Plant Salt Stress.pdf

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Plant Salt Stress

Jian-Kang Zhu, University of Arizona, Tucson, Arizona, USA

Plant salt stress is a condition of excessive salts in soil solution causing inhibition

of plant growth or plant death.

Introduction

On a world scale, no toxic substance restricts plant growthmore than does salt. Salt stress presents an increasingthreat to plant agriculture. Amongst the various sources ofsoil salinity, irrigation combined with poor drainage is themost serious, because it represents losses of once produc-tive agricultural land. The reason for this so-calledsecondary salinization (as opposed to primary salinizationof seashore salty marshes) is simple: water will evaporatebut salts remain and accumulate in the soil. The stresses

created by a high salt concentration in the soil solution aretwo-fold. Firstly, many of the salt ions are toxic to plantcells when present at high concentrations externally orinternally. Typically, sodium chloride constitutes themajority of the salts. Sodium ions are toxic to most plants,and some plants are also inhibited by high concentrationsof chloride ions. Secondly, high salt represents a waterdeficit or osmotic stress because of decreased osmoticpotential in the soil solution. The mechanism of plant salttolerance is a topic of intense research in plant biology. Theobjectives are to understand the controlof ion homeostasisand osmotic regulation, and to use the knowledge toengineer crop plants with enhanced salt tolerance.

Salt Stress Damage to Plants

General symptoms of damage by salt stress are growthinhibition, accelerated development and senescence, anddeath during prolonged exposure. Growth inhibition is theprimary injury that leads to other symptoms althoughprogrammed cell death may also occur under severesalinity shock. Salt stress induces the synthesis of abscisicacid which closes stomata when transported to guard cells.As a result of stomatalclosure, photosynthesis declines and

photoinhibition and oxidative stress occur. An immediateeffect of osmotic stress on plant growth is its inhibition ofcell expansion either directly or indirectly through abscisicacid.

Excessive sodium ions at the root surface disrupt plantpotassium nutrition. Because of the similar chemicalnature of sodium and potassium ions, sodium has a stronginhibitory effect on potassium uptake by the root. Plantsuse both low and high affinity systems for potassiumuptake. Sodium ions have a more damaging effect on the

low affinity system which has a low potassium/sodiumselectivity. Under sodiumstress,it is necessary for plants toperate the more selective high affinity potassium uptaksystem in order to maintain adequate potassium nutritionPotassium deficiency inevitably leads to growth inhibitiobecause potassium, as the most abundant cellular cationplays a critical role in maintaining cell turgor, membranpotential and enzyme activities.

Once sodium gets into the cytoplasm, it inhibits th

activities of many enzymes. This inhibition is alsdependent on how much potassium is present: a higsodium/potassium ratio is most damaging. Even in the casof halophytes that accumulate large quantities of sodiuminside the cell, their cytosolic enzymes are just as sensitivto sodium as enzymes of glycophytes. This implies thahalophytes have to compartmentalize the sodium into thvacuole, away from cytosolic enzymes.

An important factor in the battle between sodium anpotassium ions is calcium. Increased calcium supply has protective effect on plants under sodium stress. Calciumsustains potassium transport and potassium/sodium selectivity in sodium-challenged plants. This beneficial effec

of calcium is largely mediated through an intracellulasignalling pathway that regulates the expression anactivity of potassium and sodium transporters.

Glycophytes and Halophytes

Most plants are glycophytes that cannot tolerate salt stresHalophytes are plants that naturally grow under higsalinity and are therefore tolerant of salt stress. A survey ohalophytes showed that they are widespread among thvarious orders of higher plants (Flowers et al., 1977). Th

widespreadoccurrence among higher plants is indicative oa polyphyletic origin of halophytes.

Whereas glycophytes are severely inhibited or evekilled by 100200 mmol L21 NaCl, halophytes can survivsalinity in excess of 300 mmol L2 1. Some halophytes catolerate extremely high levels of salts. For exampleAtriplex vesicaria can produce high yields in the presencof 700 mmolL21 NaCl, while Salicornia europaea plantwould remain alive in 1020 mmolL2 1 NaCl. On the otheextreme are very salt-sensitive glycophytes, for exampl

Article Contents

Secondary article

. Introduction

. Salt Stress Damage to Plants

. Glycophytes and Halophytes

. Sodium Tolerance Mechanisms

. Changes in Metabolism During Salt Stress

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fruit trees suchas citrus and avocado, which are sensitive toa few millimoles per litre of NaCl.

