See

discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/225090091

SodiumA Functional Plant Nutrient *

Article in Critical Reviews in Plant Sciences September 2003
DOI: 10.1080/07352680390243495

CITATIONS

READS

105

4,145

6 authors, including:
Guntur Venkata Subbarao

Osamu Ito

Japan International Research Center for Agricu

United Nations University (UNU)

83 PUBLICATIONS 2,172 CITATIONS

73 PUBLICATIONS 1,973 CITATIONS

SEE PROFILE

SEE PROFILE

Ray Wheeler
Kennedy Space Center
278 PUBLICATIONS 3,679 CITATIONS
SEE PROFILE

Some of the authors of this publication are also working on these related projects:
Genetic and Agronomic Exploitation of BNI function in Crops and Pastures - Development of Genetic
Tools and Agronomic Strategies View project
Advanced Life Support and Hydroponics View project

All content following this page was uploaded by Guntur Venkata Subbarao on 09 December 2016.
The user has requested enhancement of the downloaded file. All in-text references underlined in blue are added to the original document
and are linked to publications on ResearchGate, letting you access and read them immediately.

Critical Reviews in Plant Sciences, 22(5):391416 (2003)

C 2003 Taylor and Francis Inc.
Copyright 
ISSN: 1040-8371
DOI: 10.1080/07352680390243495

SodiumA Functional Plant Nutrient

G. V. Subbarao,1 O. Ito,1 W. L. Berry,2 and R. M. Wheeler 3
1

Crop Production and Environment Division, Japan International Research Center

for Agricultural Sciences, Ibaraki, Japan; 2 Dept. of Organismic Biology, Ecology and
Evolution, University of California, Los Angeles, CA, USA; and 3 NASA Biological
Sciences Office, Kennedy Space Center, FL, USA

Referee: Dr. Mohammad Pessarakli, Department of Plant Sciences, The University of Arizona, Forbes Bldg.,
Room 303, Tucson, AZ, 85721

* Note: An earlier version of this manuscript was published as a book chapter in Handbook of Plant and Crop
Physiology, 2nd edition, 2002, pp. 363384, M. Pessarakli, ed., Marcel Dekker, Inc., New York.
** Author to whom correspondence should be addressed: G.V. Subbarao, Crop Production and Environment
Division, Japan International Research Center for Agricultural Sciences, Ibaraki, 305-8686, Japan.

ABSTRACT: Plant scientists usually classify plant mineral nutrients based on the concept of
essentiality defined by Arnon and Stout as those elements necessary to complete the life cycle
of a plant. Certain other elements such as Na have a ubiquitous presence in soils and waters
and are widely taken up and utilized by plants, but are not considered as plant nutrients because
they do not meet the strict definition of essentiality. Sodium has a very specific function in
the concentration of carbon dioxide in a limited number of C4 plants and thus is essential to these
plants, but this in itself is insufficient to generalize that Na is essential for higher plants. The unique
set of roles that Na can play in plant metabolism suggests that the basic concept of what comprises
a plant nutrient should be reexamined. We contend that the class of plant mineral nutrients should
be comprised not only of those elements necessary for completing the life cycle, but also those
elements which promote maximal biomass yield and/or which reduce the requirement (critical
level) of an essential element. We suggest that nutrients functioning in this latter manner should
be termed functional nutrients. Thus plant mineral nutrients would be comprised of two major
groups, essential nutrients and functional nutrients. We present an array of evidence and
arguments to support the classification of Na as a functional nutrient, including its requirement
for maximal biomass growth for many plants and its demonstrated ability to replace K in a number
of ways, such as being an osmoticium for cell enlargement and as an accompanying cation for
long-distance transport. Although in this paper we have only attempted to make the case for Na
being a functional nutrient, other elements such as Si and Se may also confirm to the proposed
category of functional nutrients.
KEYWORDS: Advanced life support, Bio-physical, Chloroplast function, Critical potassium,
Enzyme activation, Essentiality, Essential nutrient, Functional nutrient, Genetic variation, Glycophytes, Halophytes, Inorganic osmoticum, Long-distance transport, Mechanisms, Natrophobes,
Natrophiles, Nutrition, Osmtoic potential, Osmotic adjustment, Partitioning, Photosynthesis,
Potassium, Salinity, Selectivity, Sodium, Stomatal function, Translocation
TABLE OF CONTENTS
I.

Introduction ......................................................................................................................392

II.

Sodium and Essentiality ....................................................................................................394

391

III.

Concept of Functional Nutrient .....................................................................................395

IV.

Uptake and Tolerance of Sodium .......................................................................................395

A. Uptake Mechanisms ....................................................................................................395
B. Regulation, Translocation and Partitioning .....................................................................396

V.

Sodium Function in Metabolism ........................................................................................397

A. C4 Metabolism ............................................................................................................397
B. Replacing Potassium Functions ....................................................................................397
1. Internal Osmoticum ...............................................................................................398
2. Stomatal Function ..................................................................................................400
3. Photosynthesis ......................................................................................................400
4. Counter-Ion in Long-Distance Transport ..................................................................400
5. Enzyme Activation ................................................................................................401

VI.

Growth Stimulation by Sodium .........................................................................................402

VII.

Sodium and Potassium Interactions ..................................................................................403

A. Sodium Replacement of Potassium ...............................................................................404
B. Influence of Sodium on Critical Potassium Levels ..........................................................404

VIII.

Sodium, Other Perspectives ..............................................................................................406

A. Sodium Tissue Levels ..................................................................................................406
B. Genetic Variation in Tissue Sodium ...............................................................................406
C. Closed Life Support Systems for Space .........................................................................407

IX.

Concluding Remarks ........................................................................................................408

I. INTRODUCTION
Sodium nutrition of plants remains a fascinating and elusive topic, despite several decades of
intensive research efforts, particularly during the
1960s and 1970s. Using Arnon and Stouts (Arnon
and Stout, 1939) definition of essential nutrient
modified by Epstein (Epstein, 1965) as the standard
to evaluate essentiality, Na has still not been shown
to be essential for most higher plants (certain types
of C4 plants are an exception). This is despite the
fact that in many plants internal Na tissue levels can
become extremely high, often exceeding K and N
in tissue concentrations (Subbarao et al., 1999a,b,
2000a,b). Sodium and K are chemically and structurally similar monovalent cations. The hydrated Na
ion has a radius of 0.358 nm, while K ion has a radius
of 0.331 nm; thus, it does not appear that size would
be the basis for any major discrimination in uptake
between Na and K through ion channels (Marschner,
1995). Sodium concentrations in the earths crust are
similar to that of K (2.8% vs. 2.6%) (Goldschmidt,
1954; Flowers and Lauchli, 1983). Correspondingly
Na levels are very high in many irrigation waters,
especially in arid lands, often higher than that of
K and in some cases approach 10 times that of K
392

(Table 1). Many halophytic plants are able to take

advantage of this close similarity between Na and K,
and have adapted to grow in areas of high salt (NaCl)
(see review by Glenn et al., 1999) where other less
well adapted plants (i.e., glycophytes) are limited
in growth due to high salinity stress (Greenway and
Munns, 1980). Many non-halophytic plants are also
able to metabolically utilize Na to some degree under conditions of limited K availability. Apparently
there are a number of metabolic functions requiring a manovalent cation, although they may not
specifically require K even though it may be the
most efficient monocation in terms of specific reactions (Marschner, 1971; Subbarao et al., 1999a,b,
2000a,b). Glycophytic plants such as beets, celery,
turnips and spinach can utilize Na to such a degree
that it is possible for farmers to substitute relatively
inexpensive Na salts as fertilizer in place of the more
expensive K fertilizer (Marschner, 1971).
One of the most noteworthy features of Na in
plant nutrition is the remarkable difference among
species in their ability to either accumulate or exclude Na from their tissues. Despite the physical and
chemical similarity between Na and K, many higher
plants have developed a high degree of selectivity
for the uptake of K, even in the presence of large

TABLE 1
Chemical Characteristics and Comparison of Sodium and Potassium Concentrations in Soils, Natural Waters, and Plants (Flowers and Lauchli, 1983)

Atomic number
Atomic weight
Concentration in lithosphere (ppm)
Mineral Soils: (% as the oxides)
Tropical
Temperate
Soil solution (mM)
Soil solution in field soils (mM)
Sea water (mM)
Rivers of N. America (mM)
Rivers of Australasia (mM)
Plant Foliage
-Glycophytes1
-Halophytes2
1
2

Sodium

Potassium

11
23.0
28.3

19
39.5
25.9

0.010.5
0.011.0
0.4150

480
0.4
0.13

0.12
0.14
0.210
0.081.6
10
0.04
0.04

0.22.0
25154

1550
1033

Grown in 5 mM K + 1 mM Na (g kg1 dwt).

Grown in 58 mM K + 295340 mM Na (g kg1 dwt).

amounts of Na. This same high degree of discrimination in favor of K at the soil/root interface is also
often found in the stem transport of cations from the
roots to the shoots (Subbarao and Johansen, 2002).
Thus seeds, fruits and storage tissues of most plants
are relatively low in Na (Subbarao et al., 1999b,
2000a; Subbarao and Johansen, 2002). This apparently is a trait evolved in plants to conserve K, very
often the limiting environmental resource for plant
growth. However, by limiting the transfer of Na from
the soil to plants, it also limits the transfer of Na up
the food chain to animals.
Sodium is an essential element for animals (including humans) and must be present in relatively
large amounts in the diet. Sodium is the principal
electrolyte in animal systems and plays an important
role in maintaining the ionic balance of body tissues
and fluids; its osmotic characteristics are utilized
in the blood stream for regulating osmotic pressure
within the cells and body fluids, where it protects
against excessive loss of water (Harrison, 1991). In
contrast, the principal electrolyte for plants is K,
and even in ecosystems where there is a predominance of Na, plants still exhibit a strong preference
for K (Walker et al., 1996b). Because of the contrast
between plants and animals in their electrolyte requirements, there is insufficient Na available in the
edible portions of most plants for large herbivores.
Therefore the dietary requirements of herbivores for
Na must be met from external supplements, such as
salt licks.

Problems of secondary salinization associated

with irrigated agriculture can partially be related
to the long-term effect of continued discrimination against Na uptake by plants. The degree of
secondary salinization can be limited if appropriate management procedures are applied such as
leaching, biomass removal, and the use of genetic
strategies to improve Na uptake and sequestration
by plants. This paper summarizes the current level
of understanding of Na metabolism and cycling in
plants. Although Na has not been shown to be an
essential nutrient for most plants, there is a high
degree of Na utilization in many plants and some
utilization in most if not all plants. The high degree
of similarity between K and Na (in both physical
and chemical properties) plus the extensive use of
Na by a number of salt-tolerant plants suggests that
Na can replace K in many functions, if not all non-Kspecific monovalent plant functions. Under normal
environmental conditions in nature, there is a relatively limited flow of Na through the organic fraction
of the biosphere compared to other macronutrients.
In contrast, there is abundant flow of Na in the geological fraction. As the result of the flow of Na in
the geological fraction, there is often a buildup of
Na concentrations along with other salts in many geological formations with time. This results in saline
soils where the predominant cation is Na. Under
these saline conditions the growth of many plants
is limited due to the limited water availability and
specific ion toxicity from high levels of Na. Due

393

to its contribution to soil salinity, Na plays a very

significant role in denying large areas of land for
agricultural food production.
Although Na uptake and movement through
plants is limited under natural conditions, it is possible to increase the cycling of Na through plants by
implementing suitable nutrient management practices and/or appropriate genetic strategies. Increased
uptake of Na by plants could be useful in the management of certain saline agricultural systems, and
the management of low-Na pastures. Sodium uptake
by plants is also a major problem in long-term model
biosystems too small to include a mature geological
cycle. This includes the bio-regenerative life support systems being developed by NASA for space
travel. In such a closed system, it would be beneficial
for plants to take up Na so that it could be recycled
back to the crew in the normal food chain. Thus
all waste products including Na-containing wastes
(e.g., urine) could be used to grow plants, which
could then provide food, O2 and clean water for the
crew (Wheeler et al., 2002).

