Plants are well adapted to a wide range of environmental conditions. Even though they have notably prospered in our planet, stressful conditions such as salinity, drought and cold or heat, which are increasingly being observed worldwide in the context of the ongoing climate changes, limit their growth and productivity. Behind the remarkable ability of plants to cope with these stresses and still thrive, sophisticated and efficient mechanisms to re-establish and maintain ion and cellular homeostasis are involved. Among the plant arsenal to keep homeostasis are efficient stress sensing and signaling mechanisms, plant cell detoxification systems, compatible solute and osmoprotectant accumulation and a vital rearrangement of solute transport and compartmentation. The key role of ion transport systems and signaling proteins in cellular homeostasis are some of the features addressed in the present chapter. The full understanding of the plant cell complex defense mechanisms under stress may allow the engineering of more tolerant plants or the optimization of cultivation practices to improve yield and productivity, which is crucial in the present time as food resources are progressively scarce.
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Approximately 20% of the world's cultivated land and nearly half of irrigated land are affected by drought and salinity, which became major threats to agricultural production, limiting plant growth and productivity worldwide (Bartels and Sunkar 2005, Rengasamy 2006, Sahi et al. 2006, Silva and Gerós 2009). Understanding ion homeostasis mechanisms and plant tolerance to drought and salinity overall is, therefore, of crucial importance and generates one of the major research topics nowadays. Intracellular K+ and Na+ homeostasis is important for the activities of many cytosolic enzymes, and for maintaining membrane potential and an appropriate osmolyte concentration for cell volume regulation. In normal conditions, plant cells maintain a high K+/Na+ ratio in the cytosol with relatively high K+ levels, in the order of 100-200 mM, and low levels of Na+, of about 1-10 mM (Higinbotham 1973). A correct regulation of ion flux is required for cells to maintain the concentrations of toxic ions low and to accumulate essential ions. Plant cells employ primary active transport, mediated by H+-ATPases, and secondary transport, mediated by channels and co-transporters, to maintain the characteristic high K+/Na+ ratio in the cytosol.
High salinity imposes two stress factors on plants: an osmotic component that results from the reduced water availability caused by high osmotic pressure in the soil, and an ionic stress resulting from a solute imbalance, causing changes in the K+/Na+ ratio and increasing the concentration of Na+ and Cl- in the cytosol (Blumwald, Aharon and Apse 2000). Sodium toxicity arises mainly from the similarity of the Na+ and K+ ions to plant transporters and enzymes. For instance, Na+ stress disrupts K+ uptake by root cells. Additionally, when Na+ is incorporated inside the cells and accumulates to high levels, it exerts severe toxic effects towards enzymes, causing an impairment of the metabolism (Hasegawa et al. 2000). This disturbance of the ion homeostasis results in molecular and cellular damage and whole-plant growth cessation or even cell death. Thus, the regulation of ion transport by salt-stress sensing and signaling provides a model case for understanding the general regulation of ion homeostasis in plant cells. Excessive Na+ has to be effluxed or compartmentalized in the vacuole. However, contrarily to animal cells, plant cells do not have Na+-ATPases or Na+/K+-ATPases and, instead, rely on H+-ATPases and H+-pyrophosphatases to create a proton-motive force that drives the transport of all other ions and metabolites, including Na+ and K+. A wide variety of transporters of H+, K+ and Na+ have been characterized over the last decades (reviewed by Zhu 2003).
Plants can recognize abiotic stresses and elicit appropriate responses involving altered metabolism, growth and development. As drought and salt stresses occur frequently and may affect most habitats, plants have developed several strategies to cope with these challenges: either adaptation mechanisms, allowing them to survive the adverse conditions, or specific growth habits to avoid stress conditions. Stress-tolerant plants have evolved adaptive mechanisms enabling different degrees of tolerance. Differential stress tolerance could be attributed to differences in plant reactivity in terms of stress perception, signal transduction and gene expression programs, or novel metabolic pathways that are restricted to tolerant plants (Bartels and Sunkar 2005). The hypothesis that the genetic program for tolerance is at least to some extent also present in non-tolerant plants is supported by the observation that gradual acclimation of sensitive plants leads to a gain of tolerance to some extent. These plants may need gradual adaptation for appropriate expression of genes responsible for this acquisition of tolerance (Zhu 2001).
