10–20% lower  Severe stress  >15 bars lower  >20% lower  Desiccation  >35 bars lowerb  >50% lower  The data are cited from Hsiao (1973). a Data obtained from Farrant et al. (2015), Ingram et al. (1997), Jiang et al. (2007), Mladenov et al. (2015), Oliver et al. (2011a), and Cui et al. (2012). b Data obtained from Boyer (1976). View Large Table 1. Plant water status under various stress conditions Water status  Water potential (Ψ)  Relative water contents  Hydrated  0 bar  80–100%a  Mild stress  5–10 bars lower  8–10% lower  Moderate stress  12–15 bars lower  10–20% lower  Severe stress  >15 bars lower  >20% lower  Desiccation  >35 bars lowerb  >50% lower  Water status  Water potential (Ψ)  Relative water contents  Hydrated  0 bar  80–100%a  Mild stress  5–10 bars lower  8–10% lower  Moderate stress  12–15 bars lower  10–20% lower  Severe stress  >15 bars lower  >20% lower  Desiccation  >35 bars lowerb  >50% lower  The data are cited from Hsiao (1973). a Data obtained from Farrant et al. (2015), Ingram et al. (1997), Jiang et al. (2007), Mladenov et al. (2015), Oliver et al. (2011a), and Cui et al. (2012). b Data obtained from Boyer (1976). View Large Water loss in resurrection plants Resurrection plants possess desiccation tolerance; does this mean that they have better resistance mechanisms to water loss than non-desiccation-tolerant plants? Several studies have provided answers to this question. Schwab et al. (1989) found that the rate of water loss during dehydration of detached leaves of the resurrection plant C. plantagineum was comparable with or even faster than that of the mesophyte spinach under identical conditions. By comparing the resurrection plant B. hygrometrica with its desiccation-sensitive relative Chirita heterotrichia, Deng et al. (2003) also observed that leaves of B. hygrometrica lost water during dehydration more rapidly than C. heterotrichia. Similarly, the water loss in the detached leaves of Haberlea rhodopensis (desiccation tolerant) was faster than in those of spinach (desiccation sensitive) (Georgieva et al., 2005). However, not all research results are consistent. For instance, the desiccation-tolerant S. stapfianus exhibited a similar drying curve to the desiccation-sensitive S. pyramidalis (Oliver et al., 2011a). The desiccation-tolerant Selaginella lepidophylla exhibited a lower rate of water loss than the desiccation-sensitive Selaginella moellendorffii (Yobi et al., 2012). From these contrasting results, it can be concluded that the rate of limiting water loss is not a necessary part of the desiccation tolerance mechanism for all resurrection plants. Response of resurrection plants to water loss and the boundary between dehydration and desiccation Understanding physiological changes during the complete process from the hydrated state to the desiccated state is the first step for a comparison between dehydration and rehydration. From the studies of P. patens (Cui et al., 2012), S. lepidophylla (Yobi et al., 2013), X. viscosa (Farrant et al., 2015), C. plantagineum (Ingram et al., 1997), S. stapfianus (Oliver et al., 2011a), and H. rhodopensis (Mladenov et al., 2015), it can be concluded that the RWCs in resurrection plants decrease in a nearly linear fashion when water is withheld. Thus it is difficult to define a precise boundary between dehydration and desiccation using RWC as the indicator. However, physiological and molecular responses differ at various degrees of water loss (Fig. 1), and the comparison of the changes provides a clue as to how to distinguish dehydration and desiccation. The distinction of dehydration and desiccation responses is helpful in understanding acquisition of desiccation tolerance. Generally, actively growing plants have an RWC of 85–100% (Gaff and Oliver, 2013). When plants are dehydrated, a series of physiological activities, such as photosynthesis and respiration, are rearranged. By summarizing the physiological performance of various desiccation-tolerant resurrection plants (Table 2), a boundary is found to distinguish dehydration and desiccation. This boundary can be defined when using RWCs to mark the water status. The data show that an RWC of ~40% is the transition from dehydration to desiccation. The changes of gene expression, protein abundance, and metabolite levels also reflect this transition. In S. stapfianus, drought-related genes (SDG2i, SDG3i, and SDG4i) are expressed at the highest levels when the RWC decreased to 39–20% (Le et al., 2007). Kuang et al. (1995) studied protein synthesis in vivo of S. stapfianus leaves during dehydration. Two main phases were distinguished according to extensive changes of in vivo proteins in S. stapfianus leaves. In the first phase (85–51% RWC), 10 novel proteins appeared and two proteins increased in abundance. In the second phase (37–3.5% RWC), 15 novel proteins appeared and two proteins increased in abundance. Through proteome analysis, Ingle et al. (2007) also proposed that the induction of putative ‘late’ protection mechanisms during dehydration is initiated at ~40% RWC in X. viscosa. In contrast to gene expression and protein synthesis, the response on the metabolite levels is delayed. Oliver et al. (2011a) studied the metabolomes of S. stapfianus at various RWCs during dehydration. The result showed that at 20% RWC, the levels of ~75% of the metabolites displayed an increased abundance during dehydration and reached the same levels as those in the desiccated tissue, especially for sucrose, raffinose family oligosaccharides, and tocopherol. Table 2. Physiological performance of some resurrection plants at specific relative water contents Plant species  RWC   Physiological performance during dehydration   References   Xerophyta scabrida  35%  Stomatal conductance reaches minimum and photosynthesis ceases  Tuba et al. (1996)  Craterostigma wilmsii, M. flabellifolius, Xerophyta humilis, and S. stapfianus  40%  Photosynthesis stops  Schwab et al. (1989); Whittaker et al. (2007); Farrant (2000);Beckett et al. (2012)  M. flabellifolius and Xerophyta humilis  40%  Respiration rate starts to decrease  Farrant (2000)  Craterostigma wilmsii and Craterostigma plantagineum  30%  Respiration rate starts to decrease  Schwab et al. (1989); Farrant (2000)  Craterostigma wilmsii, M. flabellifolius, and Xerophyta humilis  40%  Chlorophyll degradation stops  Farrant (2000); Beckett et al. (2012)  Craterostigma wilmsii, M. flabellifolius, and Xerophyta humilis  40%  Carotenoid degradation and anthocyanin accumulation stop  Farrant (2000)  Xerophyta viscosa  50%  Sucrose and raffinose family oligosaccharides accumulate to the maximum levels  Whittaker et al. (2001),Peters et al. (2007)  S. stapfianus  30%  Sucrose contents become maximal  Whittaker et al. (2001)  C. wilmsii, X. humilis, and X. viscosa  40%  Sucrose accumulation peaks  Farrant et al. (2007)  Ramonda serbica  35%  Total phenolic acid levels decreased to the levels as desiccated status  Sgherri et al. (2004)  M. flabellifolius and X. humilis  40%  The activities of glutathione reductase and superoxide dismutase reached maximum  Farrant (2000)  Tortula ruralis  30%  The percentage of oxidized glutathione (GSH) in the total GSH pool becomes maximal  Smirnoff (1993)  Haberlea rhodopensis  25%  The contents of ABA and cytokinins in leaves reach the maximum  Djilianov et al. (2013)  Selaginella tamariscina  20%  ABA reaches its maximum level  Wang et al. (2010)  Plant species  RWC   Physiological performance during dehydration   References   Xerophyta scabrida  35%  Stomatal conductance reaches minimum and photosynthesis ceases  Tuba et al. (1996)  Craterostigma wilmsii, M. flabellifolius, Xerophyta humilis, and S. stapfianus  40%  Photosynthesis stops  Schwab et al. (1989); Whittaker et al. (2007); Farrant (2000);Beckett et al. (2012)  M. flabellifolius and Xerophyta humilis  40%  Respiration rate starts to decrease  Farrant (2000)  Craterostigma wilmsii and Craterostigma plantagineum  30%  Respiration rate starts to decrease  Schwab et al. (1989); Farrant (2000)  Craterostigma wilmsii, M. flabellifolius, and Xerophyta humilis  40%  Chlorophyll degradation stops  Farrant (2000); Beckett et al. (2012)  Craterostigma wilmsii, M. flabellifolius, and Xerophyta humilis  40%  Carotenoid degradation and anthocyanin accumulation stop  Farrant (2000)  Xerophyta viscosa  50%  Sucrose and raffinose family oligosaccharides accumulate to the maximum levels  Whittaker et al. (2001),Peters et al. (2007)  S. stapfianus  30%  Sucrose contents become maximal  Whittaker et al. (2001)  C. wilmsii, X. humilis, and X. viscosa  40%  Sucrose accumulation peaks  Farrant et al. (2007)  Ramonda serbica  35%  Total phenolic acid levels decreased to the levels as desiccated status  Sgherri et al. (2004)  M. flabellifolius and X. humilis  40%  The activities of glutathione reductase and superoxide dismutase reached maximum  Farrant (2000)  Tortula ruralis  30%  The percentage of oxidized glutathione (GSH) in the total GSH pool becomes maximal  Smirnoff (1993)  Haberlea rhodopensis  25%  The contents of ABA and cytokinins in leaves reach the maximum  Djilianov et al. (2013)  Selaginella tamariscina  20%  ABA reaches its maximum level  Wang et al. (2010)  View Large Table 2. Physiological performance of some resurrection plants at specific relative water contents Plant species  RWC   Physiological performance during dehydration   References   Xerophyta scabrida  35%  Stomatal conductance reaches minimum and photosynthesis ceases  Tuba et al. (1996)  Craterostigma wilmsii, M. flabellifolius, Xerophyta humilis, and S. stapfianus  40%  Photosynthesis stops  Schwab et al. (1989); Whittaker et al. (2007); Farrant (2000);Beckett et al. (2012)  M. flabellifolius and Xerophyta humilis  40%  Respiration rate starts to decrease  Farrant (2000)  Craterostigma wilmsii and Craterostigma plantagineum  30%  Respiration rate starts to decrease  Schwab et al. (1989); Farrant (2000)  Craterostigma wilmsii, M. flabellifolius, and Xerophyta humilis  40%  Chlorophyll degradation stops  Farrant (2000); Beckett et al. (2012)  Craterostigma wilmsii, M. flabellifolius, and Xerophyta humilis  40%  Carotenoid degradation and anthocyanin accumulation stop  Farrant (2000)  Xerophyta viscosa  50%  Sucrose and raffinose family oligosaccharides accumulate to the maximum levels  Whittaker et al. (2001),Peters et al. (2007)  S. stapfianus  30%  Sucrose contents become maximal  Whittaker et al. (2001)  C. wilmsii, X. humilis, and X. viscosa  40%  Sucrose accumulation peaks  Farrant et al. (2007)  Ramonda serbica  35%  Total phenolic acid levels decreased to the levels as desiccated status  Sgherri et al. (2004)  M. flabellifolius and X. humilis  40%  The activities of glutathione reductase and superoxide dismutase reached maximum  Farrant (2000)  Tortula ruralis  30%  The percentage of oxidized glutathione (GSH) in the total GSH pool becomes maximal  Smirnoff (1993)  Haberlea rhodopensis  25%  The contents of ABA and cytokinins in leaves reach the maximum  Djilianov et al. (2013)  Selaginella tamariscina  20%  ABA reaches its maximum level  Wang et al. (2010)  Plant species  RWC   Physiological performance during dehydration   References   Xerophyta scabrida  35%  Stomatal conductance reaches minimum and photosynthesis ceases  Tuba et al. (1996)  Craterostigma wilmsii, M. flabellifolius, Xerophyta humilis, and S. stapfianus  40%  Photosynthesis stops  Schwab et al. (1989); Whittaker et al. (2007); Farrant (2000);Beckett et al. (2012)  M. flabellifolius and Xerophyta humilis  40%  Respiration rate starts to decrease  Farrant (2000)  Craterostigma wilmsii and Craterostigma plantagineum  30%  Respiration rate starts to decrease  Schwab et al. (1989); Farrant (2000)  Craterostigma wilmsii, M. flabellifolius, and Xerophyta humilis  40%  Chlorophyll degradation stops  Farrant (2000); Beckett et al. (2012)  Craterostigma wilmsii, M. flabellifolius, and Xerophyta humilis  40%  Carotenoid degradation and anthocyanin accumulation stop  Farrant (2000)  Xerophyta viscosa  50%  Sucrose