Critical Reviews in Plant Sciences

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Root Development and Nutrient Uptake

H. Wang , Y. Inukai & A. Yamauchi

To cite this article: H. Wang , Y. Inukai & A. Yamauchi (2006) Root Development and Nutrient
Uptake, Critical Reviews in Plant Sciences, 25:3, 279-301, DOI: 10.1080/07352680600709917

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Published online: 18 Jan 2007.

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Critical Reviews in Plant Sciences, 25:279–301, 2006
Copyright
c Taylor & Francis Group, LLC
ISSN: 0735-2689 print / 1549-7836 online
DOI: 10.1080/07352680600709917

Root Development and Nutrient Uptake

H. Wang
Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya 464-8601, Japan
Present Address Soil and Fertilizer Institute, Chinese Academy of Agricultural Sciences; Key Laboratory
of Plant Nutrition and Nutrient Cycling Research, Ministry of Agriculture; Beijing, 100081, China

Y. Inukai
Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya 464-8601, Japan

A. Yamauchi
Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya 464-8601, Japan

Referee: Dr. Bobbie McMichael, Plant Physiologist, USDA-ARS, Plant Stress and Germplasm Development Unit, 3810 4th St., Lubbock, Texas 79415

Table of Contents

I. INTRODUCTION ........................................................................................................................................... 280

II. ROOT GROWTH AND FUNCTIONS REGULATED BY SHOOT .................................................................. 280

A. Root System Formation in Relation to Shoot Growth .................................................................................... 280
B. Root-Shoot Interactions in Material Cycling ................................................................................................ 280
1. Regulation of Root Growth by the Shoot ............................................................................................ 280
2. Regulation of Root Function by the Shoot .......................................................................................... 281

III. ROOT MORPHOLOGICAL PROPERTIES FOR NUTRIENT UPTAKE AND TRANSPORT ....................... 281
A. Root Morphology and Architecture ............................................................................................................. 282
B. Root Surface Area ..................................................................................................................................... 282
C. Root Hairs ................................................................................................................................................ 283

IV. PHYSIOLOGICAL MECHANISMS OF NUTRIENT UPTAKE AND TRANSPORT IN ROOTS ................... 283
A. Kinetic Mechanism .................................................................................................................................... 283
B. Nutrient Ion Homeostasis ........................................................................................................................... 284
C. Rhizosphere and Root Exudation ................................................................................................................ 285

V. ROOT NUTRIENT TRANSPORT SYSTEMS AND THEIR MOLECULAR BIOLOGY ................................. 285
A. Nitrogen ................................................................................................................................................... 287
B. Phosphorus ............................................................................................................................................... 288
C. Potassium ................................................................................................................................................. 289
D. Calcium .................................................................................................................................................... 290
E. Magnesium ............................................................................................................................................... 291
F. Sulfur ....................................................................................................................................................... 291
G. Micronutrient Metals ................................................................................................................................. 292
H. Micronutrient Anions ................................................................................................................................. 293
1. Chloride ......................................................................................................................................... 293
2. Molybdenum ................................................................................................................................... 293
3. Boron ............................................................................................................................................. 293

Address corresopondence to A. Yamauchi, Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya 464-8601,
Japan. E-mail: ayama@agr.nagoya-u.ac.jp

279
280 H. WANG ET AL.

VI. CONCLUSIONS ............................................................................................................................................. 294

REFERENCES .......................................................................................................................................................... 294