II. SODIUM AND ESSENTIALITY

According to Arnon and Stout (1939), the following conditions must be met for an element to be
considered as an essential nutrient for plants:

r the organism cannot complete its life cycle without it;

r its action must be specific and cannot be replaced

(completely) by any other element;

r its effect on the organism must be direct, not indirectly on the environment.
This set of criteria was expanded by Epstein (1965)
to include

r if an element is part of an essential compound it

also must be essential.
These criteria are based exclusively on ecological considerations for survival and reproduction;
high yield or biomass production may or may not
be an important aspect, and may not even be associated with nutrient essentiality. For example, some
mineral elements such as Na, Se and Si may promote increased biomass production, but may not
be required for the species to survive. In addition,
not all metabolic functions necessarily require a
unique elemental nutrient to function. Many essential metabolic processes are able to function to a
suitable degree with a number of different but chemically and physically similar elements. Chemically
similar elements such as Na, Rb, and K or Se and S
394

often can replace each other in certain non-specific

metabolic functions. Thus, even though an element
may function adequately in an essential function (it
may be even more efficient than any other element),
under the present criteria it would not be considered as an essential nutrient unless it has a unique
function that it alone can meet. It could be argued
from agronomic considerations that additional levels of essentiality should be defined to denote nutrients that may be required for maximal yield or
are able to replace other nutrients in certain essential metabolic functions, thus reducing the critical
level of an essential nutrient. This could have important implications in terms of understanding resource utilization in ecological studies as well as in
implementing our understanding of plant nutrition
in terms of increased agronomic yields.
Based on the expanded criteria of Arnon and
Stout (1939), Na has been shown to be essential
for certain C4 plant species, such as Atriplex vesicaria, A. tricolor, Kochia childsii, Panicum miliaceum and Distichlis spicata L. (Harmer and Benne,
1945; Barbier and Chambannes, 1951; Brownell
and Wood, 1957; Brownell, 1965; Alekseev and
Abdurakhamanov, 1966; Brownell and Jackman,
1966; Brownell and Crossland, 1972; Marschner,
1995; Pessarakli and Marcum, 2000; Pessarakli
et al., 2001). In the absence of Na, these C4 plants
grew poorly, showed visual deficiency symptoms
such as chlorosis and necrosis, or failed to form
flowers. Supplying 100 M Na enhanced growth
and alleviated visual deficiency symptoms. In the
C4 families, Amaranthaceae, Chenopodiaceae, and
Cyperaceae, where Na has been shown to be essential, it is required at micro-nutrient levels (Johnston
et al., 1988). For C4 species such as maize, sorghum
and sugarcane, Na has not even been shown to be
beneficial (Ohnishi et al., 1990). For halophytes,
where Na is clearly beneficial if not essential, it
is also required only at the micronutrient level
(Flowers et al., 1977). Thus, based on the available
evidence, Na has been shown to be essential for only
a very limited number of plants. The question left
unanswered here is how general does the essentiality of an element have to be in the plant kingdom
before it is accepted as being an essential element
or even a nutrient for plants in general.
The application of Na to the growth medium
has been shown to stimulate the growth of many
species, including asparagus, barley, broccoli, brussels sprout, caraway, carrot, chicory, cotton, flax,
millet, oat, pea, rutabaga, tomato, vetch, wheat, cabbage, celeriac, horseradish, kale, kohlrabi, mustard,
radish, rape, celery, mangel, sugar beet, red beet,
Swiss chard, and turnip (Harmer and Banne, 1945;

Larson and Pierre, 1953; Lehr, 1953; Montasir et al.,

1966). Visual leaf symptoms characteristic of low
Na have been reported for a number of crops. In
sugar beet, manigold and red beet symptoms may
appear as a dull, dark green color, rapid wilting in
drought, and a tendency for leaves to grow out horizontally from the crown. In some cases marginal
inter-venal scorch may develop, similar to that of K
deficiency (Lehr, 1953). The presence of tissue Na
is associated with reduced K content in the leaves of
sugar beet and red beet. Several researchers believe
that Na promotes growth and vigor of sugar beet,
which results in increased yield (Lehr, 1947; Troug
et al., 1953). However, any unique function of Na
in the metabolic processes of these crops remains
undetected, and if Na is required, it must be required only at micronutrient levels. Given the ubiquitous presence of Na in the environment, the task of
showing the essentiality of Na at such low levels is
very formidable indeed. The older analytical methods (before 1955, and the use of flame-photometry
or atomic absorption) were not sufficiently sensitive
to determine a relatively low level of requirement
in the presence of the high levels of Na pollution
normally found in the environment. It is therefore
questionable if the deficient solutions employed in
many of these early experiments were completely
free of Na. In addition, there is such a large potential for Na contamination, from both the investigator
and the environment, that every step in the culture
of plants needs to be checked for Na contamination.
Thus, the question of whether Na is an essential
mineral nutrient for higher plants or not is still open
and needs to be adequately tackled with modern analytical techniques, enhanced quality control, and
perhaps a reevaluation or expansion of the criteria
for mineral nutrients.

III. CONCEPT OF FUNCTIONAL

NUTRIENT
To overcome some of the limitations and difficulties associated with a strict definition of essentiality, Nicholas (1961) suggested the term functional or metabolism nutrient, which is defined
as any mineral element that functions in plant
metabolism irrespective of whether or not its action
is specific. However, the way functional nutrient
was defined, it implies that elements that can disrupt
the metabolic functions thus inhibit the plant growth
could also be considered as functional nutrients.
In our opinion, unless a mineral elements participation in plant metabolism is beneficial to the growth
of the plant or increases the plants efficiency of

resource utilization, there is no value in classifying

these elements as functional mineral nutrients. We
suggest that the term functional nutrient should be
defined as an element that is essential for maximal
biomass production or can reduce the critical level
of an essential element by partially replacing it in
an essential metabolic process. The remaining portion of this review deals with this issue and present
evidence to support the notion that Na should be
considered as a functional nutrient, based on the
above definition.

IV. UPTAKE AND TOLERANCE

OF SODIUM
A. Uptake Mechanisms
The concept of dual mechanisms has been
widely recognized in the absorption of alkali cations
by plant roots (Epstein, 1961; Epstein et al., 1963;
Maathuis and Sanders, 1993, 1996; Blumwald et al.,
2000). Because of the chemical similarity between
K and Na, it is generally assumed that K and Na
compete for common absorption sites in the root. Selective ion transport or mechanism-1 transport is effective at very low external K concentrations (Rains
and Epstein, 1965), with a maximum rate at an external K concentration of 1 mM (Epstein, 1961).
Sodium, even in 20-fold excess, fails to compete significantly with K under mechanism-1. Mechanism-1
depends on metabolic energy derived from adenosine triphosphate (ATP). At higher concentrations of
K (up to 50 mM), mechanism-2 becomes important
(Epstein, 1961; Epstein, et al., 1963). Mechanism-2
does not discriminate K from Na and thus Na can
competitively inhibit the absorption of K (Rains and
Epstein, 1965). Also, mechanism-2 does not directly
require metabolic energy to function and is thought
to operate through diffusive forces, which involve
ion channels. Sodium uptake in plants is primarily
believed to be through mechanism-2 (Rains, 1972).
Recently Kin (inward rectifying K channels)
channels have been reported in different root cells,
including cortical, root hair, stelar and xylem
parenchyma cells, that can sense K concentrations
(Findlay et al., 1994; Gassmann and Schroeder,
1994; Vogelzang and Prins, 1994; Wegner and
Raschke, 1994; Maathuis and Sanders, 1995;
Roberts and Tester, 1995; Wegner and DeBoer,
1997; Blumwald et al., 2000; Buschmann et al.,
2000). These ion channels transport at rates between 106 and 108 ions per second per channel
protein. Transport is passive, where diffusion of
ions through the channel is a function of both the
395

membrane voltage and the concentration difference

across the membrane; thus uptake is not directly
coupled to the input of other forms of free energy
(Maathuis et al., 1997; Blumwald et al., 2000). Also,
selectivity is not absolute and many channels can
conduct a range of ions, although not all ions at
the same efficiency (Maathuis et al., 1997). This
property is reflected in the so-called ionic selectivity sequence for the channel, which can have physiological significance. Thus, some K channels conduct Na to a finite extent and can impact the degree
to which plants withstand high Na (i.e. salinity) in
the root zone (Schachtman et al., 1991; Blumwald
et al., 2000). Another property of ion channels is
their ability to reside in open or closed conformational states, which either permit or prevent
ion permeation. This conformational switching can
occur in response to ligands or to a change in membrane voltage after which channels activate or deactivate (Hille, 1992). The control of activation by
membrane voltage or by ligands such as Ca may be
the key to understand the role of these ion channels
in cell biology (Maathuis et al., 1997).
Although it is widely believed that mechanism-1 does not have much affinity to transport Na in
the presence of adequate K, for some crops such as
beets this mechanism may be transporting Na independent of the external concentration (Tullin, 1954).
Several Atriplex species take up Na in preference to
K. In these species, Na competes with K during uptake, but K does not compete with Na (Rains and
Epstein, 1967; Mozafar et al., 1970; Glenn et al.,
1996). Thus specific mechanisms of Na transport
at low concentrations and in the presence of K are
open to further investigation.

B. Regulation, Translocation
and Partitioning
Plant species vary widely in their ability to
absorb Na and translocate it to the shoot (Shone
et al., 1969). Generally, species that absorb Na and
translocate it freely to the shoot are termed natrophiles (Smith et al., 1980). Most plant species
are not able to readily absorb Na, but readily absorb
K and are termed natrophobes (Shone et al., 1969;
Whitehead and Jones, 1972; Smith et al., 1980).
What Na natrophobes do take up is usually retained
in the root with relatively little translocation to the
shoot (Shone et al., 1969). In Natrophobes Na is
only translocated to the tops, when they are subjected to very high concentrations (100 mM) in the
root zone. When this happens, it generally results in

396

major growth reduction and/or death of the plants

due to the specific ion toxicity of Na (Greenway
and Munns, 1980; Cheeseman, 1988). The physiological mechanisms that regulate the Na levels of
these natrophobes are extensively addressed elsewhere (Greenway and Munns, 1980; Cheeseman,
1988; Subbarao and Johansen, 2002).
The ability to translocate large amounts of Na to
the shoot, even among natrophiles, varies widely
among plant species, where halophytes represent
the extreme on the high end (Reimann and Breckle,
1993). The general assumption related to Na tolerance among plants is that they compartmentalize
the absorbed Na in vacuoles, and use it as an inorganic osmoticum in place of or along with K. It is
widely believed that the cytoplasm itself does not
tolerate high levels of Na as it interferes with normal metabolic functioning (Greenway and Osmond,
1972). This seems to be true for both natrophiles
and natrophobes, with the only difference between
these groups being the ability of natrophiles to effectively compartmentalize the absorbed Na. Natrophobes that have limited or no ability to compartmentalize Na must spend substantial amounts of
energy in preventing Na from entering the plant in
order to survive in a saline environment (Subbarao
and Johansen, 2002).
Plant cell cytosol typically contains about
100 mM K and rarely tolerates Na levels beyond
20 mM (Walker et al., 1996a; Amtmann and
Sanders, 1999; Wyn Jones, 1999; Blumwald et al.,
2000). Enzymes isolated from salt-sensitive Phaseolus and salt tolerant Atriplex and Salicornia are
equally sensitive to Na when bioassayed (Greenway
and Osmond, 1972). This was established for four
different enzymes, which included the rather saltsensitive aspartate transaminase as well as salttolerant glucose 6-P dehydrogenase (Greenway and
Osmond, 1972). Furthermore, growth of Phaseolus and Atriplex in saline cultures failed to alter the
specific activity or Na sensitivity of the enzymes
(Greenway and Osmond, 1972). This indicates that
even natrophilic species, such as Atriplex and Salicornia, cannot tolerate high Na levels in their
cytoplasm. They maintain this relatively constant
cytoplasmic level of Na by compartmentalizing the
excess Na in their vacuoles (Greenway and Osmond,
1972). This is an important survival feature of many
halophytic plants under saline conditions (Flowers
and Yeo, 1988; Subbarao and Johansen, 2002).
Halophytes are generally considered natrophiles.
Most crop plants belong to the category of glycophytes. However, some crop plants, such as sugar
beet, red beet, Swiss chard, celery, and turnip have

a substantial ability to absorb and translocate Na to

the shoot (Duke and Atchley, 1986). For red beet,
a considerable build up of Na in the tops can occur whenever Na is present in the nutrient media
(Subbarao et al., 1999a, 2000b). Our studies indicate that Na is absorbed from the nutrient medium
and translocated to the shoot readily in red beet,
but not in either spinach or lettuce (Subbarao and
Wheeler, unpublished).
The extent to which Na is taken up by plants
is influenced by other nutrients, particularly K and
N (Reith et al., 1964), but this varies with species
(Lehr, 1960; Griffith and Walters, 1966). In tomato,
the ability of roots to exclude Na from the rest of the
plant decreased rapidly as the level of K in the nutrient solutions fell (Besford, 1978). In addition, the
rate of transpiration can influence uptake and movement of some ions (e.g., Ca) in plants (Weatherley,
1969). Pitman (1965, 1966) showed that higher rates
of transpiration increased the ratio of K to Na reaching the leaves of barley and white mustard (Sinapis
alba L.).

V. SODIUM FUNCTION
IN METABOLISM
A. C4 Metabolism
In the Calvin cycle of C4 plants, CO2 is concentrated in the bundle sheath cells. An extensive flow of
metabolites between mesophyll and bundle sheath
cells is required to operate this CO2 concentration
mechanism (Marschner, 1995). Sodium appears to
play a critical role in the regeneration of phosphoenolpyruvate (PEP) in mesophyll chloroplasts of
Amaranthus tricolor (Murata et al., 1992). Also, for
many C4 plants, Na has been reported to take part
in chlorophyll synthesis (Ando and Oguchi, 1990).
Sodium deficiency has been reported to impair this
conversion of pyruvate to PEP, which takes place
in the mesophyll chloroplasts (Marschner, 1995). In
certain C4 species, e.g., A. tricolor, the C3 metabolites alanine and pyruvate accumulate, whereas C4
metabolites PEP, malate, and aspartate decrease under Na deficiency (Johnston et al., 1988). Sodium
deficiency led to a reduction in PSII activity and
ultrastructure changes in mesophyll chloroplasts,
but not in bundle sheath chloroplasts of A. tricolor
and Kochia childsii (Johnston et al., 1989; Grof
et al., 1989). Re-supplying Na restored PSII activity (Ohnishi et al., 1990). Photosynthesis in Panicum coloratum was stimulated by Na (Murata and
Sekiya, 1992). In C4 species, nitrate assimilation

also appears to be confined to the mesophyll cells.

For A. tricolor, nitrate-reductase activity is substantially decreased in leaves of Na-deficient plants but
is restored after re-supplying Na (Ohta et al., 1987).
Sodium reportedly enhances nitrate uptake by roots
and nitrate assimilation in leaves of A. tricolor (Ohta
et al., 1989).
Sodium enhanced pyruvate uptake in isolated
chloroplasts of Panicum miliaceum (a C4 species),
indicating that Na+ /pyruvate was co-transported
into the chloroplast by light-stimulated Na efflux
pumps (Marschner, 1995). In contrast, no Na effect on pyruvate uptake rates was noted in mesophyll chloroplasts of Zea mays. Additional evidence suggests that in C4 species of the NADP+
-ME (malic enzyme) type (such as Zea mays and
Sorghum bicolor), H+ /pyruvate co-transport system
operates instead of Na+ /pyruvate co-transport system in mesophyll chloroplasts isolated from Panicum miliaceum (Ohnishi et al., 1990). This emphasizes the necessity of differentiating between
metabolic types of C4 species in studies on the role
of Na.