and raffinose family oligosaccharides accumulate to the maximum levels  Whittaker et al. (2001),Peters et al. (2007)  S. stapfianus  30%  Sucrose contents become maximal  Whittaker et al. (2001)  C. wilmsii, X. humilis, and X. viscosa  40%  Sucrose accumulation peaks  Farrant et al. (2007)  Ramonda serbica  35%  Total phenolic acid levels decreased to the levels as desiccated status  Sgherri et al. (2004)  M. flabellifolius and X. humilis  40%  The activities of glutathione reductase and superoxide dismutase reached maximum  Farrant (2000)  Tortula ruralis  30%  The percentage of oxidized glutathione (GSH) in the total GSH pool becomes maximal  Smirnoff (1993)  Haberlea rhodopensis  25%  The contents of ABA and cytokinins in leaves reach the maximum  Djilianov et al. (2013)  Selaginella tamariscina  20%  ABA reaches its maximum level  Wang et al. (2010)  View Large Fig. 1. View largeDownload slide A scheme of plant responses to water loss during dehydration and the definition of the boundary between dehydration and desiccation. The severity of water loss is sensed. Together with other signaling, such as light and energy, the plant response strategy is decided. The boundary between dehydration and desiccation is defined based on the differential physiological and molecular changes. Fig. 1. View largeDownload slide A scheme of plant responses to water loss during dehydration and the definition of the boundary between dehydration and desiccation. The severity of water loss is sensed. Together with other signaling, such as light and energy, the plant response strategy is decided. The boundary between dehydration and desiccation is defined based on the differential physiological and molecular changes. The launch of desiccation tolerance mechanisms does not occur in desiccated tissues but starts earlier and often correlates with the transition from dehydration and desiccation. Generally, the water contents of air-dry desiccation-tolerant plants in the field are only at 5–13% RWC (Gaff, 1977). Various studies revealed that physiological and molecular responses present in the desiccated state have already been initiated when plants possess RWCs of ~40%. The proteome analysis by Oliver et al. (2011b) showed that when the leaves of S. stapfianus reached an RWC of 30%, the components critical for cellular protection are already present. Whittaker et al. (2004) and Martinelli et al. (2007a) observed that in the dehydration process of S. stapfianus from 35% RWC to dryness at 5% RWC, the leaf cells immediately begin to lose water and the protective metabolites start to accumulate with a significantly higher speed. This indicates that resurrection plants finish the preparation for staying in a quiescent state in terms of gene expression, protein synthesis, and metabolite production before being completely dry. Taking these observations into account, it is proposed that the boundary between dehydration and desiccation can be set at 30–40% RWC. Water loss and acquisition of desiccation tolerance: the dehydration process determines desiccation tolerance Acquisition of desiccation tolerance in resurrection plants is characterized by specific conditions. Many resurrection plants can survive desiccation only if the drying rate is slow (Bewley, 1997). For example, protonema of Funaria hygrometrica (moss) tolerate slow dehydration but not rapid dehydration (Werner et al., 1991), and dehydration in the perennial resurrection grass S. stapfianus must proceed slowly over a period of ≥7 d (Griffiths et al., 2014), indicating that sufficient dehydration time is required to change to a gene expression profile which enables recovery following rehydration. Specific conditions are also essential to activate the survival program. The resurrection plant B. hygrometrica requires a period of acclimation by slow soil-drying to survive a subsequent period of rapid desiccation in air (Zhu et al., 2015). Protonema of the moss P. patens are tolerant only to moderate water stress (about –13 MPa by water potential), but not to complete desiccation in experimental conditions (Koster et al., 2010). Interestingly, abscisic acid (ABA) pre-treatment can lead to the tolerance of P. patens to complete desiccation (–273 MPa) (Khandelwal et al., 2010; Koster et al., 2010). Detached leaves of S. stapfianus with >60% RWC are desiccation sensitive, indicating that desiccation tolerance is conferred to vegetative tissue of S. stapfianus when the leaf RWC has declined to <60% (Griffiths et al., 2014). Other factors (e.g. nutrient status) also affect plant desiccation tolerance. Martinelli et al. (2007b) showed that older leaves of the resurrection plant S. stapfianus were desiccation sensitive whereas younger leaves were desiccation tolerant. Zhang and Bartels (2016) demonstrated that leaves of C. plantagineum starved in dark conditions lose desiccation tolerance. Farrant et al. (2003) found that drying in the dark results in loss of viability in Craterostigma wilmsii and Myrothamnus flabellifolius, and the chemical protection (anthocyanin content and antioxidant activity) appears to be regulated by light in M. flabellifolius. These examples demonstrate that the establishment of a response strategy is based on various factors, not only on the severity of water loss (Fig.1). Although it is not known how light and nutrition affect desiccation tolerance in resurrection plants, previous studies have shown that there is a link between the response to light and drought tolerance because ABA signaling participates in the common step of both response pathways (Galvezvaldivieso et al., 2009; Rossel et al., 2006). Stress and energy signaling are closely linked and they might be regulated by the evolutionarily conserved energy sensor protein kinases (Baenagonzález et al., 2007; Baenagonzález and Sheen, 2008). Based on these points, it is hypothesized that light and nutrition affect desiccation tolerance acquisition via similar ways. Comparative analysis between dehydration and desiccation To compare the different responses between dehydration and desiccation, a full understanding is necessary of the cellular and molecular transition from dehydration to desiccation (or from high RWC to lower RWC) in terms of gene expression, protein synthesis and degradation, and related metabolite changes. Many transcriptome, proteome, and metabolome studies of resurrection plants such as P. patens (Cui et al., 2012), C. plantagineum (Rodriguez et al., 2010), B. hygrometrica (Zhu et al., 2015), S. stapfianus (Oliver et al., 2011a), and X. viscosa (Ingle et al., 2007) investigated the changes of gene transcripts, protein abundance, and metabolite levels at various RWCs (from high to low) (Giarola et al., 2017). By analyzing the data from these studies, the performance of gene transcript level, protein abundance, or metabolite level from higher RWCs to lower RWCs can be classified into seven performance types (Fig. 2). Among them, type 1 does not change the performance at various RWCs during dehydration, such as the EF1a gene and GAPDH gene in C. plantagineum (Giarola et al., 2015) and the alanine and aspartate contents in H. rhodopensis (Mladenov et al., 2015). Type 2 and type 3 respond positively or negatively to dehydration, and the response intensity increases with degree of dehydration. Representatives of type 2 are late embryogenesis-like proteins (Rodriguez et al., 2010) or aldehyde dehydrogenases (Kirch et al., 2001) in C. plantagineum. Examples of type 3 are the large subunit of Rubisco in B. hygrometrica (Jiang et al., 2007) and the starch content in S. stapfianus (Whittaker et al., 2007). There are two types (type 4 and type 5) that first respond positively or negatively to dehydration and then recover to the initial level. Type 4 is exemplified by Rubisco activase in S. tamariscina (Wang et al., 2010) and fructose and galactinol in S. stapfianus (Oliver et al., 2011a), while type 5 is represented by the heat shock protein 70 (HSP 70) in S. tamariscina (Wang et al., 2010) and aspartate and pyruvate in S. stapfianus (Oliver et al., 2011a). Type 6 is completely inhibited by dehydration and thus is not present in the desiccated state. Two examples of type 6 are glutamine synthetase in S. tamariscina (Wang et al., 2010) and arginine and linolenate in S. stapfianus (Oliver et al., 2011a). In contrast, type 7 is specifically responsive to desiccation, and examples are citrate and 1-palmitoylglycerophosphocholine in S. stapfianus (Oliver et al., 2011a). It is difficult to place all reactions of a physiological process into a specific performance type. For instance, most proteins involved in photosynthesis (e.g. Rubisco) decline in abundance, but certain proteins (e.g. chloroplastic aldolase) accumulated. However, the methodology using performance types provides a good basis to understand the difference between dehydration and desiccation. Within these performance types, type 4 and type 7 show positive responses to dehydration and desiccation, respectively, thus providing an excellent starting point for comparative analysis. Comparison of gene expression between dehydration and desiccation In the transcriptome analysis of C. plantagineum, the 500 most variable transcripts were analyzed and they were divided into six clusters according to their expression signatures under hydrated (95% RWC), dehydrated (80% RWC), desiccated (5% RWC), and rehydrated (90% RWC) conditions (Rodriguez et al., 2010). These clusters can be correlated with the performance types depicted in Fig. 2. Type 4 corresponds to cluster II that includes the 112 most abundant transcripts exclusively present in the early dehydrated sample and type 7 corresponds to cluster III that contains the 88 most abundant transcripts in the desiccated sample. The profile of abundant transcripts in the early dehydrated sample indicates predominant expression of proteins involved in ABA-mediated responses to water stress and general abiotic and biotic stresses including ion homeostasis-related proteins. Cluster II mainly represents transcripts related to thiamine metabolism, which is proposed to function in response to abiotic and biotic stress in plants (Goyer, 2010), for example protecting plants from oxidative stress (Tunc-Ozdemir et al., 2009). Desiccated samples (cluster III) were characterized by a predominance of transcripts involved in tryptophan metabolism, as well as in processes related to the metabolism of indole derivatives. These biological functions may be involved in the salvage of precursors for the metabolism of proteins and nucleic acids in the desiccated, quiescent stage. In the transcriptome of the woody resurrection plant M. flabellifolia (Ma et al., 2015), the DTGs were mapped into the Kyoto Encyclopedia of Genes and Genomes (KEGG) database. Results showed that, except for the enriched pathways of DTGs due to dehydration and desiccation (biosynthesis of secondary metabolites, photosynthesis, nitrogen metabolism, glutathione metabolism, carbon fixation in photosynthetic organisms, terpenoid backbone synthesis, and flavonoid biosynthesis), enriched pathways of DTGs during early dehydration (90% water retention) include starch and sucrose metabolism, phagosome, fatty acid synthesis, phenylalanine metabolism, and linoleic acid metabolism. Enriched pathways of DTGs during moderate dehydration (75% water retention) involve fructose and mannose metabolism, pentose phosphate pathways, porphyrin and chlorophyll metabolism, and alanine, aspartate, and glutamate metabolism. In contrast, those pathways specifically include phenylalanine, tyrosine, and tryptophan biosynthesis in desiccated tissues (27% water retention). Altogether, the different gene expression patterns indicate that dehydration mainly leads to reactions to prevent or repair cellular damage and adjustment of physiological metabolism, while desiccation tends to conserve structures and prepare for the recovery process. Fig. 2. View largeDownload slide Scheme of performance types for gene transcript level, protein abundance, and