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Several efforts have been undertaken to enhance the salt tolerance of economically important plants by traditional plant breeding as well as by biotechnological approaches (Flowers 2004, Karrenberg et al. 2006). Traditional breeding programs trying to improve abiotic stress tolerance have had some success, but are limited by the multigenic nature of the trait. Arabidopsis proved to be an extremely important tool for assessing functions for individual stress-associated genes due to the availability of knock-out mutants and its proneness for genetic manipulation. The in vitro culture approach proved effective in the selection of salt-tolerant cell lines and subsequent regeneration of whole plants with improved salt tolerance, such as alfalfa (Winicov 1991), rice (Winicov 1996, Miki, Hashiba and Hisajima 2001), and potato (Ochatt et al. 1996).
This book chapter deals with several aspects concerning ion homeostasis, from its general features to the more detailed level, such as the activity and regulation of cation transporters to maintain ion homeostasis, the importance of osmolyte synthesis for protein and membrane stabilization, redox control and scavenging of reactive oxygen species (ROS), and the role that a remarkable salt-sensing mechanism plays in the achievement of ion homeostasis and, therefore, abiotic stress tolerance.
2. Plant cell detoxification strategies towards homeostasis
In order to achieve salt and drought tolerance, three related plant activities are essential. First, damage must be prevented or lessened. Second, homeostasis must be re-established in the new, stressful conditions. Third, even if at a reduced rate, plant growth must be resumed following the modifications at the cellular and whole-plant levels (Zhu 2001). The toxic effects caused by ion and osmotic homeostasis disruptions need to be quickly neutralized at the cellular level, so, stress-tolerant plants have evolved efficient detoxification mechanisms.
Plant adaptation to salinity and drought is a complex process, involving far more changes than just an attenuated growth. It implies, at the cellular level, regulation of gene expression, such as those encoding for transporter proteins highlighted later in this chapter (i.e. H+ pumps and Na+/H+ antiporters), transient increases in ABA concentration, accumulation of compatible solutes and protective proteins, increased levels of antioxidants and suppression of energy-consuming pathways (Bartels and Sunkar 2005; Chaves et al 2009). All these changes at the cellular level are critical to restore ion homeostasis after the imbalance caused by any given abiotic stress. By restoring ion homeostasis, plants will tolerate more easily those stresses.
High salt stress, besides imposing toxic effects in the activities of various enzymes, in the integrity of cellular membranes, in nutrient acquisition and in the photosynthetic mechanisms, also generates ROS (Skopelitis et al. 2006). ROS by themselves are a significant cause of damage to a plant in a salt/osmotic stress environment. As a response, plants trigger the production of several stress proteins and compatible osmolytes, among other complex molecular changes (Zhu et al. 1997). Indeed, many of the stress proteins and osmolytes with unknown functions probably play a role in detoxifying plants by scavenging ROS or preventing them from damaging cellular structures, in a similar manner as some key enzymes and osmoprotectants already known to be involved in oxidative protection (Zhu 2001). Plant engineering towards increased biosynthesis of osmolytes that are active ROS scavengers such as mannitol, proline, ononitol, trehalose, fructans, ectoine and glycinebetaine was shown to have a positive effect in abiotic stress tolerance through oxidative detoxification (Shen, Jensen and Bohnert, 1997). The contribution of osmoprotectants towards cellular homeostasis will be further approached in more detail in this chapter.
Transgenic plants overexpressing proteins like superoxide dismutase, ascorbate peroxidase, glutathione peroxidase and glutathione reductase significantly display increased salt and osmotic stress tolerance, as a consequence of a partial neutralization of ROS (Allen et al. 1997; Roxas et al. 1997). A similar gain-of-tolerance outcome was observed after the engineering of tobacco regulatory protein NPK1, a mitogen-activated protein (MAP) kinase. Corroborating the role of NPK1 in oxidative stress response, its A thaliana orthologue ANP1 is activated by H2O2 and initiates a phosphorylation cascade involving two stress MAPKs, AtMPK3 and AtMPK6 (Kovtun et al. 2000). The HOG1 MAPK pathway plays a key role in abiotic stress tolerance in yeast (de Nadal, Alepuz and Posas, 2002) and increasing evidences suggest a vital role of the MAPK pathway in oxidative protection in stressed plants (Bartels and Sunkar 2005). Astonishingly, at least 20 MAPK, 10 MAPKK and 60 MAPKKK genes have been identified in Arabidopsis based on sequence similarities (Riechmann et al. 2000, Ichimura et al. 2002).