Measurements of ion contents in plants treated with saltstress revealed that halophytes accumulate salts whereasglycophytes tend to exclude the salts. Considering thathalophytes often grow under very high salinity, it is notsurprising that they have evolved mechanisms to accumu-

late ions in order to lower cell osmotic potential. Thisosmotic adjustment is necessary because the plants have tocontinue to extract water from the salty solution to meettranspirational demands of their leaves. More than 80% ofthe accumulated ions in halophytes are carried in thetranspirational stream of the xylem to the leaves. Somehalophytes have also evolved specialized cells in the leavesand stems to remove the salts out of the plants. Thesespecialized cells, termed salt glands, can take up salt fromneighbouring cells, and excrete it on the leaf surface, whereit is removed by rain or wind.

Because developing extremely salt-tolerant cropsthrough conventional breeding or genetic engineering is

still a daunting task, some attempts have been made todomesticate halophytes for use as food, forage or oilseedcrops. Such attempts have identified Salicornia bigeloviiasa promising crop. It is a leafless, succulent, annual salt-marsh plant that flourishes in saltwater. The plant can begrown with seawater irrigation and yield oil that iscomparable in quantity and quality to soybean and otheroilseed crops. However, seawater irrigation is currentlycostly and its application is eventually restricted to coastaldesert land.

Sodium Tolerance MechanismsGenetic analysis has shown that maintenance of potassiumnutrition is the key to sodium tolerance (Zhu et al., 1998).Mutant plants that cannot do so have significantlydecreased sodium tolerance. The underlying mechanismfor maintaining at least a threshold level of cytosolicpotassium in plant cells under sodium stress seems to besimilar to that operating in the unicellular yeast Sacchar-omyces cerevisiae. Firstly, sodiumstress has to be sensed byan as yet unknown receptor(s). Presently it is also notknown whether extracellular or intracellular sodium issensed. The first detectable response to sodium stress is a

rise in the cytosolic free calcium concentration. Thiscalcium signal serves as a second messenger that is believedto turn on the machinery for potassium uptake andpotassium/sodium discrimination. In plantcells, the sensorprotein for this calcium signal is termed SOS3. It is sodesignated because a loss-of-function mutation in thisprotein renders the Arabidopsis thaliana plant overlysensitive to salt. In fact, sos3 mutant plants are specificallyhypersensitive to sodium stress. SOS3 is functionallysimilar to the B subunit of the protein phosphatase

calcineurin. In yeast cells, calcineurin upon activation bcalcium would modify potassium transporters. As a resullow affinity potassium transport is turned off because cannot sufficiently discriminate potassium from sodiumMore importantly, high affinity potassium transport turned on. High affinity potassium transporters have thability to take up potassium in the presence of hig

concentrations of the interfering sodium ion. Although has not been experimentally proven, essentially the samprocesses are believed to take place in plant cells followinactivation of SOS3 by calcium. Besides the regulation opotassium transport, the SOS3 or calcineurin pathway ialso important in the induction of transporters thatremovsodium from the cells. Such transporters include, foexample, sodium/proton antiporters.

The mechanism that deals with potassium acquisitioalso functions to exclude sodium by switching off thnonspecific low affinity potassium transport systemHowever, even with an operational sodium exclusiosystem, some sodium will still manage to leak into th

cytoplasm. Extrusion of sodium out of the cell can bachieved by sodium/proton antiporters on the plasmmembrane. But sodium extrusion may be of use only tcertain specialized cells, for example root epidermal cellsThis is because most cells in the plants are bordered bother cells and sodium extruded by one cell becomes problem for neighbouring cells.

An important mechanism for dealing with cytosolisodiumis tostore itin thevacuolar compartment whereitnot in contact with cytosolic enzymes. Vacuolar compartmentation of sodium is achieved presumably by the actioof sodium/proton antiporters on the tonoplast, thvacuolar membrane. The proton gradient that drives th

antiport is generated by the tonoplast proton-ATPase anpyrophosphatase. Compartmentation of sodium into thvacuole not only separates sodiumfrom cytosolic enzymeit also helps offset the low extracellular osmotic potentiacreated by salt stress.

