Plant Physiology

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Essay 24.2

Desiccation Tolerance in Seeds and Plants

Maria-Cecília D. Costa, Department of Molecular and Cell Biology, University of Cape Town, South Africa

Phylogenetic evidence suggests that resurrection plants have appropriated a seed-desiccation tolerance mechanism and adjusted it to the whole-plant context (Costa et al., 2017b). For instance, sucrose and oligosaccharides were shown to confer desiccation tolerance to maturing seeds of soybean (Glycine max), pea (Pisum sativum), and maize (Zea mays) (Koster and Leopold, 1988), while in leaves of the resurrection plant Haberlea rhodopensis, the maintenance of constant high levels of sucrose and raffinose increased the chances of surviving desiccation (Djilianov et al., 2011). The accumulation of dehydrins was highlighted as a major attribute for desiccation tolerance in developing Fagus sylvatica seeds (Kalemba et al., 2009) as well as the leaves of the resurrection plant Craterostigma plantagineum (Giarola et al., 2015). In developing rice (Oryza sativa) seeds and in H. rhodopensis leaves, the activation of an extensive antioxidant gene network was correlated with desiccation tolerance (Gechev et al., 2013; He et al., 2016).

Orthodox seeds represent the ultimate example of desiccation tolerance, but they are not the only life form that tolerates desiccation. We find examples of desiccation tolerance also in yeasts, crustaceans, nematodes, rotifers, tardigrades, mosses, liverworts, lichens, algae, and whole plants. It is very likely that desiccation tolerance arose in the transition from aquatic to terrestrial life forms, in organisms living in seashores and tidal habitats, where surviving cycles of dehydration and rehydration were crucial to cell formation and functioning. Later, as plants expanded their habitat onto dry land, which resulted in the establishment of more complex ecosystems, a drawback became evident: desiccation-tolerant plants grow slowly (Alpert, 2006). The processes involved in desiccation tolerance—shutting down metabolism early during drying and fully recovering it upon rehydration—consume energy; desiccation sensitive species use this energy for growth instead, giving them an advantage. This ultimately led to the loss of desiccation tolerance in leaves of vascular plants (Oliver et al., 2000; Alpert, 2006). Desiccation tolerance-related genes were then recruited for processes such as the response to water stress, improved control of water status, vegetative cellular protection and repair, and desiccation tolerance of spores, pollen grains, and seeds (Oliver et al., 2000). Nowadays, desiccation tolerance is common in pteridophytes, rare in angiosperms, and absent in gymnosperms (Porembski, 2011).

In total, only about 1,300 species of vascular plants, of which 135 are flowering plants (termed “resurrection plants”), display desiccation tolerance in their vegetative tissues (Gaff, 1971; Porembski, 2011). These plants occur predominantly in shallow soils on rocky outcrops in semitropical and tropical regions of Africa (Figure 1), America, and Australia (Gaff, 1971; Gaff, 1977; Gaff, 1987; Farrant et al., 2015). Under the harsh microclimatic and edaphic conditions of these areas, resurrection plants are not outcompeted by faster growing desiccation-sensitive plants (Porembski, 2011; Farrant et al., 2015).

Figure 1   Figure 1: Myrothamnus flabellifolia plants growing in their natural environment in Lydenburg (Mpumalanga, South Africa). (Courtesy of Andri Kruger.)

Phylogenetic evidence suggests that resurrection plants have appropriated a seed-desiccation tolerance mechanism and adjusted it to the whole-plant context (Costa et al., 2017b). For instance, sucrose and oligosaccharides were shown to confer desiccation tolerance to maturing seeds of soybean (Glycine max), pea (Pisum sativum), and maize (Zea mays) (Koster and Leopold, 1988), while in leaves of the resurrection plant Haberlea rhodopensis, the maintenance of constant high levels of sucrose and raffinose increased the chances of surviving desiccation (Djilianov et al., 2011). The accumulation of dehydrins was highlighted as a major attribute for desiccation tolerance in developing Fagus sylvatica seeds (Kalemba et al., 2009) as well as the leaves of the resurrection plant Craterostigma plantagineum (Giarola et al., 2015). In developing rice (Oryza sativa) seeds and in H. rhodopensis leaves, the activation of an extensive antioxidant gene network was correlated with desiccation tolerance (Gechev et al., 2013; He et al., 2016).

The recently published comprehensive desiccation-associated transcriptomes of resurrection plants and of seedlings in which desiccation tolerance has been re-introduced are confirming that the vegetative desiccation tolerance in resurrection plants is an adaptation of developmentally-regulated seed desiccation tolerance mechanisms, thus allowing the identification of the exact mechanisms employed (Figure 2) (Costa et al., 2017b; VanBuren et al., 2017). For example, mechanisms involved in the regulated shutdown of photosynthesis in resurrection plants and developing seeds; protection against water loss and institution of a slow drying rate; maintenance of cell integrity via the accumulation of compounds; modification of cell wall plasticity/elasticity; and longevity in the dry state (Costa et al., 2017b).