B. Replacing Potassium Functions

Next to N, K is the mineral nutrient required in
largest amounts by plants for metabolic functions
and growth (Hsiao and Lauchli, 1986). Plant nutritionists have been intrigued for decades by this high
requirement for K. Potassium plays a vital role in
a wide range of biochemical and biophysical processes in plants. It is a highly mobile charge-carrier,
and functions to maintain charge balance; it also
has an important role in the activation of many enzymes and in the process of membrane transport.
The process that is generally regarded as being the
most sensitive to a limited K supply is the maintenance of turgor pressure, and as a consequence,
cell expansion. Biochemically, most K-requiring enzymes require only relatively low concentrations of
K, about 1050 mM of K for maximum activity,
and this may be further reduced by the substitution of other monovalent cations for K such as Na
and Rb (Evans and Sorger, 1966; Wyn Jones and
Pollard, 1983b). It is reported that protein synthesis
in vitro in plant systems is maximized at 100 mM of
K or higher (Pierce and Higinbotham, 1970; Gibson
et al., 1984; Wyn Jones, 1999). Potassium exists
as a monovalent cation in biological systems and
does not participate in covalent bonding. Moreover,
it forms only weak coordination complexes due to
its small ionic charge, low electro-negativity, and

397

its completed 3p electron shell (Hsiao and Lauchli,

1986). However, K is the major cytoplasmic cation
in plant cells and fulfills a number of interrelated
and integrated roles (Leigh and Wyn Jones, 1986;
Wyn Jones, 1999). These include:

r Cofactor in enzyme activation, especially protein

synthesis (translation);

r Stabilization of the active conformation of enzymes and possibly membranes;

r Cytoplasmic volume regulation;

r Energy conservation across membranes;
r Cytoplasmic pH regulation, charge balance.
In general, K functions in plants can be summarized as both biophysical (non-K-specific role as
an osmoticum in the vacuole) and biochemical (specific and non-specific roles in the cytoplasm). According to prevalent concepts, the need of monovalent cations in most plants can be completely filled
by K, but many functions can also be filled by Na
and to some extent by other monovalent cations such
as Rb and Cs, thus reducing the total amount of K
required by the plant. In using K tissue analysis to
determine the nutrient status of K in plants, it is also
necessary in Natolerant plants to know tissue Na
levels. Elevated levels of tissue Na will reduce the
required critical level of tissue K.

1. Internal Osmoticum
The large central vacuole of the plant cell
(which occupies nearly 90% of the cells volume)
provides a large buffer volume, primarily of inorganic ions for satisfying the osmotic requirements
of terrestrial plants without maintaining a large volume of cytosol filled with energy-expensive organic
solutes (Wagner, 1982). The peripheral cytosol layer

facilitates the distribution of chloroplasts close to

the cell surface, thus maximizing the penetration
of light to the photosynthetic apparatus (Wagner,
1982). Potassium makes a major contribution to the
solute potential (s) of the cell (Lauchli and Pfluger,
1979; Wyn Jones et al., 1979). Investigations on 200
plant species by Illjin showed that the contribution
of K to the total s varied from 66% to 90% (Iljin,
1932). The accompanying inorganic anions are primarily Pi , Cl, NO3 and SO4 (Wagner, 1982; Hsiao
and Lauchli, 1986). Although K salts are the most
common inorganic osmotica in the vacuole, there
is no established absolute requirement for K in this
compartment as vacuoles contain high concentrations of many other solutes, such as Na (Harvey
et al., 1981), sugars (Leigh et al., 1979; Wagner,
1982), and amino acids (Thom et al., 1982). If
K salts were the only vacuolar solutes, the s of
the vacuole containing 200 mM K (and associated anions) would be about 0.9 MPa (Hsiao and
Lauchli, 1986). Reported sap s varied from 0.7
to 1.2 MPa for plants not subjected to salt or water
stress (Cram, 1976; Wyn Jones et al., 1979), suggesting that turgor maintenance in the vacuole is
primarily generated by K-salts under K-sufficient
conditions. Examples of K contribution to the total
leaf sap s for red beet, spinach, and lettuce under
K sufficient conditions are given in Table 2.
The vacuole is considered to be a storage organelle and the nutrients accumulated within it
are largely removed from direct active metabolism.
Nevertheless, they are important in generating and
maintaining cell turgor (Wagner, 1982; Leigh and
Deri Tomos, 1983). It has been shown that the vacuolar K levels can be highly variable (10200 mM),
determined mostly by the external concentrations of
K in the root zone. In contrast, cytoplasmic levels are
relatively stable, near 200 mM for most plant species
(Pitman, 1963; Poole, 1971; Lauchli and Pfluger,

TABLE 2
Leaf Sap K Levels, Osmotic Potential (s) and Contribution of K to the Leaf
Sap s for Red Beet, Spinach, and Lettuce Grown Under 5.0 mM K Using
Nutrient Film Technique (Subbarao et al., Unpublished Data)
Plant species

Contribution of K to the
Leaf sap K (mM) Leaf sap s (bars) lamina sap (%)

Red beet
435
(Beta vulgaris)
Spinach
242
(Spinacea oleracea)
Lettuce
244
(Lactuca sativa)

398

9.70

96

9.14

57

9.78

53

TABLE 3
Effect of Replacing K with Na in Hydroponic Solution on Leaf Na Levels of
Red Beet (Source: Subbarao and Wheeler, Unpublished Data)
% Na substituted for K
in nutrient solution (from
a total of 5 mM)

K in sap (mM)

Na + K in sap (mM)

% Na in total
Na + K in sap

0
75
95
98

414
83
25
13

415
222
237
294

0.2
63
89
96

1979; Wyn Jones et al., 1979; Pitman et al., 1981;

Leigh and Deri Tomos, 1983; Leigh and Wyn Jones,
1984; Jeschke and Wolf, 1988; Wyn Jones, 1999).
In well-fertilized crops, the vacuolar K concentration can be high, in the order of 200 mM. Since the
vacuole occupies nearly 8090% of a mature plant
cell volume, it has most of the cell K in K-sufficient
plants, providing a K concentration similar to the
averaged whole cell (Pitman, 1981).
Growth responses of halophytes to Na under
saline conditions reflect the need for an osmoticum
during osmotic adjustment to salinity stress
(Flowers and Lauchli, 1983; Glenn et al., 1996). For
halophyte Salicornia herbaceae (Kawasaki et al.,
1978), both Na and K are effective in promoting
hypocotyl elongation. Potassium has only 87% of
the effect of Na in S. herbacea, although both ions
are effective in glycophytes, but at much lower concentrations (about 10 mM as opposed to 100 to
200 mM in halophytes). In halophytes, Na accumulation and its contribution to s reach a maximum (Glenn et al., 1996). There is evidence to
suggest that this reflects the ability of the tonoplast
in the leaf cells to restrict Na efflux from vacuoles
(Flowers et al., 1977; Yeo, 1981; Jeschke, 1984). In
Ricinus communis, K initially is the principal cation
contributing to vacuole and cell expansion; however, following maturation of the root tissues it can
subsequently be replaced by Na (Jeschke and Wolf,
1988).
Many halophytes osmotically compensate for
high external osmotic potential by accumulating Na
salts, often NaCl from the environment (Leigh and
Wyn Jones, 1986; Wyn Jones and Gorham, 1983a).
The required sap s of 2 MPa to 5 MPa to maintain turgor in halophytes under sea-water salinity
(s 2.3 MPa) can be accounted for by the 400
to 700 mM Na and Cl concentrations in the sap
(Flowers et al., 1977; Flowers, 1975). Many members of the Chenopodiaceae and many halophytes

show a marked selectivity for Na over K at even low

concentrations of both ions (Collander, 1941).
Biophysical functions of K in plant cells are
non-specific (Leigh and Wyn Jones, 1984), and Na
may at times be more suitable than K (Flowers and
Lauchli, 1983). Under limited K supply, Na, Mg
and Ca can replace K in the vacuole as an alternative inorganic osmoticum (Flowers and Lauchli,
1983). Our studies with red beet showed that Na
can replace K for vacuolar function, thus offsetting
nearly 95% of the plants K requirement (Table 3).
Compared to beet, spinach and lettuce showed a relatively lower ability to substitute Na for K (Subbarao
et al., unpublished results). It appears that Na can fill
the biophysical function of K, provided the plants
have the ability to take up Na, translocate it to the
shoot, and compartmentalize it in their vacuoles.
Many of the major metabolic processes, such
as protein synthesis, photosythesis, and glycolysis,
occur within the cytoplasmic compartment, which
places them in a protected location in respect to
the occurrence of high concentrations of Na found
in the vacuole (Leigh and Wyn Jones, 1986; Wyn
Jones, 1999). Solutes that accumulate in cytoplasm
could disrupt essential metabolism and they must
therefore be maintained at concentrations in the cytoplasm that permit the various processes to proceed at favorable rates. There is considerable evidence indicating that homeostasis mechanisms exist
in plants for regulating the cytoplasmic concentrations of a range of inorganic nutrients including K,
Na, H, and Pi (Smith and Raven, 1979; Wyn Jones
et al., 1979; Lee and Ratcliffe, 1983; Leigh and Wyn
Jones, 1984; Loughman and Ratcliffe, 1984; Wyn
Jones, 1999). For all eukaryotic organisms, the inorganic composition of cytoplasm appears to be highly
conserved during evolution. Despite wide variations
in the concentrations of K, Na, and Cl in the vacuolar compartment, the cytoplasm is characterized
by 100 to 200 mM K, with apparently relative little

399

potential for Na to substitute for K in the cytoplasm

(Leigh and Wyn Jones, 1986; Jeschke and Wolf,
1988; Wyn Jones, 1999).

2. Stomatal Function
In many plant species, K+ can be the dominant
cation responsible for turgor changes in guard cells
during ion induced stomatal movement (Marschner,
1995). An increase in the K concentration of guard
cells increases s and results in the uptake of water
from the adjacent cells. The corresponding increase
in turgor of the guard cells results in stomatal opening. Closure of stomata is correlated with K efflux
and a corresponding decrease in the s of the guard
cells. Selectivity of the plants ion transport systems
for K over Na provides a fundamental limitation on
the degree to which Na may be available to substitute for K in this stomatal function (Flowers and
Lauchli, 1983). Thus, although Na can often substitute for K in vacuolar osmotic adjustment, a parallel substitution of Na in the osmotic adjustment of
stomatal cells has yet to be clearly shown even in
halophytes (Humble and Hsiao, 1969; Hsiao, 1976;
Perera et al., 1997; Very et al., 1998). However, for
Commelina communis, Na was able to replace K and
was even more effective than K in stomatal function
(Raghavendra et al., 1976). Thus, Na may have a
functional role in the stomatal physiology of some
plants, even if it does not have an obligate metabolic
function (Evans and Sorger, 1966).
Based on the differences between plant species
with respect to membrane permeability for K and
Na, one might suppose that in plant species with high
permeability to Na (e.g. Beta vulgaris), K is at least
partially replaceable with Na in stomatal function
(Marschner, 1971). Thus, Na may function as the
osmoticum during stomatal opening even as it functions in the vacuole (Fujino, 1967; Fischer, 1968;
Humble and Hsiao, 1970; Thomas, 1970, Terry and
Ulrich, 1973a,b). This would be consistent with our
results on red beet, which showed that stomatal conductance is nearly normal even when nearly 95% of
the plants K was replaced by Na, and Na levels in
the leaf sap approached 200 mM (Subbarao et al.,
unpublished).

3. Photosynthesis
Potassium is the dominant counter-ion for the
light-induced H+ influx across the thylakoid membranes (Tester and Blatt, 1989) and for the estab-

400

lishment of the trans-membrane pH gradient necessary for the synthesis of ATP similar to ATP synthesis in mitochondria (Dilley and Vernon, 1965;
Rumberg et al., 1968; Wu et al., 1991). Also, the
formation of chloroplast structure, and the translocation of assimilates (sucrose) and storage in the
sink tissue seems to depend on adequate K concentrations in the tissue (Flowers and Lauchli,
1983).
In sugar beet, chloroplasts often contain high
concentrations of Na (Marschner, 1971), and Na is
incorporated into the chloroplasts to a similar extent as K (Mix and Marschner, 1974). Since Na in
sugar beet is concentrated in the chloroplasts, it is
hypothesized that Na may be involved in photosynthesis (Moscolov and Aleksandrovskaya, 1962). In
chloroplasts of Limonium vulgare, the Na content is
even higher than K. Considering the beneficial effect
of Na in Beta vulgaris, it is possible that Na participates in photophosphorylation (Marschner, 1971).
A prerequisite for this type of function is high membrane permeability for Na. The high mobility of Na
in crops such as sugar beet suggests that this prerequisite may be fulfilled. However, Na is unable to
replace K in chlorophyll synthesis in spinach, lettuce and sugar beet (Knypl and Chylinska, 1972;
Marschner and Possingham, 1975). For sugar beet,
Na was able to replace K for chloroplast multiplication (Marschner, 1971). Nevertheless, photosynthetic rates of sugar beet declined substantially during K deficiency, even when Na was present (Terry
and Ulrich, 1973a,b). In contrast, leaf photosynthetic rates were nearly normal despite very high levels of Na and low levels of K in the leaf lamina of red
beet (up to 100 g kg1 dwt) (Subbarao et al., 1999a).
Chlorophyll fluorescence and leaf Na levels are presented for red beet, spinach and lettuce (Table 4). For
red beet, leaf chlorophyll levels and chlorophyll fluorescence (Fv /Fm ) are not affected at tissue Na concentrations of 76 g kg1 dwt (Table 4). In contrast,
in lettuce chlorophyll fluorescence is decreased significantly when leaf Na levels reach 39.8 g kg1 dwt
(Table 4).

