A Review of Salinity Stress on Plants
By Meghan Estes
All plants are subjected to a multitude of stresses throughout their life cycle.† Depending on the species of plant and the source of the stress, the plant will respond in different ways.† When a certain tolerance level is reached, the plant will eventually die.† When the plants in question are crop plants, then a problem arises.† The two major environmental factors that currently reduce plant productivity are drought and salinity (Serrano, 1999), and these stresses cause similar reactions in plants due to water stress.† These environmental concerns affect plants more than is commonly thought.† For example, disease and insect loss typically decrease crop yields by less than ten percent, but severe environmental problems can be responsible for up to sixty-five percent reduction in yield (Serrano, 1999).† There are global constraints on fresh water supplies, and this has led to a surge of interest in reusing water (Shannon and Grieve, 1999).† However, in many cases the value of water has decreased because the water is salty.† Salt stress can be a major challenge to plants.† It limits agriculture all over the world, particularly on irrigated farmlands (Rausch, 1996).† To farmers, salt tolerance is important in vegetables because of the cash value of crops (Shannon and Grieve, 1999).† As more land becomes salinized by poor irrigation practices, the impact of salinity is becoming more important (Winicov, 1998).† This is creating the need for salt tolerant plants.† Salinity resistance is a quantitative trait, and it has been resistant to plant breeding (Winicov, 1998).†
Many factors interact with salinity, and this complicates studies on the effects of salinity.† For example, humidity, temperature, light, irrigation, and soil fertility all alter the effect of salinity when present (Allen et al., 1994).† The plants that grow in saline soils have diverse ionic compositions and a range in concentrations of dissolved salts (Volkmar et al., 1998).† These concentrations fluctuate because of changes in water source, drainage, evapo-transpiration, and solute availability (Volkmar et al., 1998).† Due to these varying conditions, plant growth depends on a supply of inorganic nutrients, and this level of nutrients varies in time and space (Maathius and Amtmann, 1999).† Either extreme condition concerning nutrients results in deficiency or toxicity in plants, and this is demonstrated by salt tolerance (Maathius and Amtmann, 1999).† These conditions vary according to the plant species and growth conditions.† Little is known about the genetic basis for diversity of salt tolerance in plants, and this could be partly explained through the definitions given for salinity.
Plants in natural environments are being exposed to increasing amounts of salinity.† One-third of the land being irrigated worldwide is affected by salinity, but salinity also occurs in non-irrigated land (Allen et al., 1994).† There are large areas of primary salinity, but secondary salinity can be detected within one hundred years of settlement on an area of land.† Drought and salinity are connected because in many regions, raising plants requires irrigation.† The irrigation water contains calcium, magnesium, and sodium (Serrano et al., 1999).† As the water evaporates and transpires, calcium and magnesium transpire, leaving sodium dominant in the soil (Serrano et al., 1999).† At low salt concentrations, yields are mildly affected or not at all (Maggio et al., 2001).† As the concentrations increase, the yields move towards zero.† In fields, the salt levels fluctuate seasonally and spatially, and variation will occur due to the circumstances influencing each particular plant. This variability makes research difficult.†† The uptake of ground water by plant roots can increase the salinity of ground water or the soil around the roots due to the exclusion of salt (Niknam and McComb, 2001).† These variable conditions make research difficult, and this is compounded by the fact that each species has its own level of salt tolerance. Together, it will be a complicated process to match plants with their optimal growing conditions.