Figure 2   Summary of differences between resurrection plants and desiccation-sensitive plants (modified from Costa et al., 2017). Upon dehydration below 80–60% relative water content (RWC), resurrection plants activate a series of protective mechanisms, such as regulated shutdown of photosynthesis, reduction of leaf area exposed to light, accumulation of protective molecules, and modification of cell wall plasticity/elasticity. At similar RWCs, photosynthesis fails to be downregulated in desiccation-sensitive plants and consequently, there is an increase in the levels of reactive oxygen species (ROS), unfolded and damaged proteins, and other cellular toxins, and activation of drought-induced leaf senescence and cell death.

One of the aims of desiccation tolerance studies is the generation of information useful for the development of crops with improved drought tolerance. Some mechanisms identified by these studies have been successfully used to generate more stress-tolerant plants. For instance, the dehydration responsive element binding (DREB) proteins are some of the earliest transcription factors found to be involved in abiotic stress responses in plants (Rehman and Mahmood, 2015). VuDREB2A (from cowpea, Vigna unguiculata) enhanced drought tolerance in transgenic Arabidopsis thaliana by activating a series of stress-responsive genes (Sadhukhan et al., 2014). Tobacco plants transformed with ThDREB (from Tamarix hispida) performed better than non-transformed plants under salt and osmotic stress (Yang et al., 2017). Transgenic rice plants overexpressing both OsPIL1 and OsDREB1A showed improved drought tolerance without compromising growth (Kudo et al., 2017).

Further progress in improving drought-tolerance in sensitive plants can be made by the identification and characterization of desiccation tolerance-related genes in resurrection plants. For instance, the gene XvSAP1 (from the resurrection plant Xerophyta viscosa) enhanced tolerance to salinity and to osmotic and high-temperature stress in transgenic A. thaliana plants, possibly by stabilizing cell membranes (Garwe et al., 2006). Transgenic tobacco plants overexpressing the aldose reductase enzyme ALDRXV4 (from X. viscosa) showed improved photosynthetic efficiency, less electrolyte damage, greater water retention, and higher proline accumulation under osmotic stress conditions (Kumar et al., 2013). Rice plants constitutively expressing an osmotin from the resurrection plant Tripogon loliiformis (TlOsm) showed increased tolerance to drought, cold, and salinity stresses (Le et al., 2017).

However, individual genes identified by desiccation tolerance studies have only a limited effect on improving stress tolerance because they might require coordinated expression with other genes to be functional. In this sense, the identification of key factors in regulatory networks controlling desiccation tolerance is a more promising approach because it enables the simultaneous manipulation of multiple pathways that are required for tolerance of extreme dehydration (Farrant et al., 2015).

The plant hormone abscisic acid (ABA) is a master regulator of plant development and water loss responses (Nakashima and Yamaguchi-Shinozaki, 2013; Okamoto et al., 2013). ABA regulates embryo and seed development (promotion of seed dormancy and desiccation tolerance), germination, seedling establishment, vegetative development, general growth, and accumulation of protective molecules during dehydration (Nakashima and Yamaguchi-Shinozaki, 2013; Okamoto et al., 2013). ABA accumulates in dehydrating tissues of several species, such as A. thaliana (Harb et al., 2010), Citrus sp. (Agustí et al., 2007), maize (Lü et al., 2007), and the resurrection plants C. plantagineum (Bartels, 2005), Boea hygrometrica (VanBuren et al., 2017), Sporobolus stapfianus (Whittaker et al., 2001), and X. viscosa (Costa et al., 2017a). In dehydrating tissues, ABA leads to changes in gene transcription and in transcript processing and stability and induces the accumulation of dehydrins, antioxidants, transcription factors, protein kinases and phosphatases, and enzymes involved in phospholipid signaling. Increasing the knowledge of ABA-dependent drought responses and their core signalling components may open promising possibilities for the development of drought-tolerant crop plants.

Orthodox seeds and resurrection plants can serve as models to understand the numerous interacting factors promoting desiccation tolerance (Farrant et al., 2015; VanBuren et al., 2017; Costa et al., 2017b). Several studies have advanced our knowledge on such factors. One example is the ABA signalosome complex (PYR/PYL-PP2C-SnRK2) that regulates stress responses and seed development. When ABA levels increase due to environmental stimuli, the ABA signalosome complex induces cellular changes that help to maintain cellular water status and protect proteins and cellular organelles from collapsing under water stress. Moreover, the interaction between ABA and ethylene is crucial for desiccation tolerance. The last step in the biosynthesis of ethylene is susceptible to ABA inhibition, while ethylene modulates drought stress signalling by acting antagonistically to ABA.

A last example of interacting factors promoting desiccation tolerance is the raffinose family oligosaccharides (RFOs). RFOs participate in several crucial plant cellular functions including transport and storage of carbon, signal transduction, membrane trafficking, and mRNA export. RFOs also act as compatible solutes, signalling molecules, and antioxidants. In desiccated leaves of Craterostigma sp., de novo biosynthesis of RFOs induced by water deficit provides additional cellular protection (Egert et al., 2015). In maturing Medicago truncatula seeds, the conversion of sucrose into RFOs was linked to seed vigor during germination and seedling establishment (Vandecasteele et al., 2011).

New data from whole genome, transcriptome, metabolome, and proteome studies are revealing new genes and pathways for crop improvement from non-model plants, increasing the tool box available for plant breeders. Desiccation tolerance studies have a potential not completely explored to contribute with this tool box and facilitate efforts to develop new crop varieties better able to tolerate water deficit conditions.

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