4. Counter-Ion in Long-Distance
Transport
Potassium is often the dominant counter-ion
in long-distance transport, as well as being the
dominant counter-ion in vacuoles with high NO
3
(Marschner, 1995). As a consequence of NO3
metabolism in leaves, the remaining counter-ion
K requires the stoichiometric synthesis of organic

TABLE 4
Leaf Na Levels and Chlorophyll Fluorescence in Red Beet, Spinach and Lettuce.
Red Beets were Grown for 42 Days, and Spinach and Lettuce were Grown for
30 Days Using Nutrient-Film Technique where K and Na Levels at 0.25 and 4.75
mM Respectively. (Source: Subbarao and Wheeler, Unpublished)
Plant species
Red beet
(Beta vulgaris)
Spinach
(Spinacea oleracea)
Lettuce
(Lactuca sativa)

Leaf Na concentration
(g kg1 dwt)

Chlorophyll fluorescence
(Fv /Fm ) ratio

76.0

0.74

28.9

0.75

39.8

0.69

Note: Fv /Fm ratio under control conditions (i.e. plants grown at 5.0 mM K and no Na) are: 0.76 for red
beet, 0.81 for spinach, 0.79 for lettuce.

acids (e.g., malate) to maintain charge balance and

pH homeostasis. The newly formed K-malate can
then be retranslocated to the roots for subsequent
reutilization of K as a counter-ion for NO3 transport.
The high mobility of K in the phloem and its continuous circulation within the plant are indications of
a special function for K in the long-distance transport processes of higher plants (Marschner, 1971;
Kirkby et al., 1981). This function of K as a counterion in long-distance transport may not be specific
and other cations might be able to replace K in
this function, provided they are phloem mobile. For
many crops, e.g. maize, Na is not phloem mobile
(Marschner, 1971). But in crops such as sugar beet,
Na is reported to be phloem mobile, thus Na could
potentially be as effective as K for the long-distance
transport functions (Marschner, 1971). Our studies
with red beet indicate that NO3 levels in the shoot
were not affected by large drops in the plants tissue K concentration (concentrations below the normally accepted critical level for that tissue) when
Na was available as an alternative cation (Subbarao
et al., 1999a, 2000b). This suggests that in red beet,
Na may be able to replace K in this function. Replacing most of the plants normal level of K with
Na (>90% replacement) resulted in elevated levels
of NO3 in leaves of red beets, spinach and lettuce
(Subbarao et al., unpublished). Such an elevation of
nitrate is consistent with the reported requirement
of nitrate reductase for K as its activator (Suelter, 1970; Pfluger and Wiedemann, 1977). Also,
this shows that Na was unable to replace this Kfunction (i.e. nitrate reductase activation) even in red
beet.

5. Enzyme Activation
Potassium has a number of direct metabolic
roles within the cytoplasm (Clarkson and Hanson,
1980; Marschner, 1995). Many of the enzymes activated by K are frequently maximized at 100 mM,
which is about the same concentration range of K
that is normally found in cytoplasm (Evans and
Sorger, 1966). Potassium ions have an important
role in protein and starch synthesis (Wyn Jones et al.,
1979), as well as in respiratory and photosynthetic
metabolism (Lauchli and Pfluger, 1979). Sodium is
also functional, but generally less effective in activating these enzymes (Wyn Jones et al., 1979). Regardless of the large fluctuations of K levels in the
vacuole compartment, it seems that plant cells are
able to maintain cytoplasmic K levels in the range
of 100 to 200 mM (Hsiao and Lauchli, 1986). Cytoplasmic K levels are thought to change only under
severe K deficiency after the vacuolar K pools have
been exhausted. Thus the cytoplasm K concentration is well buffered against change by the large
vacuolar pool of K. Because of the high degree of
K homeostasis found in the cytoplasm, it is likely
that many metabolic processes and enzymatic reactions found there might have a specific requirement
for K.
Protein synthesis (Hall and Flowers, 1973; Wyn
Jones, et al., 1979) and oxidative phosphorylation
(Flowers, 1974) are both equally inhibited by high
Na in vitro, regardless of whether the organelles are
isolated from glycophytes or halophytes (Greenway
and Osmond, 1972). Starch synthetase has a requirement of about 50 mM K for normal activity (Nitsos

401

and Evans, 1969). Other monovalent cations such

as Rb, Cs and NH4 are about 80% as effective as
K, while Na is only about 20% as effective at maintaining starch synthetase activity (Nitsos and Evans,
1969). Several reports indicate that K is needed
for the normal functioning of starch synthetase in
sweet potato, taro, white potato, wheat, bush beans,
field corn, soybeans, peas, and rice (Akatsuka and
Nelson, 1966; Nigam and Fridland, 1967; Preiss
and Greenberg, 1967; Murata and Akazawa, 1968).
Sodium seems unable to replace K in this function;
even in sugar beet, K deficiency can cause the accumulation of soluble carbohydrates and reducing sugars due to the inhibition of starch synthesis (Evans
and Sorger, 1966). Glucose transport across the plasmalemma of sugar beet storage cell protoplasts is
faster in the presence of KCl than in the presence
of NaCl (Willenbrink et al., 1984). Sodium, however, is more effective in catalyzing the transport
of sucrose across the tonoplast into the vacuole and
in stimulating sucrose accumulation in the storage
tissue (Willenbrink et al., 1984). This effect of Na
on sucrose storage seems to be related to the stimulation of ATPase activity at the tonoplast of beet
storage cells (Willenbrink et al., 1984; Marschner,
1995).
Vacuolar ATPase is substrate specific and Mg
dependent, and is distinguished from non-specific
phosphatase (Wagner, 1982). Beet root ATPase is
stimulated by both Na and K ions. High ATPase activity in sugar beet and Avicennia roots is obtained
with combinations of K and Na, but not with either K
or Na alone (Hanson and Kylin, 1969). This agrees
with observations that sugar beet growth is greatest when both Na and K are present in the growing
medium. Green and Taylor (1964) proposed that ATPase activation requires two binding sites, one for
K and one for Na, and that maximum activation is
obtained only when both sites are occupied. In vitro
studies on the effect of high concentrations of KCl
and NaCl on ATPases noted differences between
genotypes and suggested differences in cellular localization of K+ and Na (Kylin and Hansson, 1971;
Hanson, 1975).
Using isolated mitochondria from Brassica
rapa, it was shown that the esterification of phosphate and PO4 /O2 ratio were increased more by
Na than K (Shah and Wedding, 1968). But it is
unclear that such an increase in the rate of phosphate metabolism was linked with the formation
of complexes with ATP. It is also unclear if an increased rate of phosphate metabolism is even desirable in terms of overall plant growth. For example, Na was able to form stable complexes with

402

polyphosphates (Lamm and Malmgren, 1940), but

the effect of Na on enzymatic activity of pyruvic
kinase is small in comparison to K (Marschner,
1971). Also, Na was not effective in activating acetic
thiokinase from spinach leaves (Hiatt and Evans,
1960).
The existence of isozymes has not been fully
considered when evaluating the ability of Na to replace K. In rice, four isozymes of malic dehydrogenase are reported (Rocha and Ting, 1970) and several isozymes of alpha-amylase have been isolated
from seeds (Tanaka et al., 1970). These isozymes
may have different ionic requirements for full functionality and they may differ in their ability to function with Na as an alternative to K (Marschner,
1971).

VI. GROWTH STIMULATION

BY SODIUM
Growth stimulation by Na has both practical
and scientific interest, as it raises the possibility
of utilizing inexpensive, low-grade Na fertilizers
(Marschner, 1995). Numerous reports suggest that
Na has beneficial effects on the growth (Williams,
1960; Montasir et al., 1966; El-Sheikh et al., 1967;
Hylton et al., 1967; Draycott and Durrant, 1976;
Galeev, 1990; Takahashi and Maejima, 1998). This
stimulation is particularly apparent in the Chenopodiaceae. In the case of sugar beet, red beet, and
spinach, Na stimulated growth even when there
appeared to be adequate K present in the system
(Larson and Pierre, 1953; Lehr and Wybenga,
1955; Tinker, 1965; El-Sheikh et al., 1967; Jeschke,
1977a,b; Milford et al., 1977; Nunes et al., 1984;
Pessarakli and Tucker, 1985; Peck et al., 1987;
Haneklaus et al., 1998). Many field experiments
showed that Na fertilization improves the growth
and yield of sugar beet and fodder beet (Milford
et al., 1977; Flowers and Lauchli, 1983; Magat
and Goh, 1990; Marschner, 1995; Haneklaus et al.,
1998). However, the extent of the positive effects
varied with cultivar, soil type, and climatic conditions (Draycott et al., 1970; Judel and Kuhn, 1975;
Draycott and Durrant, 1976; Durrant et al., 1978;
Draycott and Bugg, 1982). Our studies with red
beet showed that maximum growth occurred when
both Na and K were present rather than the just
K alone (Subbarao et al., 1999a). Also, genotypic
differences were observed for the optimum ratio
of K and Na in the nutrient medium with some
genotypes appearing to prefer higher levels of Na
(Fig. 1). In contrast to the findings of others, we

FIGURE 1. Growth response of two red beet

varieties to substitution of Na for K in the nutrient medium. Plants were harvested at 42 days
after sowing (Subbarao et al., 1999).
observed no such growth stimulation in spinach with
Na (Fig. 2).
Among non-chenopods, tomato has been reported to respond positively to additional Na
(Wooley, 1957). For example a 12% increase in dry
weight of tomato occurred following the addition
of 1 mM NaCl to the nutrient medium (Wooley,
1957). Sodium alleviated K-deficiency symptoms
and decreased the critical foliar K concentration at
which K-deficiency symptoms appeared (Besford,
1978). Also, there is some evidence to show that
potato responds positively to Na. Based on a series of field trials on sandy soils it was shown that
Na application improved potato yields of up to 6%
for plots where adequate K was given, and nearly
10% in plots where K fertilization was not given
(Lehr, 1953; Galeev, 1990). Barley, oats, and carrots showed positive responses to supplemental Na
at low K levels (Harmer and Benne, 1945; Troug

et al., 1953; Montasir et al., 1966), while alfalfa, flax,

celery, and flax showed moderate response to Na at
adequate levels of K (Troug et al., 1953; Montasir
et al., 1966).
For some crops, Na has been reported to improve the quality of the product. Although improved
crop quality may not be directly related to either essentiality or a functional nutrient requirement, it
does demonstrate that some of the metabolic effects
of Na can have a practical value. It is also possible
that it could be argued that crop quality as well as
biomass yield could be considered in establishing
an element as a functional nutrient, but presently
such an argument is much less compelling than it
is for biomass yield. For celery, Na improved resistance to blight (Septoria petroselini appli) and tissue crispiness and thus market value (Pardossi et al.,
1999). Also, taste tests demonstrated that addition
of Na tends to reduce a strong celery flavor (i.e., improve the flavor) (Harmer and Benne, 1945; Lehr,
1953). Sodium can also improve the taste of carrots
by increasing the sweetness (Lehr, 1953; Hanson
et al., 1997). In forage crops, several studies indicate that Na fertilization improves the fodder quality
and increases milk yields in dairy cows (Chiy, 1991;
Sinclair et al., 1993; Wesselmann et al., 1993;
Boberfeld et al., 1999; Chiy and Philips, 1999).

VII. SODIUM AND POTASSIUM

INTERACTIONS
Crops vary widely in their ability to utilize Na
as an alternative nutrient to K for their metabolic requirements (Harmer and Benne, 1945; Harmer et al.,
1953). Crops that have halophytic ancestors or crops
that have evolved near the sea typically have a high
potential to use Na as an alternate for much of their
K requirements. The following list of plants with
high Na/K substitution capabilities and their origins
illustrates this phenomenon:

r Beetsevolved in sandy soils near the sea in the

FIGURE 2. Growth response of two spinach

cultivars to substitution of Na for K in the nutrient medium. Plants were harvested at 42 days
after sowing. (Source: Subbarao et al., unpublished data).

Canary Isles, Persia, Babylon, and Western India

(Harmer and Benne, 1945).
r Cabbagefound in rocky coastlines (cited in
Harmer and Benne, 1945) on the Isle of Laland
in Denmark, the island of Heligoland, the south
of England and Ireland, the Channel Isles, islands off the Coast of Charente Inferceure, on the
north coast of Mediterranean near Nice, Genoa
and Lucca (Collander, 1941).

403

TABLE 5
Effect of Sodium Applied as a Nutrient on Several Crops (Source: Harmer and
Benne, 1945; a Devi and Padmaja, 1996; b Sharma and Singh, 1990)
Degree of benefit in deficiency of K

Degree of benefit in sufficiency of K

None to slight
group I

Slight to medium
group II

Slight to medium
group III

Large
group IV

Buckwheat
Corn
Lettuce
Onion
Parsley
Parsnip
Peppermint
Potato
Rye
Soybean
Spinach
Squash
Strawberry
Sunflowers
White bean

Asparagus
Barley
Broccoli
Brussels sprouts
Caraway
Carrot
Cauliflowerb
Chicory
Cotton
Flax
Millet
Oat
Pea
Rutabaga
Tomato
Vetch
Wheat

Cabbage
Celeriac
Cassavaa
Horseradish
Kale
Kohlrabi
Mustard
Radish
Rape

Celery
Mangel
Sugarbeet
Swiss chard
Red beet
Turnip

r Horseradishknown in Holland as sea-radish,

grows wild in the salty soils in the east of Russia.
r Turnipcommon in the sand on the seacoast in
Sweden, Holland and England
r Celeryin damp places from Sweden to Algeria, Egypt, Absynnia and in Asia (Harmer and
Benne, 1945).

thus tissue K with Na (Table 5). The largest potential

for replacing K with Na lies in group-3 and group-4
plants (Table 5). Based on known levels of tolerance
to external Na, and the extent of Na translocation to
the shoot and other edible plant parts, we have estimated the amount of tissue K in these plant parts that
can potentially be replaced by Na with only minimal
effects on growth (Table 6).