metabolite level during dehydration. By comparing the performance of gene transcript level, protein abundance, or metabolite level before and after the boundary of dehydration and desiccation (~40% RWC), seven performance types are summarized (type 1–type 7). Fig. 2. View largeDownload slide Scheme of performance types for gene transcript level, protein abundance, and metabolite level during dehydration. By comparing the performance of gene transcript level, protein abundance, or metabolite level before and after the boundary of dehydration and desiccation (~40% RWC), seven performance types are summarized (type 1–type 7). Comparison of protein accumulation in dehydration and desiccation Protein abundance during dehydration suggests that programmed regulation of protein expression is triggered by changes of the water status. Thirty-five percent of the analyzed proteins in the B. hygrometrica proteome were transiently induced during dehydration with different kinetics and consequently represent proteins that function at specific stages during the program that leads to dehydration tolerance. Among these 78 proteins, 30 proteins were induced by dehydration within 0.5 h (RWC 79%). These included a putative ABC transporter ATPase, glutathione peroxidase, and polyphenol oxidase. The appearance of new proteins in early dehydration may be due to rapid de novo synthesis or post-translational processing of pre-existing proteins that are modified when the dehydration signal is perceived. Accumulation of 36 proteins and 12 proteins of the dehydration-responsive proteins was initiated by dehydration after 8 h (RWC 6.7%) and after 48 h (RWC 2.4%), respectively. Proteins in this group included the Rubisco large subunit (LSU), the oxygen-evolving complex (OEC) of PSII, vacuolar H+-ATPase A subunit, and glutathione S-transferase. These proteins may be transcribed and translated in response to the initial dehydration signal. The existence of distinct expression profiles suggests that different sets of proteins are programmed to function in protection against dehydration (Jiang et al., 2007). In the proteome analysis of X. viscosa, the proteins which were increased and decreased by dehydration and the de novo synthesized proteins (54 in total) were divided into three groups based on their expression patterns. Eight proteins were early dehydration responsive (significant change at 65% RWC), suggesting a possible role during the initial stages of drying, while 24 were late dehydration responsive (change at 35% RWC), perhaps indicating a role in the late stages of drying (Ingle et al., 2007). Within the 54 proteins, 17 proteins were identified and, among them, two components of the luminal OEC of PSII (psbO and psbP), the α-subunit of the F-ATPase, transketalose, ascorbate peroxidase, and glutamate:glyoxylate aminotransferase I decreased in abundance at 35% RWC compared with at 65% RWC. In contrast, the abundance of alcohol dehydrogenase and 2-Cys peroxiredoxin became higher at 35% RWC; RNA-binding proteins and desiccation-related proteins were de novo synthesized only at 35% RWC. Wang et al. (2010) investigated the differentially expressed proteins in S. tamariscina under dehydration. A total of 138 proteins were identified, which showed at least a 1.5-fold change in abundance under dehydration and rehydration conditions. By hierarchical clustering, two main clusters (cluster I and cluster II) were formed. Cluster I included 24 proteins whose abundances increased upon dehydration, while cluster II contained 114 down-regulated proteins. In cluster II, the abundance of 23 proteins (sub-cluster I) was up-regulated 1 d after dehydration 1 (49% water content) and then down-regulated 3 d after dehydration (19% water content), and the abundance of 10 proteins (sub-cluster II) was up-regulated 5 d after dehydration (11% water content) and down-regulated at other stages. The comparison between sub-cluster I and sub-cluster II provides the possibility to distinguish dehydration and desiccation. Sub-cluster I includes Rubisco LSU, 6-phosphogluconate dehydrogenase, transketolase, enolase, methionine synthase, eukaryotic initiation factor 4A, leucine aminopeptidase, V-type proton ATPase subunit B1, putative centromere protein containing the RecF/RecN/SMC N-terminal domain, and GC3/GDAP1 (grip-related ARF-binding domain), while sub-cluster II includes high chlorophyll fluorescence 136 (HCF136), chloroplast precursor of phosphoribulokinase (PRK), electron carrier/iron–sulfur cluster binding, NBS-LRR resistance-like protein J71, and putative FtsH protease. This demonstrates that cellular changes of various aspects occur and include photosynthesis, carbohydrate metabolism, protein synthesis and degradation, and membrane transport, as well as cell division and differentiation. In contrast, the response to desiccation includes cellular proteins and stress defense; for example, the HCF136 protein is essential for assembly of PSII (Plücken et al., 2002) and FtsH contributes to maintain membrane protein stability (Ito and Akiyama, 2005). Although both dehydration and desiccation lead to increased abundance of proteins protecting cellular structure and defending against antioxidative stress, dehydration results in adjustments of various metabolic pathways while the response to desiccation contains some activities to prepare for new ‘life’ after dehydration. For instance, during dehydration of P. patens, the synthesis of proteins associated with photosynthesis and photorespiration is down-regulated and the synthesis of proteins associated with reactive oxygen species (ROS) signaling increases; in contrast, HSPs accumulate in desiccated plants to preserve protein function upon rehydration (Wang et al., 2009; Cui et al. 2012). Comparison of metabolite levels between dehydration and desiccation During early stages of dehydration (60% and 50% RWC), leaves of S. stapfianus displayed an increased abundance of many amino acids, carbohydrates, and antioxidants; for example, the amino acids glycine, isoleucine, leucine, proline, tryptophan, tyrosine, and valine all increased between 2- and 5-fold. Sugars such as fructose, galactose, glucose, maltose, raffinose, sophorose, and sucrose increased between 1.8-fold and >18-fold. As a strong cellular antioxidant, β-tocopherol increased >3-fold (Oliver et al., 2011a). Compared with dehydration, the stage near desiccation and desiccation itself resulted in a change of over half (89 of 167 metabolites) of the metabolome. More amino acid and carbohydrate species accumulated, such as α-ketoglutarate-derived amino acids, sugar alcohols, and carbohydrates involved in the tricarboxylic acid (TCA) cycle. Also, more metabolites with antioxidant functions were observed during desiccation; metabolites related to glutathione and tocopherol significantly increased (e.g. oxidized glutathione increased 100-fold and both β- and δ-tocopherol increased >30-fold) (Oliver et al., 2011a). Specific metabolite production upon desiccation is common in resurrection plants; the levels of verbascose and γ-aminobutyrate only significantly increased in the desiccated H. rhodopensis (Gechev et al., 2013). This difference in metabolite levels between dehydration and desiccation indicates that dehydration is a transition process of various metabolic pathways and the purpose of the transition is antioxidant production, nitrogen remobilization, ammonia detoxification, and soluble sugar production, which are critical for surviving desiccation. Compared with gene expression profiles and protein abundance, metabolite levels are shown to change in a uniform direction towards the desiccated state of plants. This may be determined by their functions as protective compounds to osmotic stress and as antioxidants. Sensing and signaling of water stress severity Many studies have revealed that abiotic stress sensing and signaling in plants are integrated in complex networks which involve hormones, Ca2+, ROS, sugars, etc. (Miller et al., 2010; Bose et al., 2011; Keunen et al., 2013; Choudhury et al., 2017). As discussed above, the difference between dehydration and desiccation is the severity of water stress, and the molecular responses vary with the water status of the plants. How is the severity of water stress sensed and which are the steps in signal transduction? Based on the available studies of resurrection plants, we focus mainly on the role of the plant hormone ABA and ROS in sensing and signaling between dehydration and desiccation. It is well known that the hormone ABA is produced rapidly in plants when water stress occurs (Shinozaki and Yamaguchi-Shinozaki, 1997; Osakabe et al., 2014). ABA also plays an important role in regulating plant responses to dehydration and in the acquisition of desiccation tolerance. The increase of ABA levels during dehydration in resurrection plants, such as C. plantagineum, M. fabellifolia, and X. humilis (Bartels et al., 1990; Schiller et al., 1997), indicates that this hormone participates in the development of desiccation tolerance. Desiccation tolerance in C. plantagineum callus requires a pre-treatment with ABA (Bartels, 2005), and the complete desiccation tolerance of P. patens filaments resulted from ABA incubation before dehydration. The deletion of the ABA-activating transcription factor ABI3 (ABSCISIC ACID INSENSITIVE 3) leads to the loss of desiccation tolerance of P. patens (Khandelwal et al., 2010), indicating that ABA-related processes have a central role in acquisition of desiccation tolerance. The transcriptome study in C. plantagineum revealed that the profile of abundant transcripts in the mildly dehydrated sample indicates predominant expression of proteins involved in ABA-mediated responses to water stress (Rodriguez et al., 2010). However, multiple mechanisms and several signaling pathways are involved in activating the dehydration response (Bartels, 2005). In the transcriptome of the woody resurrection plant M. flabellifolia during dehydration, the transcript levels of 53 transcription factors and 91 protein kinases increased rapidly and peaked early during dehydration. Among the signal cascades of molecular pathways that these regulators transduce, both ABA-dependent and ABA-independent drought stress pathways are included (Ma et al., 2015). An example of an ABA-independent signaling is phospholipase D (PLD) in C. plantagineum; PLD activity is induced within minutes by dehydration stress, but not by ABA (Frank et al., 2000). Stevenson et al. (2016) identified ABA-non-responsive mutants in P. patens and identified the ABA NON-RESPONSIVE (ANR) gene encoding a modular protein kinase. The anr mutants fail to accumulate dehydration tolerance-associated gene products in response to dehydration and do not acquire ABA-dependent desiccation tolerance. Despite the existence of ABA-independent signaling in the acquisition of desiccation tolerance, many studies appear to build up a correlation between ABA level and desiccation tolerance. The endogenous ABA level was determined in hydrated and dried leaves of C. plantagineum. After drying, the concentration increased 6-fold (Bartels et al., 1990). Similar increases in ABA content have been noted in Borya nitida (Gaff and Loveys, 1984), M. fabellifolia, X. humilis, and a large range of other resurrection plants (Schiller et al., 1997). The dynamic analysis of phytohormones in H. rhodopensis during desiccation showed that the ABA level reaches a maximum at 25% RWC, but it decreases when RWC becomes lower (Djilianov et al., 2013). In S. stapfianus, ABA reached the highest level in leaves at ~15% RWC and then started to decrease until the desiccated state. This demonstrates that acquisition of desiccation tolerance is closely related to high ABA levels, but the sensing and signaling for desiccation is not dependent on ABA. In addition to ABA, other hormones may also participate in the dehydration response and acquisition of desiccation tolerance. According to the study of Djilianov et al. (2013), the levels of salicylic