Vacuolar compartmentation of sodium is perhaps morimportant for halophytes that actively accumulate largamounts of sodium. Because the cytosolic enzymes are notolerant to sodium inhibition in those halophytes, most othe accumulated sodium needs to be pushed into thvacuole. Indeed, it is not uncommon to find sodium aconcentrations that approximate 0.5 mol L2 1 or more ithe vacuoles of halophytes. The counter ions are typicall

chloride and malate.

Changes in Metabolism DuringSalt Stress

Perhaps the most dramatic change in metabolism occurs ithe ice plant (Mesembryanthemum crystallinum) under sastress.Within days, salt stress canelicit a changefrom C3 t

Plant Salt Stress

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the CAM (crassulacean acid metabolism) mode of photo-synthesis in this succulent plant. Some of the enzymaticmachinery for CAM metabolism, e.g. phosphoenolpyr-uvate (PEP) carboxylase, is induced by a few hours of saltstress. The main advantage of the CAM metabolism is anincreased water use efficiency because the stomata onlyopen at night when evaporative waterloss is at a minimum.

A metabolic change common to most if not all plants isthe accumulation of low molecular weight organic solutesunder salt stress. These solutes include linear polyols(glycerol, mannitol or sorbitol), cyclic polyols (inositol orpinitol and other mono- and dimethylated inositolderivatives), amino acids (glutamate or proline) andbetaines (glycine betaine or alanine betaine). Plants thatoften experience nitrogen limitation may accumulatesulfonium compounds, e.g. dimethylsulfonium propio-nate, which are equivalent to the nitrogen-containingbetaines. Unlike the inorganic solutes such as sodium andchloride ions, these organic solutes even at high concen-trations are not harmful to enzymes and other cellular

structures. For this reason, these organic compounds areoften referred to as compatible osmolytes. At highconcentrations, compatible solutes certainly function inosmotic adjustment. This is especially true in halophytes,which often accumulate between 0.5 and 4.0 mol L2 1 ofcompatible osmolytes in the cells. The high concentrationof compatible osmolytes reside primarily in the cytosol, tobalance the high concentration of salt outside the cell onone side, and on the other side to counter the highconcentrations of sodium and chloride ions in the vacuole.

Not only are the organic solutes not harmful, they mayalso have a protectiveeffect against damageby toxic ions ordesiccation. Genes encoding rate-limiting enzymes for

polyol, proline and glycine betaine biosynthesis have beenoverexpressed in transgenic tobacco and Arabidopsis

thaliana. The transgenic plants constitutively producincompatible osmolytes perform better than control planunder salt stress. The protective effect cannot be fullexplained by the osmotic adjustment theory because imost cases the transgenic plants only produce severamillimoles per litre more of the engineered osmolyteconcentrations too low to contribute significantly t

osmotic adjustment. Current models hypothesize that thlowamount of compatible osmolytes mayprotect plants bscavenging oxygen free radicals caused by salt stress. Thimportance of antioxidants in salt stress tolerance is alssupported by experiments showing a positive effect ogenetically engineered production of oxygen free radicascavenging enzymes on plant performance under salinity

References

Flowers TJ, Troke PF and Yeo AR (1977) The mechanism of sa

tolerance in halophytes. Annual Review of Plant Physiology 2

89121.Zhu JK, Liu J and Xiong L (1998) Genetic analysis of salt tolerance

Arabidopsis thaliana. Plant Cell10: 11811192.

Further Reading

Bohnert HJ and Jensen RG (1996) Strategies for engineering water-stre

tolerance in plants. Trends in Biotechnology 14: 8997.

Flowers TJ, Troke PF and Yeo AR (1977) The mechanism of sa

tolerance in halophytes. Annual Review of Plant Physiology 2

89121.

Liu J and Zhu J-K (1998) A calcium sensor homolog required for pla

salt tolerance. Science 280: 19431945.

Niu X, Bressan RA, Hasegawa PM and Pardo JM (1995) Io

homeostasis in NaCl stress environments. Plant Physiology 10

735742.

Plant Salt Stress

ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net

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Plant Salt Stress.pdf