The response of plants to salt stress is based on the transcriptional action of many defense proteins, and research has not discovered the basis for them all (Serrano, 1999).† Osmotic stress and ion toxicity are the problems stemming from salt stress, and the resulting decrease in chemical activity causes cells to lose turgor (Serrano et al., 1999).† Cell growth depends on turgor to stretch the cell walls, and lack of turgor implies danger for cell survival.† The plantís defense against this salinity attack requires osmotic adjustment, and, to a certain degree, this can be done through synthesis of intracellular solutes (Serrano et al., 1999).† Salinity creates the specific problem of ion toxicity, because a high concentration of sodium is bad for the cells.† High salt concentrations inhibit enzymes by impeding the balance of forces controlling the protein structure (Serrano et al., 1999).† The toxic effects of salt can occur at relatively low concentrations, depending on the plant species, so the homeostasis of sodium is important for the tolerance of organisms to salt stress.† The stress caused by ion concentrations allows the water gradient to decrease, making it more difficult for water and nutrients to move through the root membrane (Volkmar et al., 1998).† In turn, the water uptake slows, and as the osmotic effect spreads from the root membrane to the internal membranes, the ion concentration inside the plant alters the solute balances (Volkmar et al., 1998).† Once high concentrations of salt have reached the inside of the plant, tissue and organs development is altered.† The salt causes a slower rate or shorter duration of expansion of cells, and this compromises the size of the leaves (Volkmar et al., 1998).† The overall effect of salinity on plants is the eventual shrinkage of leaf size, which leads to death of the leaf, and finally the plant.† Salinity may also cause reduced ATP and growth regulators in plants (Allen et al., 1994).†
There is a wide spectrum of salinity tolerance among higher plants (Robinson et al., 1997), but there is also variability in salt tolerance occurring in plants with lower salt tolerance, suggesting that there is the potential for improvements to be made in these plants (Allen et al., 1994).† Because the responses in plants are not identical, those with better adaptations may be studied in an attempt to improve the other species.† Halophytes are known for their adaptation to living in salty solution environments, and these plants adapt to salinity through altering their energy metabolism (Winicov and Bastola, 1997).† These plants provide viable organisms to study the mechanisms they use to handle high concentrations of salt.† By using these plants as models, research should be capable of improving the tolerance of non-halophytic plants. It is known that salinity induces a change in the signals of root origin, which changes the hormonal balance of the plant, and this affects root and shoot growth (Lerner et al., 1994).† Through observation of root and shoot growth and response to salinity, the varying degrees of salt tolerance can be determined.†
The ability of plants to survive and maintain their growth under saline conditions is known as salt tolerance.† This is a variable trait that is dependent on many factors, including the species of the plant.† There is a continuous spectrum of plant tolerance to saline conditions ranging from glycophytes that are sensitive to salt, to halophytes which survive in very high concentrations of salt (Volkmar et al., 1998).† Unfortunately, most crops are not halophytic.† Studies in crops suggest that salt tolerance is a multigenic trait (Niknam and McComb, 2000), which makes it more difficult to study and improve.† Although, it has also been noted that in some species the salt tolerance acquired can be passed along to offspring (Niknam and McComb, 2000).† Tolerant species use more than one strategy to tolerate or avoid stress.† It is important to keep the levels of ions low in the leaves, particularly in the young ones.† This can be done by excluding the ions at the point of uptake and reducing the translocation of ions to the shoot (Niknam and McComb, 2000).† The capacity of the plant leaves to accommodate the export of salt from the root is linked to the growth rate, so the ability of the plant to continue to grow would indicate a high level of salt tolerance.† Plants have morphological features in their roots that can prevent the uptake of large amounts of salt.† If salt does enter the plant, there are physiological and metabolic events that can counteract salt at a cellular level (Winicov, 1998).† Specifically, there are two mechanisms commonly used by plants to tolerate high salt concentrations.† Avoidance is the process of keeping the salt ions away from the parts of the plant where they are harmful (Allen et al., 1994).† This can be done through the passive exclusion of ions by a permeable membrane, the active expelling of ions by ion pumps, or by dilution of ions in the tissue of the plant (Allen et al., 1994).† Secondly, tissue tolerance occurs when ions have already accumulated in the tissue of the plant, and they are then compartmentalized into the plantís vacuoles for storage (Allen et al., 1994).† These two methods prevent the ions from accumulating and causing damage to the plant.† These would be ideal targets for genetic manipulation of plants to become more tolerant of saline conditions.†
In order to judge the tolerance of plants to salinity, the growth or survival of the plant is measured because this is the culmination of many physiological mechanisms occurring within the plant (Niknam and McComb, 2000).† In low to moderate salinity conditions, salt exclusion is the strategy.† Hence, the growth and yield are measured as determinants of salt stress (Niknam and McComb, 2000).† However, under higher salinity conditions, ion toxicity becomes a cause of death, so survival is measured (Niknam and McComb, 2000).† Researchers must decide whether to test for the ability to survive under mild salt stress and never know the full potential of the plant to grow.† On the other hand, subjecting plants to concentrations beyond their capability results in death of the plant and little knowledge of the salt tolerance.†