acid (SA) in H. rhodopensis continuously increased with RWCs declining from 25% to 13%. This indicates that SA may play a role in desiccation sensing and signaling. Although the role of SA in desiccation tolerance is not known, studies from model plants and crops have demonstrated that SA participates in the signaling of various abiotic stresses (Horváth et al., 2007) and its accumulation enhances drought tolerance by interacting with ROS (Miura et al., 2013). Also zeatin and zeatin riboside accumulate to high levels in desiccated C. wilmsii leaves (Vicré et al., 2004). Possibly, the accumulation of cytokinins is necessary for the recovery of metabolism upon rehydration. Another explanation is that cytokinins also participate in the stress signaling of desiccation. Studies on model plants (e.g. Arabidopsis) reveal that plant hormones are involved in multiple processes and the crosstalk between different plant hormones produces synergetic or antagonic interactions, which are crucial to modulate responses to abiotic stress (Peleg and Blumwald, 2011). Future research should focus on the balance of various plant hormones to understand the signaling of dehydration or desiccation. As the accumulation of ROS is a general stress response that can be triggered by osmotic and ionic imbalance in water-stressed cells, the antioxidant response is also an important part of desiccation tolerance. In S. tamariscina, the activities of four antioxidant enzymes [superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and glutathione reductase (GR)] increased gradually during dehydration (Wang et al., 2010). Similarly, dehydration resulted in an increase in glutathione in S. stapfianus leaves, primarily late during the drying regime, to an ~100-fold higher amount in desiccated versus hydrated control tissue (Oliver et al., 2011a). As well as causing oxidative stress, ROS play an integral part as signaling molecules in the regulation of numerous biological processes such as growth, development, and responses to biotic and/or abiotic stimuli in plants (Baxter et al., 2014). Jovanović et al. (2011) demonstrated a critical phase (RWC decreases from 70% to 50%) for Ramonda nathaliae during which hydrogen peroxide accumulates and lipid peroxidation as well as ion leakage take place. They proposed that controlled elevation of ROS, such as hydrogen peroxide, could be an important mechanism for sensing dehydration and triggering an appropriate response program (Jovanović et al., 2011). Results obtained from traditional measurements are questionable, because they ignore the various sources of ROS (from disruptions in metabolic activity or produced for the purpose of signaling) and their subcellular localization. ROS can be produced in the apoplast, chloroplast, peroxisome, mitochondria, vacuole, cytosol, and nuclei (Suzuki et al., 2012). Each cellular ROS compartment has its own ROS homeostasis; the different ROS levels of various compartments form a particular ROS signature (Choudhury et al., 2017). The ROS signature will be affected by different abiotic stresses in plant cells; similarly, dehydration and desiccation may lead to differential ROS signatures. These signatures may create stress-specific signals for dehydration and desiccation, resulting in differential responses. Although it is reasonable to hypothesize a role for ROS in sensing and signaling the severity of water stress, studies with regard to ROS signature changes between dehydration and desiccation still need to be conducted. The connection between studies from resurrection plants and their application in crops To date, the major emphasis of biotechnological approaches for improving crop drought tolerance has been in engineering genes that encode compatible organic osmolytes, plant growth regulators, antioxidants, heat shock and late embryogenesis abundant proteins, and transcription factors involved in gene expression (Ashraf, 2010). Therefore, the comparison between responses to dehydration and desiccation provides insights into improving crop drought tolerance just from these above aspects. Although many transgenic lines which show improved growth under water-limiting conditions have been identified under controlled environments, the development of drought-tolerant crops is still some distance away (Deikman et al., 2012). Compared with crops that show tolerance to drought, desiccation-tolerant plants exhibit extreme tolerance. Therefore, mechanisms in place in desiccation-tolerant plants may provide better cellular protection in crop plants (Fig. 3). First, there are substantial species-specific genes related to dehydration or desiccation tolerance in resurrection plants (Giarola et al., 2017) which may be candidates for transgenes to be tested. Secondly, key genes encoding proteins or metabolites related to acquisition of desiccation tolerance could be candidates. For example, the genes involved in synthesis of SA or zeatin that are correlated to desiccation could be considered to be tested. As some resurrection plants share relatively high similarity in genome architecture with important staple crops, such as O. thomaeum and Oryza or Sorghum (VanBuren et al., 2015), the regulating networks of stress could be important for water stress tolerance, So transcription factors as well as components of the signal transduction pathways that co-ordinate expression of downstream regulons are thought to be optimal targets for engineering of complex traits, such as drought tolerance (Wang et al., 2003). The comparison between dehydration and desiccation help to reveal important TFs in acquisition of desiccation tolerance such as the bHLH, MYB, and WRKY families in M. flabellifolia (Ma et al., 2015). Fig. 3. View largeDownload slide A scheme to explain the benefits of resurrection plants for improving crop drought tolerance. The mechanism to tolerate extreme water stress is the key point to enhance or extend water stress tolerance in crops. Fig. 3. View largeDownload slide A scheme to explain the benefits of resurrection plants for improving crop drought tolerance. The mechanism to tolerate extreme water stress is the key point to enhance or extend water stress tolerance in crops. Concluding remarks Dehydration and desiccation are defined in this review by the water status of plants. This allowed us to compare plant responses to dehydration and desiccation. By analyzing plant performance in terms of main physiological activities, accumulation of protective compounds, synthesis of key hormones, and establishment of antioxidant systems, we propose 30–40% RWC as the boundary between dehydration and desiccation. Research has revealed that desiccation-tolerant plants have similar water loss rates during dehydration to desiccation-sensitive plants. Although dehydration and desiccation can be categorized as moderate and severe water stress, respectively, experiments revealed that the response to dehydration and the acquisition of desiccation tolerance in resurrection plants are based on additional factors, not only on the severity of water stress. To carry out a comparative molecular analysis between dehydration and desiccation, we classified seven main performance types of gene expression, protein accumulation, or metabolite levels during dehydration (Fig. 2). Although a clear distinction between dehydration and desiccation is not pointed out, the comparative analysis suggests that the molecular responses to dehydration tend to be involved in damage repair and adjustments in cellular structure and in physiological metabolism, while those to desiccation preferentially protect cellular structures and prepare cells for recovery. Specific sensing and signaling may exist for dehydration and desiccation, respectively. 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For permissions, please email: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Experimental Botany Oxford University Press

Molecular responses to dehydration and desiccation in desiccation-tolerant angiosperm plants

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Oxford University Press
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© The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com
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0022-0957
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1460-2431
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10.1093/jxb/erx489
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Abstract

Abstract Due to the ability to tolerate extreme dehydration, desiccation-tolerant plants have been widely investigated to find potential approaches for improving water use efficiency or developing new crop varieties. The studies of desiccation-tolerant plants have identified sugar accumulation, specific protein synthesis, cell structure changes, and increased anti-oxidative reactions as part of the mechanisms of desiccation tolerance. However, plants respond differently according to the severity of water loss, and the process of water loss affects desiccation tolerance. A detailed analysis within the dehydration process is important for understanding the process of desiccation tolerance. This review defines dehydration and desiccation, finds the boundary for the relative water content between dehydration and desiccation, compares the molecular responses to dehydration and desiccation, compares signaling differences between dehydration and desiccation, and finally summarizes the strategies launched in desiccation-tolerant plants for dehydration and desiccation, respectively. The roles of abscisic acid (ABA) and reactive oxygen species (ROS) in sensing and signaling during dehydration are discussed. We outline how this knowledge can be exploited to generate drought-tolerant crop plants. ABA, dehydration, desiccation, desiccation tolerance, molecular responses, ROS, stress signaling Introduction Water stress often affects growth and development of crop plants and leads to substantial loss in food production. How to improve water stress tolerance in plants is a core question in agricultural activities. In nature, there are some plants that can tolerate >90% water loss and resume physiological activities within hours after regaining water supply (Alpert, 2006). These plants are grouped as ‘resurrection plants’ and their ability to tolerate nearly complete drying is called ‘desiccation tolerance’ (Jenks and Wood, 2008; Lüttge et al., 2011). The studies of resurrection plants may provide approaches for developing new crop varieties and designing new water management strategies in crop production. To date, research has demonstrated that the mechanism of plant desiccation tolerance is closely related to the accumulation of sugars (e.g. sucrose), the large-scale synthesis of specific proteins (e.g. late embryogenesis abundant proteins), and the adaptive adjustment of cell structures (e.g. cell wall) (Hoekstra et al., 2001; Moore et al., 2009). A few resurrection plant species including Physcomitrella patens (Cove et al., 2006), Craterostigma plantagineum (Bartels and Salamini, 2001), Boea hygrometrica (Mitra et al., 2013), Xerophyta viscosa (Farrant et al., 2015), and Sporobolus stapfianus (Gaff et al., 2009) have been substantially investigated so that they are becoming potential model plants. In recent years, increasing systematic data from transcriptomes, proteomes, and metabolomes are facilitating our understanding of plant desiccation tolerance (Gechev et al., 2012; Giarola et al., 2017). The availability of genome sequences makes some plants suitable as model plants among resurrection plants, such as P. patens (Rensing et al., 2008) B. hygrometrica (Xiao et al., 2015), Oropetium thomaeum (VanBuren et al., 2015), and X. viscosa (Costa et al., 2017). Most studies focus on comparing well-watered plants with desiccated plants and rehydrated plants to reveal important factors affecting plant desiccation tolerance. A comparison between moderate dehydration and complete dehydration (desiccation) has hardly been addressed. To