In addition to variation between species, the

uptake of Na can vary between genotypes of the
same species, such as sugar beet (Marschner et al.,
1981a,b), celery (Harmer, 1943), red beet (Subbarao
et al., 1999a) and tomato (Rush and Epstein, 1981).

B. Influence of Sodium on Critical

Potassium Levels

A. Sodium Replacement
of Potassium
In general, crop plants can be classified into
four Na response groups (Table 5) (Richards, 1954).
Plants that discriminate less against Na during uptake are likely to have a greater ability to utilize
Na to fill their monovalent cation requirements.
Group-1 plants that do not respond favorably
to Na even under K deficiency have little potential for utilizing Na (Table 5). For group-2
plants, there is a slight potential (about 10%) for
replacing some K with Na in certain functions, and

404

The presence of Na in the environment and its

uptake by plants can reduce the amount of K required to meet the plants basic metabolic requirements. Thus, in the presence of Na, the critical level
of K can be reduced (the lowest tissue K level at
which 95% of the maximum yield can be achieved)
(Greenwood and Stone, 1998). For crops that have
a capacity to substitute Na for K, the critical level
for K is reduced as a function of the Na supply.
For red beet, K levels of leaf tissues can drop from
100 g kg1 dwt (leaf tissue with high availability
of K) to 4 g kg1 dwt when K availability is low
and high levels of Na are provided (Subbarao et al.,
1999a, 2000b). This decrease in leaf K occurred
without any observable short-term effect on growth,

TABLE 6
Concentrations of K in the Edible Portions of Some Crops and Estimates of Na
Replacement (Source: Subbarao et al., 2000a)

Crop

K (%) in edible
plant part

Red beet
Chard
Celery
Lettuce
Spinach
Radish
Tomato
Potato
Sweet potato
Wheat
Soybean
Rice
Peanut

10
10
10
10
9
9
5
2.5
2.5
0.5
1.7
0.2
0.7

90
90
75
25
50
25
25
40
40
1
1
1
1

% of K replaced
with Na (estimate)

Based on studies at Kennedy Space Center, USA.

Source: Duke and Atchley (1986).

Estimations based on our experience with some of the above crops and other published sources.

suggesting that 4 g kg1 dwt may be approaching

the critical level for K in these tissues. Other plants
seem to have a higher specific K requirement, but
this may in part be a result of limitations in Na uptake and translocation rather than the direct ability
to utilize Na. These critical K levels were about 30
g kg1 dwt for spinach and 65 g kg1 dwt for lettuce (Fig. 3). In red beet, leaf Na levels can reach
100 g kg1 dwt without negative effects on growth
rates, whereas for spinach it was 17 g kg1 dwt, and
for lettuce it was 4.9 g kg1 dwt (Fig. 4). For Rhodes
grass, the critical leaf K levels are progressively reFIGURE 4. Leaf Na levels and total dry matter
production (expressed as % of control) for red
beet, spinach, and lettuce for the same tissues
shown in Fig. 3.

FIGURE 3. Leaf K levels of red beet, spinach

and lettuce in presence of adequate levels of
Na (>1 mM) in the nutrient medium (Source:
Subbarao et al., unpublished data).

duced from 27 g kg1 dwt in plants not fertilized

with Na to 5 g kg1 dwt in plants receiving 400 mg
Na pot1 (Smith, 1974).
It is suggested that as total tissue K concentration declines, the cytoplasm maintains a homeostasis concentration of K to maintain K-dependent
processes (Leigh and Wyn Jones, 1986; Wyn Jones,
1999). Therefore, initial changes in tissue K concentrations are likely to be at the expense of vacuolar K, with other solutes being diverted to the
vacuole to maintain s (Wyn Jones, 1999). Leigh
and Wyn Jones (1984) argue that cytoplasmic K

405

concentration would be expected to decline below

15 g kg1 dwt, which is consistent with the values
of critical K concentrations of 5 to 20 g kg1 dwt
reported for various tissues in a number of crops.
When other cations (e.g., Na and Mg) are abundant
in tissue, critical K concentrations range from 10 to
20 g kg1 dwt, but when they are low, critical K values can increase up to 40 to 70 g kg1 dwt, depending on the species (Hylton et al., 1967; Smith et al.,
1982). For Italian ryegrass, the leaf K critical level
decreases from 35 g kg1 dwt to 8 g kg1 dwt when
Na is provided as an alternate ion (Hylton et al.,
1967). For fodder beet, sugar beet, red beet, oats,
barley, ryegrass, English ryegrass, turnips, lupins,
red and white clover, potatoes, kale and rapeseed,
the critical K levels are lower when Na is supplied (Lehr, 1953; Marschner, 1971; Subbarao et al.,
1999a).

VIII. SODIUM, OTHER

PERSPECTIVES
A. Sodium Tissue Levels
Regardless of Na supply, most crops translocate very little Na to reproductive or storage structures such as seeds, fruits, or storage roots, which
comprise the edible portions of many staple crops
(Watt and Merrill, 1975). This is the case for cereals
such as wheat and rice, fruit crops such as tomatoes,
and tubers such as potatoes, and roots such as sweet
potato. The main reason for this low Na concentration in the reproductive or storage organs appears to
be that they are fed mostly through phloem, where
there is a considerable discrimination against Natranslocation.
In contrast, vegetative structures maintained
primarily by xylem flow tend to be higher in Na.
Under environmental conditions where there are relatively high concentrations of Na compared to K
in the nutrient supply, it is possible for some leafy
crops to accumulate Na in leaves at reasonably high
levels without adversely affecting productivity or
crop quality. This phenomenon of using Na as an
alternative mineral nutrient in leaf tissue could have
a practical application for some greenhouse crops
like lettuce or spinach, where a significant portion
of the applied K fertilizers could be replaced with
relatively inexpensive Na salts. This also applies
to field crops like beets, celery, and radish, where
there is a large potential to replace K with Na. In
ecological or production systems where high tissue
Na is required, Na levels in the plant tissues can

406

be enhanced by limiting the availability of K in the

presence of readily available Na (Subbarao et al.,
1999a,b, 2000a).

B. Genetic Variation in Tissue

Sodium
As noted previously, there are genotypic
differences within species for Na uptake and
partitioning to edible structures, viz., sugar beet,
red beet and celery. Some wild relatives of the
cultivated tomato translocate substantially higher
than normal levels of Na to the fruits (Shannon,
personal communication). Some of the tomato
lines derived from crosses of these wild relatives
accumulate a level of Na nearly 10 times higher in
the fruits than the cultivated tomato growing under
identical conditions (Fig. 5).
There are considerable differences among forage species in the contents of Na in their shoots, even
when the supplies to their roots are similar (Griffith
and Walters, 1966; Smith et al., 1980; Guan et al.,
1997; WenHua et al., 1998). Such differences could
be due to selectivity during absorption (Smith et al.,
1980) or to differences in transport to shoots (Shone
et al., 1969). Identification and testing of germplasm
adapted to low K and high Na conditions could be
useful in understanding the physiological roles of
monovalent cations as well as in providing breeding materials for forage production on soils low in
K, especially where K fertilizers may be costly or
unavailable (Jarvis, 1982).
Generally, Na levels in forage grasses are inadequate to meet the nutritional requirements of
herbivores for Na without supplementation from
either natural or supplied salt licks (Garcia et al.,
1990). The electrolyte balance in animals is based
primarily on Na while that of plants is based primarily on K. Thus the animal requirement for Na
generally exceeds that of plants. This discrepancy
in the Na requirement between plants and animals
must be considered in maintaining biological systems, especially in small limited systems. Thus, Na
cycling in livestock pasture systems can be a real
practical consideration in maintaining the health of
the overall system. Genetic selection for high tolerance to salinity has been shown to increase tissue
Na levels in some forage grasses such as Lolium
perenne. Increases in the overall Na content of forage and pasture crops is important in animal nutrition (Marschner, 1995; Rajcevic et al., 1995), as
shown by the fact that Na fertilization improves
forage quality (Sinclair et al., 1993; Wesselmann

FIGURE 5. Sodium levels of tomato fruits derived from the crosses between L. esculentum X L .
cheesmani (Source: M. Shannon, unpublished data from USDA Salinity Laboratory, Riverside).
et al., 1993; Chiy and Philips, 1999; Boberfeld et al.,
1999). Sodium fertilization has improved the fodder quality in ryegrass as expressed through improved digestibility and water-soluble carbohydrate
concentration (Chiy and Phillips, 1998; Chiy et al.,
1998). The Na requirements for lactating dairy cows
is approximately 2 g kg1 dwt in forage (Smith
and Middleton, 1978), which is higher than the average Na content of natrophobic pasture species
(Smith et al., 1980). In contrast, the K content (20
to 25 g kg1 dwt) in natrophobic species is usually
adequate or in excess of animal needs. A higher than
average Na content can increase the acceptability of
forage to animals and can enhance their daily nutrient intake (Ziegler, 1975).

C. Closed Life Support Systems

for Space
Advanced Life Support Systems (ALSS) being studied for space travel must ultimately strive
for self-sufficiency in providing food, potable water, and a breathable atmosphere for humans. Such
closed life support systems could form the basis
for human colonies on the lunar or Martian surface (MacElroy and Bredt, 1985). Bio-regenerative
components of such systems would use plants to
regenerate oxygen, food and clean water through
photosynthesis and transpiration. However, to minimize re-supply costs, all the systems waste products
need to be recycled to provide a continuous nutrient

supply for sustained plant production. For example, non-edible plant biomass could be processed in
bioreactors with the effluent nutrients recycled to the
food production systems (Mackowiak et al., 1997;
Garland et al., 1993; Mackowiak et al., 1996a,b).
Human wastes (both solid and liquid) could also be
processed as a source of nutrient and water inputs. If
the nutrient requirements of both plants and humans
were in the same proportion, then nutrient cycling
from one component to another would not be a problem. However, some elements such as Na are needed
in relatively high levels for human metabolism, but
are only absorbed and utilized by plants in limited
amounts. This discrepancy in Na utilization between
humans and plants could pose a threat to the systems long-term equilibrium because of incomplete
cycling or the addition of external (imported) Na to
meet the metabolic requirements of humans (Fig. 6).
In a functional bio-regenerative system, human
urine would be one of the waste products recycled
back to the plant production system as a source of
water and nutrients, especially N. Nearly 900 mmol
of N person1 day1 are excreted in urine by humans who eat a typical Western diet (Putnam, 1972).
But this same volume of urine would also contain
nearly 180 mmol of Na (Putnam, 1972). Thus, Na inputs from human liquid wastes (which include urine,
gray water, etc.) could amount to nearly 200 mmol
per person day1 . Assuming a nutrient solution volume of 17 L per m2 for a hydroponic crop production system providing the estimated required 40 m2
growing area person1 (Wheeler et al., 1999), Na

407

FIGURE 6. Some considerations for Na flows

in closed systems in space where crops might
be used for life support.
inputs from waste recycling could lead to a 0.28 mM
increase in Na concentration per day (Subbarao
et al., 1999b, 2000a). If plants fail to remove this
Na and recycle it to the crews through the food
chain, Na concentrations could reach 100 mM in
the nutrient solutions within one year just from
the urine input alone; this increase in salinity (a
high tech form of secondary salinization) would
kill most crops, resulting in a collapse of the food
production system (Subbarao et al., 1999b, 2000a).
Thus, appropriate nutrient management approaches,
coupled with crop selection strategies, are required
to manage the cycling of Na between humans
and plants in tightly closed systems. One possible approach to this problem would involve getting Na into the edible portions of the crops, which
would remove Na from the recycled material and
recycle it to the humans through the food loop.
The ultimate goal in any such recycling approach
would be to eliminate any external supply of Na
(Fig. 6).

the productivity potential of biological systems. In

spite of decades of research, the full role of Na in
plant metabolism remains unresolved. Much of the
indecision in regard to the sodiums role in plant
nutrition is because it does not fit neatly into any of
the categories used to describe the essential mineral
nutrients. The determination of Na to be an essential
nutrient under the Arnon and Stout (1939) definition
has been established only for a few C4 plants, but
as of now not for many higher plants. All the other
accepted essential mineral nutrients seem to be required across the board by all higher plants. However, numerous reports indicate a significant stimulation in the growth of many crops in response to
Na, even under conditions of K-sufficiency. There
also is convincing evidence that Na can substitute
for K in non-specific functions, such as being an osmoticum during cell enlargement and as a counterion during long-distance transport. The significance
of the role of Na is also shown by the fact that the
critical level of K is reduced in the presence of Na
in many crops. In the above roles, Na influences
plant growth in a very significant way both as to
growth rate and in efficient nutrient resource utilization. The functional role of Na in plant nutrition can
be large, multi-faceted and of critical importance in
both natural bio-systems and controlled plant production systems. Clearly Na plays a unique role in
plant nutrition that does not fit neatly in the classification put forward by Arnon and Stout for essentiality, but does significantly influence plant growth
in many environments. Therefore, there needs to be
a category to designate such a role. The term functional nutrient, defined as a nutrient being required
for maximal biomass yield and/or is functional in a
metabolic role to the extent that the critical level
of an essential nutrient is reduced, is proposed.
Thus, mineral nutrients would be composed of two
classes, essential mineral nutrients and functional mineral nutrients. We feel that Na clearly
fits into such a classification as a functional mineral
nutrient.