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The accentuated expression of late embryogenesis abundant (LEA) proteins like barley HVA1 and stress-related transcription factors such as CBF/DREBs, in transgenic plants are good examples of detoxifying roles played by either the actual expressed proteins or their downstream target proteins. A characteristic of this type of detoxification effect is its remarkable lack of specificity to a given abiotic stress. Transgenic plants overexpressing these proteins have improved tolerance to salinity, drought and freezing stress (Liu et al. 1998). The CBF/DREB transcription factors are able to bind to the DRE/CRT element of the promoters of some stress-related responsive genes, leading to an expression of these target genes regardless of stress (Stockinger, Gilmour and Thomashow, 1997; Liu et al. 1998). Despite the scarce information until now, the biochemical function of these activated genes, mainly LEAs or dehydrins is being progressively understood. One of them, the A. thaliana COR15A, is up-regulated under freezing conditions, when low water availability arises as consequence, and seems to exert a "cryoprotective" role by interacting with cellular membranes to prevent the formation of impaired membrane structures (Steponkus et al. 1998). Findings in the anhydrobiotic nematode Aphelenchus avenae shed some light in the way that LEA proteins may act. The LEA protein identified in A. avenae acts synergistically with the accumulation of trehalose in response to dehydration, by stabilizing the water-replacing hydration envelopes, often named as organic bioglass, that this osmolyte forms to stabilize the cell's content (Browne, Tunnacliffe and Burnell, 2002). Indeed, LEA proteins are extremely hydrophilic and resistant to denaturation by heat, prompting suggestions that they help to avoid damage by water stress, by acting as hydration buffer, molecular chaperone, ion sink or membrane stabilizer (Crowe, J., Hoekstra and Crowe, L. 1992; Dure 1993; Hundertmark and Hincha, 2008). Proving the importance of LEA proteins in plants, 51 LEA protein encoding genes were recently identified in A. thaliana, with a wide range of sequence diversity, intracellular localizations, and expression patterns (Hundertmark and Hincha, 2008). According to the authors, the high fraction of retained duplicate genes and the inferred functional diversification indicate that they confer an evolutionary advantage for an organism under multiple stressful environmental conditions.
3. Sensing and signaling environmental stress
Sensing of salt and dehydration stresses, and of high or low temperatures, is of utmost importance in a process of achieving cellular homeostasis in plants. The sensing mechanisms allow the activation of multiple signaling cascades responsible for the triggering of various cellular responses and, together, stress sensing and signal transduction form crucial adaptive mechanisms in the tolerance to the negative effect of multiple environmental stresses. Plants suffering from dehydration, under high salinity and drought, as well as low-temperature conditions, trigger the biosynthesis of abscisic acid (ABA) which activates a significant set of genes induced by drought, salt and cold (Boudsocq and Laurière, 2005). Probably the most iconic gene up-regulated by ABA is AtNHX1 that encodes the vacuolar Na+/H+ exchanger in A. thaliana (Shi and Zhu, 2002). However, the mechanisms involved in the sensing of osmotic and salt stress in plants are still poorly comprehended, and the majority of the available information comes from studies in microorganisms.
In yeast, hyperosmotic stress is sensed by two types of osmosensors, SLN1 and SHO1, which signal the HOG (high-osmolarity glycerol) MAPK pathway (Bartels and Sunkar 2005). In plants, drought stress may be sensed in part by stretch-activated channels and by transmembrane protein kinases, such as two-component histidine kinases (Urao et al. 1999) and wall-associated kinases (Kohorn 2001). Indeed, in Arabidopsis, the SLN1 homologue ATHK1 acts as osmosensor and sends the stress signal to a MAPK cascade downstream. Recently, direct genetic evidence was found demonstrating that ATHK1 not only is involved in the water stress response in early vegetative stages of plant growth but also plays a distinctive role in the regulation of desiccation processes during seed formation (Wohlbach, Quirino and Sussman, 2008). Heterologous expression of the ATHK1 cDNA into the yeast double mutant, which lacks SLN1, suppressed cell death in high-salinity media and triggered the high osmolarity glycerol response 1 (HOG1) mitogen-activated protein kinase (MAPK) (Urao et al. 1999). Also, the activity of the plant histidine kinase cytokinin response 1 (Cre1) is regulated by changes in turgor pressure, in a similar manner as yeast's SLN1, which prompts it as a probable candidate for sensing osmotic stress in plants (Reiser, Raitt and Saito, 2003). The gene NtC7 from tobacco encodes a receptor-like protein functioning in osmotic adjustment whose membrane location was confirmed in onion epidermis cells transiently expressing an NtC7-GFP fusion protein. NtC7 transcripts rapidly increase after not only salt and osmotic stress treatments but also after wounding (Tamura et al. 2003).