understand mechanisms underlying desiccation, the recognition of changes in terms of water stress sensing and transition of metabolic reactions during mild to moderate and complete dehydration is necessary. For example, in the transcriptome analysis of Myrothamnus flabellifolia, a total of 8287 differentially transcribed genes (DTGs) were detected during dehydration, but only 204 DTGs were up-regulated and 547 DTGs were down-regulated during all different dehydration stages [90, 75, and 27% relative water contents (RWCs)] (Ma et al., 2015). This raises the question: what are the roles of the DTGs up-regulated or down-regulated from slight to moderate or from moderate to complete dehydration? Another example is the proteome analysis of X. viscosa, which identified a number of dehydration-responsive proteins. These proteins were grouped into three classes based on their expression patterns: early dehydration-responsive (significant change only at 65% RWC), late dehydration-responsive (significant change only at RWC 35%), and full dehydration-responsive (with altered levels of expression at both 65% and 35% RWC) (Ingle et al., 2007). This shows that differential responses exist at early and late stages of dehydration. Similarly, non-resurrection plants, such as Arabidopsis thaliana or Sorghum bicolor, respond with different gene expression programs to mild and severe dehydration (Buchanan et al., 2005; Denby and Gehring, 2005). This difference is also reflected on the metabolite level. Using untargeted global metabolomics analysis, Oliver et al. (2011a) revealed that the levels of glucose, fructose, and galactinol declined in S. stapfianus only at RWCs from 80% to 40%, and the levels of alanine and aspartate only significantly decreased at 50% RWC. Because of the importance of understanding the differences of plant responses between dehydration and desiccation, this review summarizes the advance of studies on model or non-resurrection plants. New hypotheses are proposed on plant response mechanisms to dehydration and desiccation. Drought, dehydration, and desiccation When water stress is mentioned, ‘drought, dehydration, or desiccation’ are used to describe the stressed status of plants. A clear distinction between drought, dehydration, and desiccation is the first step for a comparative analysis in terms of morphological, physiological, and molecular responses. Early in 1973, Hsiao tried to classify the plant water status into ‘hydrated, mild stress, moderate stress, severe stress, and desiccation’ according to the severity of stress (Hsiao, 1973; for details see Table 1). However, this classification of the water status does not describe the differences between drought, dehydration, and desiccation correctly, because not only is the amount of water loss important, but the rate of dehydration and the duration of the stress also determine responses to water deficit (Bray, 1997). As ‘drought’ is closely related to agricultural production, it is often used to describe water deficit, even in some experimental studies regarding resurrection plants, such as the studies by Cui et al., (2012) or Gechev et al. (2013). According to Huang et al., (2010), Levitt (1985), and Talamè et al. (2007), we propose the following definitions: (i) drought is a slow process during which transpiration exceeds water uptake in plants that mainly grow in soil; (ii) dehydration implies that whole plants or detached organs encounter a steady water loss and are often kept in air to lose water; and (iii) desiccation is the final result of dehydration and the water status is equilibrated with the air (desiccated is equal to extremely dehydrated). This review focuses on comparing plant responses to dehydration and desiccation. Table 1. Plant water status under various stress conditions Water status  Water potential (Ψ)  Relative water contents  Hydrated  0 bar  80–100%a  Mild stress  5–10 bars lower  8–10% lower  Moderate stress  12–15 bars lower  10–20% lower  Severe stress  >15 bars lower  >20% lower  Desiccation  >35 bars lowerb  >50% lower  Water status  Water potential (Ψ)  Relative water contents  Hydrated  0 bar  80–100%a  Mild stress  5–10 bars lower  8–10% lower  Moderate stress  12–15 bars lower  10–20% lower  Severe stress  >15 bars lower  >20% lower  Desiccation  >35 bars lowerb  >50% lower  The data are cited from Hsiao (1973). a Data obtained from Farrant et al. (2015), Ingram et al. (1997), Jiang et al. (2007), Mladenov et al. (2015), Oliver et al. (2011a), and Cui et al. (2012). b Data obtained from Boyer (1976). View Large Table 1. Plant water status under various stress conditions Water status  Water potential (Ψ)  Relative water contents  Hydrated  0 bar  80–100%a  Mild stress  5–10 bars lower  8–10% lower  Moderate stress  12–15 bars lower  10–20% lower  Severe stress  >15 bars lower  >20% lower  Desiccation  >35 bars lowerb  >50% lower  Water status  Water potential (Ψ)  Relative water contents  Hydrated  0 bar  80–100%a  Mild stress  5–10 bars lower  8–10% lower  Moderate stress  12–15 bars lower  10–20% lower  Severe stress  >15 bars lower  >20% lower  Desiccation  >35 bars lowerb  >50% lower  The data are cited from Hsiao (1973). a Data obtained from Farrant et al. (2015), Ingram et al. (1997), Jiang et al. (2007), Mladenov et al. (2015), Oliver et al. (2011a), and Cui et al. (2012). b Data obtained from Boyer (1976). View Large Water loss in resurrection plants Resurrection plants possess desiccation tolerance; does this mean that they have better resistance mechanisms to water loss than non-desiccation-tolerant plants? Several studies have provided answers to this question. Schwab et al. (1989) found that the rate of water loss during dehydration of detached leaves of the resurrection plant C. plantagineum was comparable with or even faster than that of the mesophyte spinach under identical conditions. By comparing the resurrection plant B. hygrometrica with its desiccation-sensitive relative Chirita heterotrichia, Deng et al. (2003) also observed that leaves of B. hygrometrica lost water during dehydration more rapidly than C. heterotrichia. Similarly, the water loss in the detached leaves of Haberlea rhodopensis (desiccation tolerant) was faster than in those of spinach (desiccation sensitive) (Georgieva et al., 2005). However, not all research results are consistent. For instance, the desiccation-tolerant S. stapfianus exhibited a similar drying curve to the desiccation-sensitive S. pyramidalis (Oliver et al., 2011a). The desiccation-tolerant Selaginella lepidophylla exhibited a lower rate of water loss than the desiccation-sensitive Selaginella moellendorffii (Yobi et al., 2012). From these contrasting results, it can be concluded that the rate of limiting water loss is not a necessary part of the desiccation tolerance mechanism for all resurrection plants. Response of resurrection plants to water loss and the boundary between dehydration and desiccation Understanding physiological changes during the complete process from the hydrated state to the desiccated state is the first step for a comparison between dehydration and rehydration. From the studies of P. patens (Cui et al., 2012), S. lepidophylla (Yobi et al., 2013), X. viscosa (Farrant et al., 2015), C. plantagineum (Ingram et al., 1997), S. stapfianus (Oliver et al., 2011a), and H. rhodopensis (Mladenov et al., 2015), it can be concluded that the RWCs in resurrection plants decrease in a nearly linear fashion when water is withheld. Thus it is difficult to define a precise boundary between dehydration and desiccation using RWC as the indicator. However, physiological and molecular responses differ at various degrees of water loss (Fig. 1), and the comparison of the changes provides a clue as to how to distinguish dehydration and desiccation. The distinction of dehydration and desiccation responses is helpful in understanding acquisition of desiccation tolerance. Generally, actively growing plants have an RWC of 85–100% (Gaff and Oliver, 2013). When plants are dehydrated, a series of physiological activities, such as photosynthesis and respiration, are rearranged. By summarizing the physiological performance of various desiccation-tolerant resurrection plants (Table 2), a boundary is found to distinguish dehydration and desiccation. This boundary can be defined when using RWCs to mark the water status. The data show that an RWC of ~40% is the transition from dehydration to desiccation. The changes of gene expression, protein abundance, and metabolite levels also reflect this transition. In S. stapfianus, drought-related genes (SDG2i, SDG3i, and SDG4i) are expressed at the highest levels when the RWC decreased to 39–20% (Le et al., 2007). Kuang et al. (1995) studied protein synthesis in vivo of S. stapfianus leaves during dehydration. Two main phases were distinguished according to extensive changes of in vivo proteins in S. stapfianus leaves. In the first phase (85–51% RWC), 10 novel proteins appeared and two proteins increased in abundance. In the second phase (37–3.5% RWC), 15 novel proteins appeared and two proteins increased in abundance. Through proteome analysis, Ingle et al. (2007) also proposed that the induction of putative ‘late’ protection mechanisms during dehydration is initiated at ~40% RWC in X. viscosa. In contrast to gene expression and protein synthesis, the response on the metabolite levels is delayed. Oliver et al. (2011a) studied the metabolomes of S. stapfianus at various RWCs during dehydration. The result showed that at 20% RWC, the levels of ~75% of the metabolites displayed an increased abundance during dehydration and reached the same levels as those in the desiccated tissue, especially for sucrose, raffinose family oligosaccharides, and tocopherol. Table 2. Physiological performance of some resurrection plants at specific relative water contents Plant species  RWC   Physiological performance during dehydration   References   Xerophyta scabrida  35%  Stomatal conductance reaches minimum and photosynthesis ceases  Tuba et al. (1996)  Craterostigma wilmsii, M. flabellifolius, Xerophyta humilis, and S. stapfianus  40%  Photosynthesis stops  Schwab et al. (1989); Whittaker et al. (2007); Farrant (2000);Beckett et al. (2012)  M. flabellifolius and Xerophyta humilis  40%  Respiration rate starts to decrease  Farrant (2000)  Craterostigma wilmsii and Craterostigma plantagineum  30%  Respiration rate starts to decrease  Schwab et al. (1989); Farrant (2000)  Craterostigma wilmsii, M. flabellifolius, and Xerophyta humilis  40%  Chlorophyll degradation stops  Farrant (2000); Beckett et al. (2012)  Craterostigma wilmsii, M. flabellifolius, and Xerophyta humilis  40%  Carotenoid degradation and anthocyanin accumulation stop  Farrant (2000)  Xerophyta viscosa  50%  Sucrose and raffinose family oligosaccharides accumulate to the maximum levels  Whittaker et al. (2001),Peters et al. (2007)  S. stapfianus  30%  Sucrose contents become maximal  Whittaker et al. (2001)  C. wilmsii, X. humilis, and X. viscosa  40%  Sucrose accumulation peaks  Farrant et al. (2007)  Ramonda serbica  35%  Total phenolic acid levels decreased to the levels as desiccated status  Sgherri et al. (2004)  M. flabellifolius and X. humilis  40%  The activities of glutathione reductase and superoxide dismutase reached maximum  Farrant (2000)  Tortula ruralis  30%  The percentage of oxidized glutathione (GSH) in the total GSH pool becomes maximal  Smirnoff (1993)  Haberlea rhodopensis  25%  The contents of ABA and cytokinins in leaves reach the maximum  Djilianov et al. (2013)  Selaginella tamariscina  20%  ABA reaches its maximum level  Wang et al. (2010)  Plant species  RWC   Physiological performance during dehydration   References   Xerophyta scabrida  35%  Stomatal conductance reaches minimum and photosynthesis ceases  Tuba et al. (1996)  Craterostigma wilmsii, M. flabellifolius, Xerophyta humilis, and S. stapfianus  40%  Photosynthesis stops  Schwab et al. (1989); Whittaker et al. (2007); Farrant (2000);Beckett et al. (2012)  