IX. CONCLUDING REMARKS

Sodium cycling through plants and the overall
environment can be a critical factor influencing the
productivity of biological systems. Not only does
the selectivity of plant uptake for K over Na impact the salt balance of herbivores; it is also a major
contributing factor to the secondary salinization of
many soil systems. Thus, the knowledge of how Na
is utilized and cycled through plants and the environment is critical in understanding and managing

408

ACKNOWLEDGMENTS
We would like to thank Dr. William Knott,
Biomedical Office, Kennedy Space Center for the
support and encouragement for this project. This
research was in part supported through National Research Council and NASAs Life Support Contract
(NAS 10-20701).

REFERENCES
Akatsuka, T., and Nelson, O. E. 1966. Granule
bound adenosine diphosphate glucose-starch glucosyl transferase of maize seeds. J. Biol. Chem.
241:22802286.
Alekseev, A. M., and Abdurakhamanov, A. A. 1966. On
the influence of ions of mineral nutrient salts on the
state of the protoplasm of plant cells. Fiziol. Rast.
13:414419.
Amtmann, A., and Sanders, D. 1999. Mechanisms of
Na+ uptake by plant cells. Adv. Bot. Res. 29:75
112.
Ando, T., and Oguchi, Y. 1990. A possible role of
sodium in chlorophyll biosynthesis of sodiumrequiring C4 plants. In: Transactions 14th International Congress of Soil Science, Kyoto, Japan,
August 1990, vol. IV.
Arnon, D. I., and Stout, P. R. 1939. The essentiality of
certain elements in minute quantity for plants with
special reference to copper. Plant Physiol. 14:371
375.
Barbier, G., and Chabannes, J. 1951. Accumulation du
sodium dans les racines des plantes. Comptes R.
Acad. Sci. 232:13721374.
Besford, R. T. 1978. Effect of replacing nutrient potassium
by sodium on uptake and distribution of sodium in
tomato plants. Plant Soil 50:399409.
Blumwald, E., Aharon, G. S., and Apse, M. P. 2000.
Sodium transport in plant cells. Biochem. Biophys.
Acta 1465:140151.
Boberfeld, W. O., von Schlosser, M., and Laser, H. 1999.
Effect of Na amounts on forage quality and feed
consumption on Lolium perenne depending on
fertilizer and nutrient ratio. Agribiological Res.
52:261270.
Brownell, P. F., and Wood, J. G. 1957. Sodium as an essential micronutrient element for Atriplex vesicaria
Heward. Nature 179:365366.
Brownell, P. F., and Jackman, M. E. 1966. Changes during
recovery from sodium deficiency in Atriplex. Plant
Physiol. 41:617622.

by K+ starvation in wheat root cells. Plant Physiol.

122:13871397.
Cheeseman, J. M. 1988. Mechanisms of salinity tolerance
in plants. Plant Physiol. 87:547550.
Chiy, P. 1991. Sodium fertilizers lift milk yields. Milk
Producer 38:14.
Chiy, P. C., and Phillips, C. J. C. 1998. Sodium fertilizer application to pasture. 6. Effects of combined
application with sulfur on herbage production and
chemical composition in the season of application.
Grass and Forage Sci. 53:110.
Chiy, P. C., Al-Tulihan, A. L. A., Hassan, M. H., and
Phillips, C. J. C. 1998. Effects of sodium and potassium fertilizers on the composition of herbage and
its acceptability to dairy cows. J. Sci. Food Agric.
76:289297.
Chiy, P. C., and Phillips, C. J. C. 1999. Sodium fertilizer
application to pasture. 8. Turnover and defoliation
of leaf tissue. Grass and Forage Sci. 54:297311.
Clarkson, D. T., and Hanson, J. B. 1980. The mineral
nutrition of higher plants. Ann. Rev. Plant Physiol.
31:239298.
Collander, R. 1941. Selective absorption of cations by
higher plants. Plant Physiol. 16:691720.
Cram, W. J. 1976. Negative feedback regulation of transport in cells. The maintenance of turgor, volume
and nutrient supply. In: Encyclopedia of Plant
Physiology, new edition vol. 2A, Transport in Plant
Cells, pp. 284316, Luttge, U. and Pitman, M. G.,
eds., Springer Verlag, Berlin.
Devi, C. R. S., and Padmaja, P. 1996. Effects of partial
substitution of muriate of potash by common salt
on the tuber quality parameters of cassava. J. Root
Crops 22:2327.
Dilley, R. A., and Vernon, L. P. 1965. Ion and water transport processes related to light-dependent shrinkage
of spinach chloroplasts. Arch. Biochem. Biophys.
111:365375.
Draycott, A. P., Marsh, J. A. P., and Tinker, P. B. H. 1970.
Sodium and potassium relationships in sugar beet.
J. Agric. Sci. (Camb) 74:568573.

Brownell, P. F., and Crossland, C. J. 1972. The requirements of sodium as a micronutrient by species having the C4 dicarboxylic photosynthetic pathway.
Plant Physiol. 49:794797.

Draycott, A. P., and Durrant, M. J. 1976. Response by

sugar beet to potassium and sodium fertilizers,
particularly in relation to soils containing little
exchangeable potassium. J. Agric. Sci. (Camb)
87:105112.

Buschmann, P. H., Rama Vaidyanathan Gassmann, W.,

and Schroeder, J. I. 2000. Enhancement of Na+
uptake currents, time-dependent inward-rectifying
K+ channel currents, and K+ channel transcripts

Draycott, A. P., and Bugg, S. M. 1982. Response by sugarbeet to various amounts and times of application
of sodium chloride fertilizer in relation to soil type.
J. Agric. Sci. 98:579592.

409

Duke, J. A., and Atchley, A. A. 1986. CRC Handbook of

Proximate Analysis Tables of Higher Plants. CRC
Press Inc., Boca Raton, Florida.
Durrant, M. J., Draycott, A. P., and Milford, G. F. J. 1978.
Effect of sodium fertilizer on water status and yield
of sugar beet. Ann. Appl. Biol. 88:321328.
El-Sheikh, A. M., Ulrich, A., and Broyer, T. C. 1967.
Sodium and rubidium as possible nutrients for
sugar beet plants. Plant Physiol. 42:12021208.
Epstein, E. 1961. The essential role of calcium in selective cation transport by plant cells. Plant Physiol.
36:437444.
Epstein, E., Rains, D. W., and Elzam, O. E. 1963. Resolution of dual mechanisms of potassium absorption
by barley roots. Proc. Nat. Acad. Sci. USA 49:684
692.
Epstein, E. 1965. Mineral metabolism. In: Plant Biochemistry, pp. 438466, Bonner, J. and Varner, J. E., eds.,
Academic Press, New York.

Garcia, A., Rodriguez, B., and Garcia, B. 1990. Mineral nutrients in pasture herbage of central
western Spain. In: Soil-grassland-animal relationships. Proceedings of 13th general meeting
of the European Grassland Federation, Banska
Bystrica, Czechoslovakia, June 2529, 1990,
vol. 2. Gaborcik, N., Krajcovic, V., and Zimkova,
M., eds., Czechoslovakia.
Garland, J. L., Mackowiak, C. L., and Sager, J. C. 1993.
Hydroponic crop production using recycled nutrients from inedible crop residues. SAE Tech. Paper
932173.
Gassmann, W., and Schroeder, J. I. 1994. Inwardrectifying K+ channel currents in root hairs
of wheat: A mechanism for aluminumsensitive low-affinity K+ uptake and membrane potential control. Plant Physiol. 105:1399
1408.

Evans, H. J., and Sorger, G. J. 1966. Role of mineral

elements with emphasis on the univalent cations.
Annu. Rev. Plant Physiol. 17:4776.

Gibson, T. S., Spiers, J., and Brady, C. J. 1984. Salttolerance in plants. II. In vitro translation of mRNAs from salt-tolerant and salt-sensitive plants
on wheat germ ribosomes. Responses to ions and
compatible organic solutes. Plant Cell Env. 7:579
587.

Findlay, G. P., Tyerman, S. D., Garrill, A., and Skerrett,

M. 1994. Pump and K+ inward rectifiers in the
plasmalemma of wheat root protoplasts. J. Membr.
Biol. 139:103116.

Glenn, E. P., Fister, R. P., Brown, J. J., Thompson, T. L.,

and OLeary, J. 1996. Na and K accumulation and
salt tolerance of Atriplex canescens (Chenopodiaceae) genotypes. Am. J. Bot. 83:9971005.

Fischer, R. A. 1968. Stomatal opening: Role of potassium

uptake by guard cells. Science 160:784785.

Glenn, E. P., Brown, J. J., and Blumwald, E. 1999. Salt

tolerance and crop potential of halophytes. Crit.
Rev. Plant Sci. 18:227255.

Flowers, T. J. 1974. Salt tolerance in Suaeda maritima

(L) Dum. A comparison of mitochondria isolated
from green tissues of Suaeda and Pisum. J. Exp.
Bot. 101:101110.
Flowers, T. J., Troke, P. F., and Yeo, A. R. 1977. The
mechanism of salt tolerance in halophytes. Annu.
Rev. Plant Physiol. 28:89121.
Flowers, T. J., and Lauchli, A. 1983. Sodium versus
potassium: Substitution and compartmentation. In:
Encyclopedia of Plant Physiology, new series,
vol. 15B, pp. 651681, Pirson, A. and Zimmermann, M. H., eds., Springer-Verlag, Berlin.
Flowers, T. J., and Yeo, A. R. 1988. Ion relations of salt
tolerance. In: Solute Transport in Plant Cells and
Tissues, pp. 392416, Baker, D. A. and Hall, J. L.,
eds., Longman, New York.
Fujino, M. 1967. Role of adenosine triphosphate and
adenosine triphosphatase in stomatal movement.
Sci. Bull. Fac. Educ. Nagasaki Univ. 18:147.
Galeev, R. R. 1990. Application of sodium humate to potatoes. Kartofel I Ovoshchi No. 2:1213.

410

Goldschmidt, V. M. 1954. Geochemistry. Clarendon

Press, Oxford.
Green, A. L., and Taylor, C. B. 1964. Kinetics of (Na + K)
stimulated adenosine triphosphatase (ATPase) of
rabbit kidney microsome. Biochem. Biophys. Res.
Commu. 14:118123.
Greenway, H., and Osmond, C. B. 1972. Salt responses
of enzymes from species differing in salt tolerance.
Plant Physiol. 49:256259.
Greenway, H., and Munns, R. 1980. Mechanisms of salt
tolerance in nonhalophytes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 31:149190.
Greenwood, D. J., and Stone, D. A. 1998. Prediction and
measurement of the decline in the critical-K, the
maximum-K and total cation plant concentrations
during the growth of field vegetable crops. Ann.
Bot. 82:871881.
Griffith, G., and Walters, R. J. K. 1966. The sodium and
potassium content of some grass genera, species
and varieties. J. Agric. Sci. (Camb) 67:81.

Grof, G. P. L., Johnston, M., and Brownell, P. F. 1989.

Effect of sodium nutrition on the ultrastructure of
chloroplasts of C4 plants. Plant Physiol. 89:539
543.
Guan, J., Buxton, D. R., Goff, J. P., and Horst, R. L. 1997.
Alfalfa cultivar variation for minerals concentration. U.S. Dairy Forage Research Center Research
Summaries, pp. 8082.
Hall, J. L., and Flowers, T. J. 1973. The effect of salt
on protein synthesis in the halophyte Suaeda maritima. Planta 110:361368.
Haneklaus, S., Knudsen, L., and Schnug, E. 1998. Relationship between potassium and sodium in sugar
beet. Commun. Soil Sci. Plant Analy. 29:1793
1798.
Hanson, G., and Kylin, A. 1969. ATP-ase activities in homogenats from sugar-beet roots, relation to Mg++
and (Na+ + K+ )-stimulation. Z Pflanzenphysiol.
60:270275.
Hanson, G. 1975. Patterns of ionic influences on sugr beet
ATPases. PhD dissertation, Univ. of Stockholm,
Sweden, ISBN 91-7222-106-2.
Hanson, O. B., Stenstrup, L. T., and Knudsen, L. 1997.
Trials with sodium for carrots. Gartnertidende
(Denmark) 112:89.
Harmer, P. M. 1943. Muck soil management for sugar
beet production. Mich. Agr. Exp. Sta. Cir. Bul.
187.
Harmer, P. M., and Benne, E. J. 1945. Sodium as a crop
nutrient. Soil. Sci. Soc. Am. J. 60:137148.
Harmer, P. M., Benne, E. J., Laughlin, W. M., and Key,
C. 1953. Factors affecting crop response to sodium
applied as a common salt on Michigan muck soil.
Soil Sci. 76:117.
Harrison, T. R. 1991. Harrisons Principles of Internal
Medicine. 12th ed., McGraw-Hill, Inc., New York.
Harvey, D. M. R., Hall, J. L., Flowers, T. J., and Kent, B.
1981. Quantitative ion localization within Suaeda
maritima leaf mesophyll cells. Planta 151:555
560.
Hiatt, A. J., and Evans, H. J. 1960. Influence of
certain cations on activity of acetic thiokinase
from spinach leaves. Plant Physiol. 35:673
677.
Hille, B. 1992. Ionic channels of excitable membranes.
Sinauer Associates, Sunderland.
Hsiao, T. C. 1976. Stomatal ion transport. In: Encyclopedia of Plant Physiology, new series, vol. 2B,
pp. 193221, Luttge, U. and Pitman, M. G., eds.,
Springer-Verlag, Berlin.