Plants have several processes to respond to salt stress.† A basic two-phase model describes the overall growth response to salinity as an initial water deficit lasting for a few days or weeks.† Then the second phase occurs, where the ion toxicity initiates leaf death (Rausch et al., 1996).† This overview of plantsí response to salt stress broadly categorizes the cellular mechanisms, but there is more detail to the cellular reaction.† The early response of plants reacting to salt that has reached their leaves is to exclude it from the cytoplasm (Volmar et al., 1998).† One means of eliminating the salt that accumulates in plant cells is through storage of the salt ions in vacuoles.† This is an important adaptation of plants to salinity.† Another method is allowing the salt to build up outside the cells, in the intracellular space.† This leads to a gradient of water moving out of the cells to accommodate the change in ion concentration, and eventually too much water leaves the cell and the cell becomes dehydrated (Volmar et al., 1998).† This will lead to cell death.† The vacuoles comprise most of the cell volume making them good for storage, but the cytoplasm is only one percent of the cell volume (Volkmar et al., 1998).† This makes the cytoplasm very sensitive to slight changes in rate of saline transport.†† The rate of salt passing through the membrane must not exceed the rate of salt being collected into the vacuoles, or there will be an imbalance in the cell (Volkmar et al., 1998).† As older cells lose their capacity to grow and provide vacuoles, the new growth cannot handle the burden of collecting all the salt ions, this leads to premature death in the cells of leaves, and the plant will quickly succumb to the decreasing ability to compartmentalize the salt (Volkmar et al., 1998).†
Exclusion of salt from the shoot is a prime form of tolerance in non-halophytic plants, and most of the sodium going from the roots to the shoots is via the xylem stream (Robinson et al., 1997).† This means that the rate of accumulation is mostly determined by the rate of transpiration (Volkmar et al., 1998).† Therefore the stomatal control of transpiration would control the uptake of sodium, and the inhibition of stomatal opening would regulate the salt level in the shoot (Volkmar et al., 1998).† This inhibition combined with the compartmentalization in vacuoles would help achieve a tolerable level of salt within the cell.† These two mechanisms also provide feasible pathways to genetically manipulate for more salt tolerant plants.† Additionally, the ability of plants to counteract stress will depend on the levels of potassium available to the plant (Maathius and Amtmann, 1999).† Potassium is important to all plants as a balancing charge, and the plant must maintain a high potassium level to counter balance the excess salt.† Alternatively, sodium is only essential for some C4 species, where it functions as a micronutrient (Maathius and Amtmann, 1999).† For most other species, sodium is not necessary for growth.† The availability of some sodium is beneficial to the plant, but too much will cause damage.† Another means of salt stress damage is found in relation to potassium within the cell.† Due to the similar structures of sodium and potassium, the competition for binding sites causes potassium deficiency within the cell (Maathius and Amtmann, 1999).† The sodium competing for potassium binding sites in the cytoplasm inhibits metabolic processes that depend on potassium, and this is another pathway that mandates cellular levels of sodium must be kept to a minimum.† Some studies have shown that plants able to maintain a high level of potassium are also associated with salt tolerance (Volkmar et al., 1998).
The ratio of sodium and potassium in a cell is controlled by transport systems on plasma and vacuolar membranes, and there are three processes that transport these ions.† Pumps are transporters fueled by energy and transported across an electrochemical gradient, but there are no pumps found in higher plants (Maathius and Amtmann, 1999).† Next, carrier proteins undergo conformational change during transport, and finally ion channels are proteins that catalyze the dissipation of transmembrane ionic gradients (Maathius and Amtmann, 1999; Yeo, 1998).† All of these mechanisms transport ions across membranes, and they could all potentially be useful in altering the salt tolerance in plants by over-expression of these genes.† There is not an extensive amount of understanding surrounding these transporters, but it is thought that they activate long distance signaling pathways (Maathius and Amtmann, 1999).† Similarly, a sodium-hydrogen antiport has been reported in salt tolerant species, but it is absent in salt sensitive species (Maathius and Amtmann, 1999).† This demonstrates that it may be implicated as a factor influencing sodium accumulation.† There may be specific processes or individual enzymes that are especially sensitive to salinity, and if these processes are overcome, tolerance may be achieved for a wider variety of plants at a higher concentration of salinity (Yeo, 1998).† There would also need to be a high level of specificity of expression in a gene engineered to pump out sodium (Yeo, 1998).† If the pump was active on a continuing basis, it could be lethal to the cell.† In reality, many processes will have to work together to achieve tolerance.†