M. flabellifolius and Xerophyta humilis  40%  Respiration rate starts to decrease  Farrant (2000)  Craterostigma wilmsii and Craterostigma plantagineum  30%  Respiration rate starts to decrease  Schwab et al. (1989); Farrant (2000)  Craterostigma wilmsii, M. flabellifolius, and Xerophyta humilis  40%  Chlorophyll degradation stops  Farrant (2000); Beckett et al. (2012)  Craterostigma wilmsii, M. flabellifolius, and Xerophyta humilis  40%  Carotenoid degradation and anthocyanin accumulation stop  Farrant (2000)  Xerophyta viscosa  50%  Sucrose and raffinose family oligosaccharides accumulate to the maximum levels  Whittaker et al. (2001),Peters et al. (2007)  S. stapfianus  30%  Sucrose contents become maximal  Whittaker et al. (2001)  C. wilmsii, X. humilis, and X. viscosa  40%  Sucrose accumulation peaks  Farrant et al. (2007)  Ramonda serbica  35%  Total phenolic acid levels decreased to the levels as desiccated status  Sgherri et al. (2004)  M. flabellifolius and X. humilis  40%  The activities of glutathione reductase and superoxide dismutase reached maximum  Farrant (2000)  Tortula ruralis  30%  The percentage of oxidized glutathione (GSH) in the total GSH pool becomes maximal  Smirnoff (1993)  Haberlea rhodopensis  25%  The contents of ABA and cytokinins in leaves reach the maximum  Djilianov et al. (2013)  Selaginella tamariscina  20%  ABA reaches its maximum level  Wang et al. (2010)  View Large Table 2. Physiological performance of some resurrection plants at specific relative water contents Plant species  RWC   Physiological performance during dehydration   References   Xerophyta scabrida  35%  Stomatal conductance reaches minimum and photosynthesis ceases  Tuba et al. (1996)  Craterostigma wilmsii, M. flabellifolius, Xerophyta humilis, and S. stapfianus  40%  Photosynthesis stops  Schwab et al. (1989); Whittaker et al. (2007); Farrant (2000);Beckett et al. (2012)  M. flabellifolius and Xerophyta humilis  40%  Respiration rate starts to decrease  Farrant (2000)  Craterostigma wilmsii and Craterostigma plantagineum  30%  Respiration rate starts to decrease  Schwab et al. (1989); Farrant (2000)  Craterostigma wilmsii, M. flabellifolius, and Xerophyta humilis  40%  Chlorophyll degradation stops  Farrant (2000); Beckett et al. (2012)  Craterostigma wilmsii, M. flabellifolius, and Xerophyta humilis  40%  Carotenoid degradation and anthocyanin accumulation stop  Farrant (2000)  Xerophyta viscosa  50%  Sucrose and raffinose family oligosaccharides accumulate to the maximum levels  Whittaker et al. (2001),Peters et al. (2007)  S. stapfianus  30%  Sucrose contents become maximal  Whittaker et al. (2001)  C. wilmsii, X. humilis, and X. viscosa  40%  Sucrose accumulation peaks  Farrant et al. (2007)  Ramonda serbica  35%  Total phenolic acid levels decreased to the levels as desiccated status  Sgherri et al. (2004)  M. flabellifolius and X. humilis  40%  The activities of glutathione reductase and superoxide dismutase reached maximum  Farrant (2000)  Tortula ruralis  30%  The percentage of oxidized glutathione (GSH) in the total GSH pool becomes maximal  Smirnoff (1993)  Haberlea rhodopensis  25%  The contents of ABA and cytokinins in leaves reach the maximum  Djilianov et al. (2013)  Selaginella tamariscina  20%  ABA reaches its maximum level  Wang et al. (2010)  Plant species  RWC   Physiological performance during dehydration   References   Xerophyta scabrida  35%  Stomatal conductance reaches minimum and photosynthesis ceases  Tuba et al. (1996)  Craterostigma wilmsii, M. flabellifolius, Xerophyta humilis, and S. stapfianus  40%  Photosynthesis stops  Schwab et al. (1989); Whittaker et al. (2007); Farrant (2000);Beckett et al. (2012)  M. flabellifolius and Xerophyta humilis  40%  Respiration rate starts to decrease  Farrant (2000)  Craterostigma wilmsii and Craterostigma plantagineum  30%  Respiration rate starts to decrease  Schwab et al. (1989); Farrant (2000)  Craterostigma wilmsii, M. flabellifolius, and Xerophyta humilis  40%  Chlorophyll degradation stops  Farrant (2000); Beckett et al. (2012)  Craterostigma wilmsii, M. flabellifolius, and Xerophyta humilis  40%  Carotenoid degradation and anthocyanin accumulation stop  Farrant (2000)  Xerophyta viscosa  50%  Sucrose and raffinose family oligosaccharides accumulate to the maximum levels  Whittaker et al. (2001),Peters et al. (2007)  S. stapfianus  30%  Sucrose contents become maximal  Whittaker et al. (2001)  C. wilmsii, X. humilis, and X. viscosa  40%  Sucrose accumulation peaks  Farrant et al. (2007)  Ramonda serbica  35%  Total phenolic acid levels decreased to the levels as desiccated status  Sgherri et al. (2004)  M. flabellifolius and X. humilis  40%  The activities of glutathione reductase and superoxide dismutase reached maximum  Farrant (2000)  Tortula ruralis  30%  The percentage of oxidized glutathione (GSH) in the total GSH pool becomes maximal  Smirnoff (1993)  Haberlea rhodopensis  25%  The contents of ABA and cytokinins in leaves reach the maximum  Djilianov et al. (2013)  Selaginella tamariscina  20%  ABA reaches its maximum level  Wang et al. (2010)  View Large Fig. 1. View largeDownload slide A scheme of plant responses to water loss during dehydration and the definition of the boundary between dehydration and desiccation. The severity of water loss is sensed. Together with other signaling, such as light and energy, the plant response strategy is decided. The boundary between dehydration and desiccation is defined based on the differential physiological and molecular changes. Fig. 1. View largeDownload slide A scheme of plant responses to water loss during dehydration and the definition of the boundary between dehydration and desiccation. The severity of water loss is sensed. Together with other signaling, such as light and energy, the plant response strategy is decided. The boundary between dehydration and desiccation is defined based on the differential physiological and molecular changes. The launch of desiccation tolerance mechanisms does not occur in desiccated tissues but starts earlier and often correlates with the transition from dehydration and desiccation. Generally, the water contents of air-dry desiccation-tolerant plants in the field are only at 5–13% RWC (Gaff, 1977). Various studies revealed that physiological and molecular responses present in the desiccated state have already been initiated when plants possess RWCs of ~40%. The proteome analysis by Oliver et al. (2011b) showed that when the leaves of S. stapfianus reached an RWC of 30%, the components critical for cellular protection are already present. Whittaker et al. (2004) and Martinelli et al. (2007a) observed that in the dehydration process of S. stapfianus from 35% RWC to dryness at 5% RWC, the leaf cells immediately begin to lose water and the protective metabolites start to accumulate with a significantly higher speed. This indicates that resurrection plants finish the preparation for staying in a quiescent state in terms of gene expression, protein synthesis, and metabolite production before being completely dry. Taking these observations into account, it is proposed that the boundary between dehydration and desiccation can be set at 30–40% RWC. Water loss and acquisition of desiccation tolerance: the dehydration process determines desiccation tolerance Acquisition of desiccation tolerance in resurrection plants is characterized by specific conditions. Many resurrection plants can survive desiccation only if the drying rate is slow (Bewley, 1997). For example, protonema of Funaria hygrometrica (moss) tolerate slow dehydration but not rapid dehydration (Werner et al., 1991), and dehydration in the perennial resurrection grass S. stapfianus must proceed slowly over a period of ≥7 d (Griffiths et al., 2014), indicating that sufficient dehydration time is required to change to a gene expression profile which enables recovery following rehydration. Specific conditions are also essential to activate the survival program. The resurrection plant B. hygrometrica requires a period of acclimation by slow soil-drying to survive a subsequent period of rapid desiccation in air (Zhu et al., 2015). Protonema of the moss P. patens are tolerant only to moderate water stress (about –13 MPa by water potential), but not to complete desiccation in experimental conditions (Koster et al., 2010). Interestingly, abscisic acid (ABA) pre-treatment can lead to the tolerance of P. patens to complete desiccation (–273 MPa) (Khandelwal et al., 2010; Koster et al., 2010). Detached leaves of S. stapfianus with >60% RWC are desiccation sensitive, indicating that desiccation tolerance is conferred to vegetative tissue of S. stapfianus when the leaf RWC has declined to <60% (Griffiths et al., 2014). Other factors (e.g. nutrient status) also affect plant desiccation tolerance. Martinelli et al. (2007b) showed that older leaves of the resurrection plant S. stapfianus were desiccation sensitive whereas younger leaves were desiccation tolerant. Zhang and Bartels (2016) demonstrated that leaves of C. plantagineum starved in dark conditions lose desiccation tolerance. Farrant et al. (2003) found that drying in the dark results in loss of viability in Craterostigma wilmsii and Myrothamnus flabellifolius, and the chemical protection (anthocyanin content and antioxidant activity) appears to be regulated by light in M. flabellifolius. These examples demonstrate that the establishment of a response strategy is based on various factors, not only on the severity of water loss (Fig.1). Although it is not known how light and nutrition affect desiccation tolerance in resurrection plants, previous studies have shown that there is a link between the response to light and drought tolerance because ABA signaling participates in the common step of both response pathways (Galvezvaldivieso et al., 2009; Rossel et al., 2006). Stress and energy signaling are closely linked and they might be regulated by the evolutionarily conserved energy sensor protein kinases (Baenagonzález et al., 2007; Baenagonzález and Sheen, 2008). Based on these points, it is hypothesized that light and nutrition affect desiccation tolerance acquisition via similar ways. Comparative analysis between dehydration and desiccation To compare the different responses between dehydration and desiccation, a full understanding is necessary of the cellular and molecular transition from dehydration to desiccation (or from high RWC to lower RWC) in terms of gene expression, protein synthesis and degradation, and related metabolite changes. Many transcriptome, proteome, and metabolome studies of resurrection plants such as P. patens (Cui et al., 2012), C. plantagineum (Rodriguez et al., 2010), B. hygrometrica (Zhu et al., 2015), S. stapfianus (Oliver et al., 2011a), and X. viscosa (Ingle et al., 2007) investigated the changes of gene transcripts, protein abundance, and metabolite levels at various RWCs (from high to low) (Giarola et al., 2017). By analyzing the data from these studies, the performance of gene transcript level, protein abundance, or metabolite level from higher RWCs to lower RWCs can be classified into seven performance types (Fig. 2). Among them, type 1 does not change the performance at various RWCs during dehydration, such as the EF1a gene and GAPDH gene in C. plantagineum (Giarola et al., 2015) and the alanine and aspartate contents in H. rhodopensis (Mladenov et al., 2015). Type 2 and type 3 respond positively or negatively to dehydration, and the response intensity increases with degree of dehydration. Representatives of type 2 are late embryogenesis-like proteins (Rodriguez et al., 2010) or aldehyde dehydrogenases (Kirch et al., 2001) in C. plantagineum. Examples of type 3 are the large subunit of Rubisco in B. hygrometrica (Jiang et al., 2007) and the starch content in S. stapfianus (Whittaker et al., 2007). There are two types (type 4 and type 5) that first respond positively or negatively to dehydration and then recover to the initial level. Type 4 is exemplified by Rubisco activase in