Hsiao, T. C., and Lauchli, A. 1986. Role of potassium in

plant-water relations. Adv. Plant Nutr. 2:281312.
Humble, G. D., and Hsiao, T. C. 1969. Specific requirement of potassium for light-activated opening of
stomata in epidermal strips. Plant Physiol. 44:230
234.
Humble, G. D., and Hsiao, T. C. 1970. Light-dependent
influx and efflux of potassium of guard cells during stomatal opening and closing. Plant Physiol.
46:483487.
Hylton, L. O., Ulrich, A., and Cornelius, D. R. 1967.
Potassium and sodium interrelations in growth
and mineral content of Italian Ryegrass. Agron. J.
59:311314.
Iljin, W. S. 1932. Zusammensetzung der Salze
in der Pflanze auf verschiedenen Standorten.
Kalkpflanzen. Beih. Bot. Zbl. 50:95137.
Jarvis, S. C. 1982. Sodium absorption and distribution in
forage grasses of different potassium status. Ann.
Bot. 49:199206.
Jeschke, W. D. 1977a. K+ -Na+ exchange and selectivity
in barley root cells: Effect of Na+ on the Na+ fluxes.
J. Exp. Bot. 28:12891305.
Jeschke, W. D. 1977b. K+ - Na+ selectivity in roots, localisation of selective fluxes and their regulation. In:
Regulation of Cell Membrane Activities in Plants,
pp. 6378, Marre, E. and Ciferri, O., eds., Elsevier,
North Holland.
Jeschke, W. D. 1984. K+ -Na+ exchange at cellular membranes, intracellular compartmentation of cations,
and salt tolerance. In: Salinity Tolerance in Plants:
Strategies for Crop Improvement, pp. 3766,
Staples, R. C. and Toennissen, G. H., eds., Wiley,
New York.
Jeschke, W. D., and Wolf, O. 1988. External potassium
supply is not required for root growth in saline
conditions: Experiments with Ricinus communis
L. grown in a reciprocal split-root system. J. Exp.
Bot. 39:11491167.
Johnston, M., Grof, C. P., and Brownell, P. F. 1988. The
effect of sodium nutrition on the pool sizes of intermediates of the C4 photosynthetic pathway. Aust.
J. Plant Physiol. 15:749760.
Johnston, M., Grof, C. P. L., and Brownell, P. F. 1989.
Chlorophyll a/b ratios and photosystem activity
of mesophyll and bundle sheath fractions from
sodium-deficient C4 plants. Aust. J. Plant Physiol.
16:449457.
Judel, G., and Kuhn, H. 1975. Uber die wirkung einer natriumdungung zu zuckerruben bei guter versogung
mit kalium in gefabversuchen. Zucker. 28:6871.

411

Kawasaki, H., Takada, H., and Kamisaka, S. 1978. Requirement of sodium chloride for the action of gibberellic acid in stimulating hypocotyl elongation
of a halophyte Salicornia herbacea L. Plant Cell
Physiol. 19:14151425.
Kirkby, E. A., Armstrong, M. J., and Leggett, J. E.
1981. Potassium recirculation in tomato plants in
relation to potassium supply. J. Pl. Nutr. 3:955
966.
Knypl, J. S., and Chylinska, K. M. 1972. Comparison
of the stimulatory effect of potassium on growth,
chlorophyll and protein synthesis in the lettuce
cotyledons with the effects produced by other univalent ions. Biochem. Physiol. Pflanz. 163:5263.
Kylin, A., and Hansson, G. 1971. Transport of sodim and
potassium and properties of (sodim + potassium)
activated adenosine triphosphatase: Possible connection with salt tolerance in plants. pp. 6468. In:
8th Coll. Int. Potash Inst., Berlin.
Lamm, O., and Malmgren, H. 1940. Measurements of
the degree of dispersion of a highly polymerized
metaphosphate prepared according to Tammann.
Z. Anor. U allgm. Chem. 245:103120.
Larson, W. E., and Pierre, W. H. 1953. Interaction of
sodium and potassium on yield and cation composition of selected crops. Soil Sci. Soc. Am. J.
76:5164.
Lauchli, A., and Pfluger, R. 1979. Potassium transport
through plant cell membranes and metabolic role
of potassium in plants. In: Potassium Research
Review and Trends, pp. 111163, International
Potash Institute, Berlin.
Lee, R. B., and Ratcliffe, R. G. 1983. Phosphorus nutrition and the intracellular distribution of inorganic
phosphate I pea root tips: A quantitative study using 31 P-NMR. J. Exp. Bot. 34:12221244.

Leigh, R. A., and Deri Tomos, A. 1983. An attempt to use

isolated vacuoles to determine the distribution of
sodium and potassium in cells of storage roots of
redbeet (Beta vulgaris L.). Planta 159:469475.
Leigh, R. A., and Wyn Jones, R. G. 1984. A hypothesis relating critical potassium concentrations for growth
to the distribution and functions of this ion in the
plant cell. New Phytol. 97:113.
Leigh, R. A., and Wyn Jones, R. G. 1986. Cellular compartmentation in plant nutrition: The selective cytoplasm and the promiscuous vacuole. Adv. Plant
Nutr. 2:249279.
Loughman, B. C., and Ratcliffe, R. G. 1984. Nuclear
magnetic resonance and the study of plants. In:
Advances in Plant Nutrition, vol. 1, pp. 241
283, Tinker, P. B., and Lauchli, A., eds., Praeger,
New York.
Maathuis, F. J. M., and Sanders, D. 1993. Energization of
potassium uptake in Arabidopsis thaliana. Planta
191:302307.
Maathuis, F. J. M., and Sanders, D. 1995. Contrasting roles in ion transport of two K+ channel
types in root cells of Arabidopsis thaliana. Planta
197:456464.
Maathuis, F. J. M., and Sanders, D. 1996. Mechanisms of
potassium absorption by higher plant roots. Physiol. Plant. 96:158168.
Maathuis, F. J. M., Ichida, A. M., Sanders, D., and
Schroeder, J. I. 1997. Roles of higher plant K+
channels. Plant Physiol. 114:11411149.
MacElroy, R. W., and Bredt, J. 1985. Controlled ecological life support systems. Life support systems in
space travel: Current concepts and future directions
of CELSS. NASA Conf. Pub. 2378 XXV COSPAR
Meeting, Graz, Austria.

Lehr, J. J. 1953. Sodium as a plant nutrient. J. Sci. Food

Agric. 4:460471.

Mackowiak, C. L., Wheeler, R. M., Stutte, G. W., Yorio,

N. C., and Sager, J. C. 1977. Use of biologically reclaimed minerals for continuous hydroponic potato
production in a CELSS. Adv. Space Res. 20:1815
1820.

Lehr, J. J., and Wybenga, J. M. 1955. Exploratory pot

experiements on sensitiveness of different crops to
sodium. Plant Soil 3:251261.

Mackowiak, C. L., Garland, J. L., and Sager, J. C. 1996a.

Recycling crop residues for use in recirculating hydroponic crop production. Acta Hort. 440:1924.

Lehr, J. J. 1960. The sodium content of meadow grass

in relation to species and fertilization, pp. 101
103, Proceedings of the 8th International Grassland
Congress.

Mackowiak, C. L., Garland, J. L., Strayer, R. G., Finger,

B. W., and Wheeler, R. M. 1996b. Comparison of
aerobically treated and untreated crop residue as a
source of recycled nutrients in a recirculating hydroponic system. Adv. Space Res. 18:281287.

Lehr, J. J. 1947. The importance of sodium for plant nutrition. Soil Sci. 63:479.

Leigh, R. A., ApRees, T., Fuller, W. A., and Banfield,

J. 1979. The location of acid invertase activity and
sucrose in vacuoles of storage root of beetroot (Beta
vulgaris). Biochem. J. 178:539547.

412

Magat, S. S., and Goh, K. M. 1990. Effect of chloride

fertilizers on ionic composition and cation-anion
balance and ratio of fodder beet (Beta vulgaris L.)

grown under field conditions. New Zealand J Agric.

Res. 33:2940.
Marschner, H. 1971. Why can sodium replace potassium
in plants? pp. 5063. In: Proceedings of 8th Colloquem of International Institute of Potash Institute,
Berlin.
Marschner, H., and Possingham, J. V. 1975. Effects of
K+ and Na+ on growth of leaf discs of sugar beet
and spinach. Z. Pflanzenphysiol. Bd. 75:616.
Marschner, H., Kylin, A., and Kuiper, P. J. C. 1981a. Differences in salt tolerance of three sugar beet genotypes. Physiol. Plant. 51:234238.
Marschner, H., Kuiper, P. J. C., and Kylin, A. 1981b.
Genotypic differences in the response of sugar beet
plants to replacement of potassium by sodium.
Physiol. Plant. 51:239244.
Marschner, H. 1995. Mineral Nutrition of Higher Plants.
Academic Press, London.
Milford, G. F. J., Cormack, W. F., and Durrant, M. J.
1977. Effects of sodium chloride on water status
and growth of sugar beet. J. Exp. Bot. 28:1380
1388.
Mix, G., and Marschner, H. 1974. Mineralstoffverteilung
zwischen chloroplasten und ubrigem blattgewebe.
Z. Pflanzenphysiol. 73:307312.
Montasir, A. H., Sharoubeem, H. H., and Sidrak, G. H.
1966. Partial substitution of sodium for potassium
in water cultures. Plant Soil. 25:181194.
Moscolov, J. V., and Aleksandrovskaya, V. A. 1962. Physiological role of sodium in plants. Chem. Abstr.
56:1784.
Mozafar, A., Goddin, J. R., and Oertli, J. J. 1970. Naand K-interactions in increasing the salt tolerance
of Atriplex halimus L. I. Yield characteristic and
osmotic potential. Agron. J. 62:478481.
Murata, T., and Akazawa, T. 1968. Enzymatic mechanism
of starch synthesis in sweet potato root. I. Rquirement of potassium ions for starch synthetase. Arch.
Biochem. Biophys. 126:873879.
Murata, S., and Sekiya, J. 1992. Effects of sodium on
photosynthesis in Panicum coloratum. Plant Cell
Physiol. 33:12391242.
Murata, S., Kobayashi, M., Matoh, T., and Sekiya, J.
1992. Sodium stimulates regeneration of phosphoenolpyruvate in mesophyll chloroplasts of Amaranthus tricolor. Plant Cell Physiol. 33:1247
1250.
Nicholas, D. J. D. 1961. Minor mineral nutrients. Annu.
Rev. Plant Physiol. 12:6390.

Nigam, V. N., and Fridland, A. 1967. Studies on glycogen

synthesis in pigeon liver homognates. Biochem. J.
105:505513.
Nitsos, R. E., and Evans, H. J. 1969. Effects of univalent cations on the activity of particular starch synthetase. Plant Physiol. 44:12601266.
Nunes, M. A., Dias, M. A., Correia, M., and Oliveira, M.
M. 1984. Further studies on growth and osmoregulation of sugarbeet leaves under low salinity conditions. J. Exp. Bot. 35:322331.
Ohta, D., Matoh, T., and Takahashi, E. 1987. Early responses of sodium-deficient Amaranthus tricolor
L. plants to sodium application. Plant Physiol.
84:112117.
Ohta, D., Yasuoka, S., Matoh, T., and Takahashi, E. 1989.
Sodium stimulates growth of Amaranthus tricolor
L. plants through enhanced nitrate assimilation.
Plant Physiol. 89:11021105.
Ohnishi, J., Flugge, U., Heldt, H. W., and Kanai, R. 1990.
Involvement of Na+ in active uptake of pyruvate
in mesophyll chloroplasts of some C4 plants. Plant
Physiol. 94:950959.
Pardossi, A., Bagnoli, G., Malorgio, F., Campiotti, C.
A., and Tognoni, F. 1999. NaCl effects on celery
(Apium graveolens L.) grown in NFT. Scienti. Hort.
81:229242.
Peck, N. H., VanBuren, J. P., MacDonald, G. E., Hemmat,
H., and Becker, R. F. 1987. Table beet plant and
canned root responses to Na, K, and Cl from soils
and from applications of NaCl and KCl. J. Am. Soc.
Hort. Sci. 112:188194.
Perera, L. K. R. R., Silva, D. L. R., and de Mansfield,
T. A. 1997. Avoidance of sodium accumulation
by the stomatal guard cells of the halophyte Aster
tripolium. J. Exp. Bot. 48:707711.
Pessarakli, M., and Tucker, T. C. 1985. Uptake of
Nitrogen-15 by cotton under salt stress. Soil Sci.
Soc. Am. J. 49:149152.
Pessarakli, M., and Marcum, K. B. 2000. Growth responses and Nitrogen-15 absorption of Distichlis
under sodium chloride stress. ASA-CSSA-SSSA
Annual Meetings, Nov. 59, 2000, Minneapolis,
Minnesota (Agronomy abstracts).
Pessarakli, M., Marcum, K. B., and Kopec, D. M. 2001.
Growth responses of desert saltgrass (Distichlis
spicata L.) under salt stress. Turfgrass Landscape
and Urban IPM Research Summary 2001, Cooperative Extension, Agricultural Experiment Station,
The University of Arizona, Tucson, U.S. Department of Agriculture, AZ1246 Series P-126, pp. 70
73.

413

Pfluger, W., and Wiedemann, W. 1977. Der Einflus

monovalenter kationen auf die nitratreduktion von
Spinacia oleracea L. Z Pflanzephysiol. 85:125
133.
Pierce, W. S., and Higinbotham, N. 1970. Compartments
and fluxes of K+ , Na+ and Cl in Avena coleoptile
cells. Plant Physiol. 46:660673.
Pitman, M. G. 1963. The determination of the salt relations of the cytoplasmic phase in beet root tissue.
Aust. J. Biol. Sci. 16:647668.
Pitman, M. G. 1965. Transpiration and selective uptake of
potassium by barley seedlings (Hordeum vulgare
cv. Boliva). Aust. J. Biol. Sci. 18:987.
Pitman, M. G. 1966. Uptake of potassium and sodium
by seedlings of Sinapsis alba. Aust. J. Biol. Sci.
19:257.