Concentrating on larger scale methods of dealing with salt stress, plants have several mechanisms to adjust to a saline environment.† Lots of information states that roots play a crucial role for short-term adaptation to salt tolerance.† The concentrated salt surrounds the root membrane, and it is thought that the morphology of the roots affects the amount of salt taken into the plant (Maggio et al., 2001).† Some features of the root must be advantageous because they help the root take in water.† Because salinity is first perceived in the root, the root sends the signal hormone abscisic acid, which directly or indirectly down regulates the leaf expansion rate (Rausch et al., 1996).† Salt exclusion from the root is likely to be part of the salt tolerance found in plants.† However, when salt ions make it into the plant, they accumulate in the leaf.† As stated above, it is beneficial to the cells of the leaves to compartmentalize the salt ions into the vacuoles.† Leaf cell growth is sensitive to salt, because the energy used for compartmentalization takes energy away from cell growth (Volkmar et al., 1998).† The root signal tells the shoot to stop growing to conserve energy as well.† Growth could be considered a means of regulating the concentration of salt, although high concentrations of salt induce inhibition of growth when the plant needs to continue growth to dilute salt concentrations and find space for vacuoles.† All of these broad reactions to salt stress could be target systems to regulate tolerance by the plants: the structural components of the roots, ion transporters, or cell wall and membrane components (Winicov and Bastola, 1997).† These mechanisms are the only way that plants can adapt to saline conditions themselves, but there have been suggestions of external maneuvers to counteract the salinity.†
Some scientists have suggested that trees could be planted to take up some of the excess salt.† Trees have high water use and can lower water tables to reduce salt discharge into streams (Niknam and McComb, 2000).† This would prevent secondary salinization of the surrounding areas, and benefit plants living near the tree.† It has not been proven to what extent the tree planting would assist in preventing salt stress in plants.† Many other studies have shown that salt stress can also be alleviated by an increased supply of calcium to the growth medium (Rausch et al., 1996).† Depending on the concentration ratio, sodium and calcium can replace each other from the plasma membrane, and calcium might reduce salt toxicity† (Rausch et al., 1996).†† If none of these mechanisms are available to the plant, eventually the leaf death rate will overcome the leaf growth rate and plant death will occur.† The differences found in salt tolerant plant species are related to the time it takes salt to reach its maximum accumulation and cause plant death.† By studying plants with varying tolerance, eventually scientists will discover the differences in the plant genome that are causing sensitivity or resistance.†† A new strategy to study salt sensitive plants involves selecting root mutants with high sensitivity (Maggio et al., 2001).† This is hard to study because there are not many species that have root mutants other than Arabidopsis.† If there are gene sequences that are similar, then this method should be helpful in discovering the genes responsible for salt sensitivity.†
Although there is not enough knowledge on the specifics of salt tolerance in every plant species, there are numerous options for genetic modification of plants to make them more tolerant to salt stress.† Some progress has been made with the tomato plant, and transgenes have been successfully inserted into its genome (Allen et al., 1994).† The tomato plant was recently made to harbor excess sodium in its leaves while leaving the fruit tasting the same.† Many studies have been done on yeast because of the ease with which they are studied, and there are many similarities at the cellular level between fungi, plants, and animals (Yeo, 1998).† Hopefully the studies with yeast will soon prove fruitful in gaining a better understanding of the cellular processes involved in salt stress reactions.† Some studies have shown that acquired cellular salt tolerance can be achieved in the laboratory for some species (Winicov and Bastola, 1997).† This has been achieved through over-expression of genes that become limiting under salt stress.† Consistent with the multigenic characteristics of the salt tolerant trait, these findings imply that small improvements could be made from enhanced expression (Winicov and Bastola, 1997).† These transgenic activities may be successful in over-expressing the transcription of a gene, but many of the processes are dependent on more than one pathway (Winicov, 1998).† This would require the complete understanding of all pathways to have a strong impact on salt tolerance.†
Another option for genetic modification is assistance to the cell in achieving ion homeostasis under salt stress.† This would include altering ion channels or other transporters.† Several of these mechanisms need to be changed because altering one gene may not be sufficient to optimize adaptation to salinity (Winicov, 1998), but altering an ion pump may be a viable option to explore.† As researchers are able to understand the developments happening within the plant, there will be more evidence to support the responses of the plant to the genetic modification.† Some optimistic discussion of salt tolerant plants includes the notion of plants that are able to live virtually in seawater.† Scientists are most likely far away from that ability, but they are working to improve the growing conditions and yield for the crops that are affected by minor secondary salinization (Winicov, 1998).† Maximizing the root growth would also provide relief from the salt stress, and this could be modified within the genome of plants.† It is most likely that multiple modifications will have to occur to overcome the multigenic trait of salt sensitivity.†
Many scientists have become discouraged by the fact that salt tolerance remains largely unexplained due to the many processes that are affected by the stress.† This presents difficulties when transgenic genes are inserted into plants, and the results are not apparent.† As they learn more about the cellular mechanisms and what pathways are explored, then it will be easier to use genetic modification.† Most likely the modification will have to tackle multiple aspects of the salt sensitivity.† Furthermore, the aim of this modification is to assist crop growing, but not to formulate plants that can grow in abnormally high concentrations of salt.† The future of plants looks bright, and this is aided by continual research on the topic.† One day soon, crops will be altered to survive and produce maximum yield grown under minimal conditions.† The problem of salt stress will be alleviated and farmers will be satisfied.†
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