S. tamariscina (Wang et al., 2010) and fructose and galactinol in S. stapfianus (Oliver et al., 2011a), while type 5 is represented by the heat shock protein 70 (HSP 70) in S. tamariscina (Wang et al., 2010) and aspartate and pyruvate in S. stapfianus (Oliver et al., 2011a). Type 6 is completely inhibited by dehydration and thus is not present in the desiccated state. Two examples of type 6 are glutamine synthetase in S. tamariscina (Wang et al., 2010) and arginine and linolenate in S. stapfianus (Oliver et al., 2011a). In contrast, type 7 is specifically responsive to desiccation, and examples are citrate and 1-palmitoylglycerophosphocholine in S. stapfianus (Oliver et al., 2011a). It is difficult to place all reactions of a physiological process into a specific performance type. For instance, most proteins involved in photosynthesis (e.g. Rubisco) decline in abundance, but certain proteins (e.g. chloroplastic aldolase) accumulated. However, the methodology using performance types provides a good basis to understand the difference between dehydration and desiccation. Within these performance types, type 4 and type 7 show positive responses to dehydration and desiccation, respectively, thus providing an excellent starting point for comparative analysis. Comparison of gene expression between dehydration and desiccation In the transcriptome analysis of C. plantagineum, the 500 most variable transcripts were analyzed and they were divided into six clusters according to their expression signatures under hydrated (95% RWC), dehydrated (80% RWC), desiccated (5% RWC), and rehydrated (90% RWC) conditions (Rodriguez et al., 2010). These clusters can be correlated with the performance types depicted in Fig. 2. Type 4 corresponds to cluster II that includes the 112 most abundant transcripts exclusively present in the early dehydrated sample and type 7 corresponds to cluster III that contains the 88 most abundant transcripts in the desiccated sample. The profile of abundant transcripts in the early dehydrated sample indicates predominant expression of proteins involved in ABA-mediated responses to water stress and general abiotic and biotic stresses including ion homeostasis-related proteins. Cluster II mainly represents transcripts related to thiamine metabolism, which is proposed to function in response to abiotic and biotic stress in plants (Goyer, 2010), for example protecting plants from oxidative stress (Tunc-Ozdemir et al., 2009). Desiccated samples (cluster III) were characterized by a predominance of transcripts involved in tryptophan metabolism, as well as in processes related to the metabolism of indole derivatives. These biological functions may be involved in the salvage of precursors for the metabolism of proteins and nucleic acids in the desiccated, quiescent stage. In the transcriptome of the woody resurrection plant M. flabellifolia (Ma et al., 2015), the DTGs were mapped into the Kyoto Encyclopedia of Genes and Genomes (KEGG) database. Results showed that, except for the enriched pathways of DTGs due to dehydration and desiccation (biosynthesis of secondary metabolites, photosynthesis, nitrogen metabolism, glutathione metabolism, carbon fixation in photosynthetic organisms, terpenoid backbone synthesis, and flavonoid biosynthesis), enriched pathways of DTGs during early dehydration (90% water retention) include starch and sucrose metabolism, phagosome, fatty acid synthesis, phenylalanine metabolism, and linoleic acid metabolism. Enriched pathways of DTGs during moderate dehydration (75% water retention) involve fructose and mannose metabolism, pentose phosphate pathways, porphyrin and chlorophyll metabolism, and alanine, aspartate, and glutamate metabolism. In contrast, those pathways specifically include phenylalanine, tyrosine, and tryptophan biosynthesis in desiccated tissues (27% water retention). Altogether, the different gene expression patterns indicate that dehydration mainly leads to reactions to prevent or repair cellular damage and adjustment of physiological metabolism, while desiccation tends to conserve structures and prepare for the recovery process. Fig. 2. View largeDownload slide Scheme of performance types for gene transcript level, protein abundance, and metabolite level during dehydration. By comparing the performance of gene transcript level, protein abundance, or metabolite level before and after the boundary of dehydration and desiccation (~40% RWC), seven performance types are summarized (type 1–type 7). Fig. 2. View largeDownload slide Scheme of performance types for gene transcript level, protein abundance, and metabolite level during dehydration. By comparing the performance of gene transcript level, protein abundance, or metabolite level before and after the boundary of dehydration and desiccation (~40% RWC), seven performance types are summarized (type 1–type 7). Comparison of protein accumulation in dehydration and desiccation Protein abundance during dehydration suggests that programmed regulation of protein expression is triggered by changes of the water status. Thirty-five percent of the analyzed proteins in the B. hygrometrica proteome were transiently induced during dehydration with different kinetics and consequently represent proteins that function at specific stages during the program that leads to dehydration tolerance. Among these 78 proteins, 30 proteins were induced by dehydration within 0.5 h (RWC 79%). These included a putative ABC transporter ATPase, glutathione peroxidase, and polyphenol oxidase. The appearance of new proteins in early dehydration may be due to rapid de novo synthesis or post-translational processing of pre-existing proteins that are modified when the dehydration signal is perceived. Accumulation of 36 proteins and 12 proteins of the dehydration-responsive proteins was initiated by dehydration after 8 h (RWC 6.7%) and after 48 h (RWC 2.4%), respectively. Proteins in this group included the Rubisco large subunit (LSU), the oxygen-evolving complex (OEC) of PSII, vacuolar H+-ATPase A subunit, and glutathione S-transferase. These proteins may be transcribed and translated in response to the initial dehydration signal. The existence of distinct expression profiles suggests that different sets of proteins are programmed to function in protection against dehydration (Jiang et al., 2007). In the proteome analysis of X. viscosa, the proteins which were increased and decreased by dehydration and the de novo synthesized proteins (54 in total) were divided into three groups based on their expression patterns. Eight proteins were early dehydration responsive (significant change at 65% RWC), suggesting a possible role during the initial stages of drying, while 24 were late dehydration responsive (change at 35% RWC), perhaps indicating a role in the late stages of drying (Ingle et al., 2007). Within the 54 proteins, 17 proteins were identified and, among them, two components of the luminal OEC of PSII (psbO and psbP), the α-subunit of the F-ATPase, transketalose, ascorbate peroxidase, and glutamate:glyoxylate aminotransferase I decreased in abundance at 35% RWC compared with at 65% RWC. In contrast, the abundance of alcohol dehydrogenase and 2-Cys peroxiredoxin became higher at 35% RWC; RNA-binding proteins and desiccation-related proteins were de novo synthesized only at 35% RWC. Wang et al. (2010) investigated the differentially expressed proteins in S. tamariscina under dehydration. A total of 138 proteins were identified, which showed at least a 1.5-fold change in abundance under dehydration and rehydration conditions. By hierarchical clustering, two main clusters (cluster I and cluster II) were formed. Cluster I included 24 proteins whose abundances increased upon dehydration, while cluster II contained 114 down-regulated proteins. In cluster II, the abundance of 23 proteins (sub-cluster I) was up-regulated 1 d after dehydration 1 (49% water content) and then down-regulated 3 d after dehydration (19% water content), and the abundance of 10 proteins (sub-cluster II) was up-regulated 5 d after dehydration (11% water content) and down-regulated at other stages. The comparison between sub-cluster I and sub-cluster II provides the possibility to distinguish dehydration and desiccation. Sub-cluster I includes Rubisco LSU, 6-phosphogluconate dehydrogenase, transketolase, enolase, methionine synthase, eukaryotic initiation factor 4A, leucine aminopeptidase, V-type proton ATPase subunit B1, putative centromere protein containing the RecF/RecN/SMC N-terminal domain, and GC3/GDAP1 (grip-related ARF-binding domain), while sub-cluster II includes high chlorophyll fluorescence 136 (HCF136), chloroplast precursor of phosphoribulokinase (PRK), electron carrier/iron–sulfur cluster binding, NBS-LRR resistance-like protein J71, and putative FtsH protease. This demonstrates that cellular changes of various aspects occur and include photosynthesis, carbohydrate metabolism, protein synthesis and degradation, and membrane transport, as well as cell division and differentiation. In contrast, the response to desiccation includes cellular proteins and stress defense; for example, the HCF136 protein is essential for assembly of PSII (Plücken et al., 2002) and FtsH contributes to maintain membrane protein stability (Ito and Akiyama, 2005). Although both dehydration and desiccation lead to increased abundance of proteins protecting cellular structure and defending against antioxidative stress, dehydration results in adjustments of various metabolic pathways while the response to desiccation contains some activities to prepare for new ‘life’ after dehydration. For instance, during dehydration of P. patens, the synthesis of proteins associated with photosynthesis and photorespiration is down-regulated and the synthesis of proteins associated with reactive oxygen species (ROS) signaling increases; in contrast, HSPs accumulate in desiccated plants to preserve protein function upon rehydration (Wang et al., 2009; Cui et al. 2012). Comparison of metabolite levels between dehydration and desiccation During early stages of dehydration (60% and 50% RWC), leaves of S. stapfianus displayed an increased abundance of many amino acids, carbohydrates, and antioxidants; for example, the amino acids glycine, isoleucine, leucine, proline, tryptophan, tyrosine, and valine all increased between 2- and 5-fold. Sugars such as fructose, galactose, glucose, maltose, raffinose, sophorose, and sucrose increased between 1.8-fold and >18-fold. As a strong cellular antioxidant, β-tocopherol increased >3-fold (Oliver et al., 2011a). Compared with dehydration, the stage near desiccation and desiccation itself resulted in a change of over half (89 of 167 metabolites) of the metabolome. More amino acid and carbohydrate species accumulated, such as α-ketoglutarate-derived amino acids, sugar alcohols, and carbohydrates involved in the tricarboxylic acid (TCA) cycle. Also, more metabolites with antioxidant functions were observed during desiccation; metabolites related to glutathione and tocopherol significantly increased (e.g. oxidized glutathione increased 100-fold and both β- and δ-tocopherol increased >30-fold) (Oliver et al., 2011a). Specific metabolite production upon desiccation is common in resurrection plants; the levels of verbascose and γ-aminobutyrate only significantly increased in the desiccated H. rhodopensis (Gechev et al., 2013). This difference in metabolite levels between dehydration and desiccation indicates that dehydration is a transition process of various metabolic pathways and the purpose of the transition is antioxidant production, nitrogen remobilization, ammonia detoxification, and soluble sugar production, which are critical for surviving desiccation. Compared with gene expression profiles and protein abundance, metabolite levels are shown to change in a uniform direction towards the desiccated state of plants. This may be determined by their functions as protective compounds to osmotic stress and as antioxidants. Sensing and signaling of