Reith, J. W. S., Inkson, R. H. E., Holmes, W., Maclusky, D.

S., Reid, D., Heddle, R. G., and Copeman, G. J. F.
1964. The effect of fertiliser on herbase production. II. The effect of nitrogen, phosphorus, and
potassium on botanical and chemical composition.
J. Agric. Sci. (Camb) 63:209.
Richards, L. A. 1954. Diagonosis and Improvement of
Saline and Alkali Soils. USDA Handbook No. 60.
Roberts, S. K., and Tester, M. 1995. Inward and outward
K+ -selective currents in the plasma membrane of
protoplasts from maize root cortex and stele. Plant
J. 8:811825.
Rocha, V., and Ting, I. P. 1970. Tissue distribution of
mocrobody, mitochondrial, and soluble malate dehydrogenase isoenzymes. Plant Physiol. 46:754
756.

Pitman, M. G., Lauchli, A., and Stelzer, R. 1981. Ion distribution in roots of barley seedlings measured by
electron probe X-ray microanalysis. Plant Physiol.
68:673679.

Rumburg, B., Reinwald, E., Schroder, H., and Sippel, U.

1968. Correlation between electron flow, proton
translocation and phosphorylation in chloroplasts.
Naturwiss 55:7779.

Poole, R. J. 1971. Effect of sodium on potassium fluxes at

the cell membrane and vacuole membrane of red
beet. Plant Physiol. 47:731734.

Rush, D. W., and Epstein, E. 1981. Comparative studies

on the sodium, potassium, and chloride relations
of a wild halophytic and a domestic salt-sensitive
tomato species. Plant Physiol. 68:13081313.

Preiss, J., and Greenberg, E. 1967. Biosynthesis of

starch in Chlorella pyrenoidosa. I. Purification and
properties of the adenosine diphosphoglucose:4-glucosyl transferase from Chlorella. Arch.
Biochem. Biophys. 118:702708.
Putnam, D. F. 1972. Composition and concentrative properties of human urine. NASA CR-1802.
Raghavendra, A. M., Rao, J. M., and Das, V. S. R. 1976.
Replaceability of potassium by sodium for stomatal opening in epidermal strips of stomatal opening in epidermal strips of Commelina benghalensis.
Z Pflanzenphysiol 80:3642.
Rains, D. W., and Epstein, E. 1965. Transport of sodium
in plant tissue. Science 148:1611.
Rains, D. W., and Epstein, E. 1967. Preferential absorption of potassium by leaf tissue of the mangrove,
Avicennia marina: An aspect of halophylic compentence in coping with salt. Aust. J. Biol. Sci.
20:847857.
Rains, D. W. 1972. Salt transport by plants in relation to
salinity. Annu. Rev. Plant Physiol. 23:367388.
Rajcevic, M., Stekar, J. M. A., Vardjan, S., and Zlindra,
J. 1995. Availability of major elements from grassland in cows. Krmiva 37:279285.
Reimann, C., and Breckle, S. W. 1993. Sodium relations in
Chenopodiaceae: A comparative approach. Plant
Cell Env. 16:323328.

414

Schachtman, D., Tyerman, S., and Terry, B. 1991. The

K+ /Na+ selectivity of a cation channel in the
plasma membrane of root cells do not differ in
salt-tolerant and salt-sensitive wheat species. Plant
Physiol. 97:598605.
Shah, B. H., and Wedding, R. T. 1968. Sodium ion influence on phosphorylations associated with oxidation of succinate by turnip root mitochondria.
Science 160:304306.
Sharma, C. P., and Singh, S. 1990. Sodium helps overcome
potassium deficiency effects on water relations of
cauliflower. HortSci. 25:458459.
Shone, M. G. T., Clarkson, D. T., and Sanderson, J. 1969.
The absorption and translocation of sodium by
maize seedlings. Planta 86:301314.
Sinclair, A. H., Macdonald, D. C., Ferrier, R., and
Edwards, A. C. 1993. The use of minor nutrients
for grassland. In: Forward With Grass into Europe:
Proceedings of the British Grassland Society Winter Meeting held at Great Malvern, Worcestershire,
1617th Nov. 1992. Hopkins, A. and Younie, D.,
eds., UK.
Smith, F. W. 1974. The effect of sodium on potassium
nutrition and ionic relations in Rhodes grass. Aust.
J. Agric. Res. 25:407414.
Smith, G. S., and Middleton, K. R. 1978. Sodium and
potassium content of top-dressed pastures in New

Zealand in relation to plant and animal nutrition.

N. Z. J. Exp. Agric. 6:217225.

leaves of sugar beet under conditions of low sodium

supply. Plant Physiol. 51:10991101.

Smith, F. A., and Raven, J. A. 1979. Intracellular pH and

its regulation. Annu. Rev. Plant Physiol. 30:289
311.

Tester, M., and Blatt, M. R. 1989. Direct measurement of

K+ channels in thylakoid membranes by incorporation of vesicles into planar lipid bilayers. Plant
Physiol. 91:249252.

Smith, G. S., Middleton, K. R., and Edmonds, A. S. 1980.

Sodium nutrition of pasture plants. I. Translocation
of sodium and potassium in relation to transpiration
rates. New Phytol. 84:603612.
Smith, G. S., Lauren, D. R., Cornforth, I. S., and Agnew,
M. P. 1982. Evaluation of putrescine as a biochemical indicator of potassium requirements of lucerne.
New Phytol. 91:419428.
Subbarao, G. V., Wheeler, R. M., Stutte, G. W., and
Levine, L. H. 1999a. How far can sodium substitute for potassium in redbeet? J. Pl. Nutr. 22:1745
1761.
Subbarao, G. V., Mackowiak, C., and Wheeler, R. M.
1999b. Recycling of Na in adanced life support:
Strategies based on crop production systems. Life
Support and Biosphere Sci. 6:153160.
Subbarao, G. V., Wheeler, R. M., and Stutte, G. W. 2000a.
Feasibility of substituting sodium for potassium in
crop plants for advanced life support systems. Life
Support and Biosphere Sci. 7:225232.
Subbarao, G. V., Wheeler, R. M., Stutte, G. W., and
Levine, L. H. 2000b. Low potassium enhances
sodium uptake in red-beet under moderate saline
conditions. J. Plant Nutrition 23:14491470.
Subbarao, G. V., and Johansen, C. 2002. Physiological mechanisms relevant to genetic improvement
of salinity tolerance in crop plants. In: Handbook of Plant and Crop Physiology, pp. 857
880, Pessarakli, M., ed., Marcel Dekker Inc.,
New York.
Suelter, C. H. 1970. Enzymes activated by monovalent
cations. Science 168:289295.
Takahashi, E., and Maejima, K. 1998. Comparative research on sodium as a beneficial element for crop
plants. Memoirs of the faculty of Agriculture of
Kinki University VO:5772.
Tanaka, Y., Ito, T., and Akazawa, T. 1970. Enzymatic
mechanism of starch breakdown in germinating
rice seed. III. -Amylase isoenzymes. Plant Physiol. 46:650654.
Terry, N., and Ulrich, A. 1973a. Effects of potassium
deficiency on the photosynthesis and respiration
of leaves of sugar beet. Plant Physiol. 51:783
786.
Terry, N., and Ulrich, A. 1973b. Effects of potassium deficiency on the photosynthesis and respiration of

Thom, M., Maretzki, A., and Komor, E. 1982. Vacuoles from sugarcane suspension cultures. I. Isolation and partial characterization. Plant Physiol.
69:13151319.
Thomas, D. A. 1970. The regulation of stomatal aperture
in tobacco leaf epidermal strips. I. The effect of
ions. Aust J. Biol. Sci. 23:961979.
Tinker, P. B. H. 1965. The effects of nitrogen, potassium
and sodium fertilizers on sugar beet. J. Agric. Sci.
(Camb) 65:207212.
Troug, E., Berger, K. C., and Attoe, O. J. 1953. Response of nine economic plants to fertilization with
sodium. Soil Sci. Soc. Am. J. 76:4150.
Tullin, V. 1954. Response of the sugar beet to common
salt. Physiol. Plant. 7:810834.
Very, A. A., Robinson, M. F. Mansfield, T. A., and
Sanders, D. 1998. Guard cell cation channels are involved in Na+-induced stomatal closure in a halophyte. Plant J. 14:509521.
Vogelzang, S. A., and Prins, H. B. A. 1994. Patch clamp
analysis of the dominant plasma membrane K+
channel in root cell protoplasts of Plantago media
L: Its significance for the P and K state. J. Membr.
Biol. 141:113122.
Wagner, G. J. 1982. Compartmentation in plant cells:
The role of the vacuole. In: Cellular and Subcellular Localization in Plant Metabolism, pp. 145,
Creasy, L. L., and Hrazdina, G., eds., Plenum Press,
New York.
Walker, D. J., Leigh, R. A., and Miller, A. J. 1996a. Potassium homeostasis in vacuolate plant cells. Proc.
Natl. Acad. Sci. USA 93:1051010514.
Walker, N. A., Sanders, D., and Maathuis, F. J. M. 1996b.
High-affinity potassium uptake in plants. Science
273:977978.
Watt, B. K., and Merrill, A. L. 1975. Composition of
Foods. USDA Handbook No. 8.
Weatherley, P. E., 1969. Ion movement within the plant.
In: Ecological Aspects of the Mineral Nutrition of
Plants, pp. 323340, Rorison, I. H., ed., Blackwell,
Oxford.
Wegner, L. H., and Raschke, K. 1994. Ion channels in the
xylem parenchyma of barley roots. Plant Physiol.
105:799813.

415

Wegner, L. H., and DeBoer, A. 1997. Two inward K+

channels in the xylem parenchyma cells of barley roots are regulated by G-protein modulators
through a membrane-delimited pathway. Planta
203:506516.
Wenhua, F., Bin Bai, W., Zhang, Y., and Zhang, Y. 1998.
Sodium contents in plants of natural grassland
reserve in Wutai Mountain. Grassland of China
VO:3639.
Wesselmann, U., Fuer Gruenlandwirtschaft, L. V. A.,
Futterbau, and Bredstedt, L. 1993. Sodium fertilization on pasture. Milchpraxis (Germany)
31:225228.
Wheeler, R. M., Sager, J. C., Mackowiak, C. L., Stutte,
G. W., Yorio, N. C., Ruffe, L. M., and Berry, W. L.
1999. Nutrient, acid and water budgets of hydroponically grown crops. Acta Hort. 481:655661.
Wheeler, R., Stutte, G., Subbarao, G. V., and Yorio, N.
C. 2002. Plant growth and human life support for
space travel. In: Handbook of Plant and Crop Physiology, pp. 925941, Pessarakli, M., ed., Marcel
Dekker Inc., New York.
Whitehead, D. C., and Jones, L. H. P. 1972. The effect of
replacing potassium by sodium on cation uptake
and transport to the shoots in four legumes and
Italian ryegrass. Ann. Appl. Biol. 71:8189.
Willenbrink, J., Doll, S., Getz, H. P., and Meyer, S. 1984.
Zuckeraufnahme in isolierten vakuolen und protoplasten aus dem speichergewebe von beta-ruben.
Ber. Deutsch. Bot. Ges. 97:2739.
Williams, M. C. 1960. Effect of sodium and potassium
salts on growth and oxalate content of halogeton.
Plant Physiol. 35:500509.
Wooley, J. T. 1957. Sodium and silicon as nutrients for
the tomato plant. Plant Physiol. 1:317321.

416

Wu, W., Peters, J., and Berkowitz, G. A. 1991.

Surface charge-mediated effects of Mg2+ ,
on K+ flux across the chloroplast envelope
are associated with regulation of stromal pH
and photosynthesis. Plant Physiol. 97:580
587.
Wyn Jones, R. G., Brady, C. J., and Speirs, J. 1979. Ionic
and osmotic relations in plant cells. In: Recent Advances in the Biochemistry of Cereals, pp. 63
103, Laidman, D. C., and Wyn Jones, R. G., eds.,
Academic Press, New York.
Wyn Jones, R. G., and Gorham, J. 1983a. Osmoregulation. In: Encyclopedia of Plant Physiology,
vol. 12c, pp. 3558, Lange, O. L., Nobel, P. S.,
Osmond, C. B., and Zeigler, H., eds., Springer
Verlag, Berlin.
Wyn Jones, R. G., and Pollard, A. 1983b. Proteins, enzymes and inorganic ions. In: Encyclopedia of
Plant Physiology, new series vol. 15B, pp. 528
562, Laidman, D. L., and Wyn Jones, R. G., eds.,
Springer-Verlag, Berlin.
Wyn Jones, R. G. 1999. Cytoplasmic potassium homeostasis: Review of the evidence and its implications. In: Frontiers in Potassium Nutrition: New
Perspectives on the Effects of Potassium on Physiology of Plants, pp. 1322, Oosterhuis, D. and
Berkowitz, G., eds., Potash and Phosphate Institute of Canada, Saskatoon, Canada.
Yeo, A. R. 1981. Salt tolerance in the halophyte
Suaeda maritima L. Dum.: Intracellular compartmentation of ions. J. Exp. Bot 32:487
497.
Ziegler, H. 1975. Nature of transported substances. In: Encyclopedia of Plant Physiology, new series, vol. 1,
pp. 59100, Zimmermann, M. H., and Milburn,
J. A., eds., Springer-Verlag, Berlin.