water stress severity Many studies have revealed that abiotic stress sensing and signaling in plants are integrated in complex networks which involve hormones, Ca2+, ROS, sugars, etc. (Miller et al., 2010; Bose et al., 2011; Keunen et al., 2013; Choudhury et al., 2017). As discussed above, the difference between dehydration and desiccation is the severity of water stress, and the molecular responses vary with the water status of the plants. How is the severity of water stress sensed and which are the steps in signal transduction? Based on the available studies of resurrection plants, we focus mainly on the role of the plant hormone ABA and ROS in sensing and signaling between dehydration and desiccation. It is well known that the hormone ABA is produced rapidly in plants when water stress occurs (Shinozaki and Yamaguchi-Shinozaki, 1997; Osakabe et al., 2014). ABA also plays an important role in regulating plant responses to dehydration and in the acquisition of desiccation tolerance. The increase of ABA levels during dehydration in resurrection plants, such as C. plantagineum, M. fabellifolia, and X. humilis (Bartels et al., 1990; Schiller et al., 1997), indicates that this hormone participates in the development of desiccation tolerance. Desiccation tolerance in C. plantagineum callus requires a pre-treatment with ABA (Bartels, 2005), and the complete desiccation tolerance of P. patens filaments resulted from ABA incubation before dehydration. The deletion of the ABA-activating transcription factor ABI3 (ABSCISIC ACID INSENSITIVE 3) leads to the loss of desiccation tolerance of P. patens (Khandelwal et al., 2010), indicating that ABA-related processes have a central role in acquisition of desiccation tolerance. The transcriptome study in C. plantagineum revealed that the profile of abundant transcripts in the mildly dehydrated sample indicates predominant expression of proteins involved in ABA-mediated responses to water stress (Rodriguez et al., 2010). However, multiple mechanisms and several signaling pathways are involved in activating the dehydration response (Bartels, 2005). In the transcriptome of the woody resurrection plant M. flabellifolia during dehydration, the transcript levels of 53 transcription factors and 91 protein kinases increased rapidly and peaked early during dehydration. Among the signal cascades of molecular pathways that these regulators transduce, both ABA-dependent and ABA-independent drought stress pathways are included (Ma et al., 2015). An example of an ABA-independent signaling is phospholipase D (PLD) in C. plantagineum; PLD activity is induced within minutes by dehydration stress, but not by ABA (Frank et al., 2000). Stevenson et al. (2016) identified ABA-non-responsive mutants in P. patens and identified the ABA NON-RESPONSIVE (ANR) gene encoding a modular protein kinase. The anr mutants fail to accumulate dehydration tolerance-associated gene products in response to dehydration and do not acquire ABA-dependent desiccation tolerance. Despite the existence of ABA-independent signaling in the acquisition of desiccation tolerance, many studies appear to build up a correlation between ABA level and desiccation tolerance. The endogenous ABA level was determined in hydrated and dried leaves of C. plantagineum. After drying, the concentration increased 6-fold (Bartels et al., 1990). Similar increases in ABA content have been noted in Borya nitida (Gaff and Loveys, 1984), M. fabellifolia, X. humilis, and a large range of other resurrection plants (Schiller et al., 1997). The dynamic analysis of phytohormones in H. rhodopensis during desiccation showed that the ABA level reaches a maximum at 25% RWC, but it decreases when RWC becomes lower (Djilianov et al., 2013). In S. stapfianus, ABA reached the highest level in leaves at ~15% RWC and then started to decrease until the desiccated state. This demonstrates that acquisition of desiccation tolerance is closely related to high ABA levels, but the sensing and signaling for desiccation is not dependent on ABA. In addition to ABA, other hormones may also participate in the dehydration response and acquisition of desiccation tolerance. According to the study of Djilianov et al. (2013), the levels of salicylic acid (SA) in H. rhodopensis continuously increased with RWCs declining from 25% to 13%. This indicates that SA may play a role in desiccation sensing and signaling. Although the role of SA in desiccation tolerance is not known, studies from model plants and crops have demonstrated that SA participates in the signaling of various abiotic stresses (Horváth et al., 2007) and its accumulation enhances drought tolerance by interacting with ROS (Miura et al., 2013). Also zeatin and zeatin riboside accumulate to high levels in desiccated C. wilmsii leaves (Vicré et al., 2004). Possibly, the accumulation of cytokinins is necessary for the recovery of metabolism upon rehydration. Another explanation is that cytokinins also participate in the stress signaling of desiccation. Studies on model plants (e.g. Arabidopsis) reveal that plant hormones are involved in multiple processes and the crosstalk between different plant hormones produces synergetic or antagonic interactions, which are crucial to modulate responses to abiotic stress (Peleg and Blumwald, 2011). Future research should focus on the balance of various plant hormones to understand the signaling of dehydration or desiccation. As the accumulation of ROS is a general stress response that can be triggered by osmotic and ionic imbalance in water-stressed cells, the antioxidant response is also an important part of desiccation tolerance. In S. tamariscina, the activities of four antioxidant enzymes [superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and glutathione reductase (GR)] increased gradually during dehydration (Wang et al., 2010). Similarly, dehydration resulted in an increase in glutathione in S. stapfianus leaves, primarily late during the drying regime, to an ~100-fold higher amount in desiccated versus hydrated control tissue (Oliver et al., 2011a). As well as causing oxidative stress, ROS play an integral part as signaling molecules in the regulation of numerous biological processes such as growth, development, and responses to biotic and/or abiotic stimuli in plants (Baxter et al., 2014). Jovanović et al. (2011) demonstrated a critical phase (RWC decreases from 70% to 50%) for Ramonda nathaliae during which hydrogen peroxide accumulates and lipid peroxidation as well as ion leakage take place. They proposed that controlled elevation of ROS, such as hydrogen peroxide, could be an important mechanism for sensing dehydration and triggering an appropriate response program (Jovanović et al., 2011). Results obtained from traditional measurements are questionable, because they ignore the various sources of ROS (from disruptions in metabolic activity or produced for the purpose of signaling) and their subcellular localization. ROS can be produced in the apoplast, chloroplast, peroxisome, mitochondria, vacuole, cytosol, and nuclei (Suzuki et al., 2012). Each cellular ROS compartment has its own ROS homeostasis; the different ROS levels of various compartments form a particular ROS signature (Choudhury et al., 2017). The ROS signature will be affected by different abiotic stresses in plant cells; similarly, dehydration and desiccation may lead to differential ROS signatures. These signatures may create stress-specific signals for dehydration and desiccation, resulting in differential responses. Although it is reasonable to hypothesize a role for ROS in sensing and signaling the severity of water stress, studies with regard to ROS signature changes between dehydration and desiccation still need to be conducted. The connection between studies from resurrection plants and their application in crops To date, the major emphasis of biotechnological approaches for improving crop drought tolerance has been in engineering genes that encode compatible organic osmolytes, plant growth regulators, antioxidants, heat shock and late embryogenesis abundant proteins, and transcription factors involved in gene expression (Ashraf, 2010). Therefore, the comparison between responses to dehydration and desiccation provides insights into improving crop drought tolerance just from these above aspects. Although many transgenic lines which show improved growth under water-limiting conditions have been identified under controlled environments, the development of drought-tolerant crops is still some distance away (Deikman et al., 2012). Compared with crops that show tolerance to drought, desiccation-tolerant plants exhibit extreme tolerance. Therefore, mechanisms in place in desiccation-tolerant plants may provide better cellular protection in crop plants (Fig. 3). First, there are substantial species-specific genes related to dehydration or desiccation tolerance in resurrection plants (Giarola et al., 2017) which may be candidates for transgenes to be tested. Secondly, key genes encoding proteins or metabolites related to acquisition of desiccation tolerance could be candidates. For example, the genes involved in synthesis of SA or zeatin that are correlated to desiccation could be considered to be tested. As some resurrection plants share relatively high similarity in genome architecture with important staple crops, such as O. thomaeum and Oryza or Sorghum (VanBuren et al., 2015), the regulating networks of stress could be important for water stress tolerance, So transcription factors as well as components of the signal transduction pathways that co-ordinate expression of downstream regulons are thought to be optimal targets for engineering of complex traits, such as drought tolerance (Wang et al., 2003). The comparison between dehydration and desiccation help to reveal important TFs in acquisition of desiccation tolerance such as the bHLH, MYB, and WRKY families in M. flabellifolia (Ma et al., 2015). Fig. 3. View largeDownload slide A scheme to explain the benefits of resurrection plants for improving crop drought tolerance. The mechanism to tolerate extreme water stress is the key point to enhance or extend water stress tolerance in crops. Fig. 3. View largeDownload slide A scheme to explain the benefits of resurrection plants for improving crop drought tolerance. The mechanism to tolerate extreme water stress is the key point to enhance or extend water stress tolerance in crops. Concluding remarks Dehydration and desiccation are defined in this review by the water status of plants. This allowed us to compare plant responses to dehydration and desiccation. By analyzing plant performance in terms of main physiological activities, accumulation of protective compounds, synthesis of key hormones, and establishment of antioxidant systems, we propose 30–40% RWC as the boundary between dehydration and desiccation. Research has revealed that desiccation-tolerant plants have similar water loss rates during dehydration to desiccation-sensitive plants. Although dehydration and desiccation can be categorized as moderate and severe water stress, respectively, experiments revealed that the response to dehydration and the acquisition of desiccation tolerance in resurrection plants are based on additional factors, not only on the severity of water stress. To carry out a comparative molecular analysis between dehydration and desiccation, we classified seven main performance types of gene expression, protein accumulation, or metabolite levels during dehydration (Fig. 2). Although a clear distinction between dehydration and desiccation is not pointed out, the comparative analysis suggests that the molecular responses to dehydration tend to be involved in damage repair and adjustments in cellular structure and in physiological metabolism, while those to desiccation preferentially protect cellular structures and prepare cells for recovery. Specific sensing and signaling may exist for dehydration and desiccation, respectively. 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