II. ROOT GROWTH AND FUNCTIONS REGULATED

Root system formation proceeds in close coordination with shoot BY SHOOT
growth. Accordingly, root growth and its functions are regulated
tightly by the shoot through materials cycling between roots and A. Root System Formation in Relation to Shoot Growth
shoots. A plant root system consists of different kinds of roots that Roots of higher plants are the unique organs responsible for
differ in morphology and functions. The spatial configuration and mineral nutrition with the xylem as the principal pathway for
distribution of these roots determine root system architecture in
the soil, which in turn primarily regulates the acquisition of soil transporting nutrient elements. However, the xylem per se is
resources like nutrients and water. Morphological and physiolog- inadequate for supplying the shoot with the mineral elements
ical properties of each root and the concomitant tissues further essential for growth. A functional co-operation between root
affect nutrient uptake and transport, while the root traits that are and shoot, i.e., between root-sourced xylem and leaf-sourced
related to such acquisition also depend on the kinds of nutrients phloem, is needed for supplying growing organs, including
and their mobility in the soil. In addition, mechanisms involved in
the uptake and transport of mineral nutrients recently have been roots, with the required nutrients, as shown especially for N (re-
elucidated at the molecular level. A number of genes for acquisition viewed by Jeschke and Hartung, 2000; Yoneyama et al., 2003).
and transport of various mineral nutrients have been identified in Tatsumi and Kono (1980) reported that in rice plants, the major
model plant systems such as Arabidopsis thaliana, and rice, and in portion of N absorbed by the root tends to be transported to the
other plant species. An integration of studies on nutrient behav- shoot, whereas a lesser portion is directly utilized by the roots,
ior in soils and the morphological and physiological functions of
root systems will further elucidate the mechanism of plant nutri- and thus root growth largely depends on the N supplied from the
ent uptake and transport by roots, and offer a real possibility of shoot. Therefore, the formation of the root system keeps pace
genetically improving crop productivity in problem soils. with the development of the shoot. For example, the emergence
of nodal (adventitious) roots in rice proceeds acropetally along
Keywords channels, ion pumps, nutrient mobility, root-shoot interac- both the main stems and tillers, keeping pace with successive leaf
tion, root system architecture, transporters, transport pro- unfolding. Lateral roots also develop in synchrony with shoot
teins growth. In fact, a positive correlation is usually found between
the number of root primordia and the surface area of the vascular
cylinder in the stem (reviewed by Morita and Nemoto, 1995).
I. INTRODUCTION
This paper reviews recent research progress in root system B. Root-Shoot Interactions in Material Cycling
development and function specifically on nutrient uptake and 1. Regulation of Root Growth by the Shoot
transport. A plant root system consists of different kinds of roots Root development is extremely sensitive to a wide range
that differ in morphology and function. The spatial configuration of physical, chemical and biological factors (Schiefelbein and
and distribution of these roots determine root system architecture Benfey, 1991; McMichael and Quisenberry, 1993; Robinson,
in soil (Yamauchi et al., 1996), which primarily regulates the ac- 1994; Yamauchi et al., 1996). A striking example of its plastic-
quisition of soil resources like nutrients and water. Furthermore, ity is seen in the way in which many plant species respond to an
the morphological and physiological properties of each root and uneven distribution of nutrients (NO− +
3 , NH4 or inorganic phos-
the concomitant tissues and cells further affect nutrient uptake phate) by proliferating their lateral roots preferentially within
and transport. nutrient-rich zones (Drew, 1975; Robinson, 1994; Leyser and
We first describe the process of root system formation with Fitter, 1998; Huang and Eissenstat, 2000). In contrast, a high
special emphasis on its relationship with shoot development and rate of N supply to the entire root system is usually associated
whole plant growth, and the material transport from shoot to with a reduced allocation of resources to root growth (Ericsson,
roots. Similarly, shoot and plant development as a whole is 1995). Roots also respond in a similar manner to fluctuating soil
also strongly dependent on root functions. Although a num- moisture conditions (Bañoc et al., 2000) and the responses in
ber of materials are involved in such developmental processes, branching are closely related with the supply of photosynthates
we focus on soil nutrient uptake and transport from roots to from the shoot (Ogawa et al., 2005). These observations clearly
aerial organs. For each topic, we describe first the morpholog- indicate that shoots control root development.
ical and physiological traits and then discuss their molecular In fact, experiments with split-root systems have con-
basis. firmed the existence of systemic controls on NO− 3 -induced root
 ROOT DEVELOPMENT AND NUTRIENT UPTAKE 281

branching and provided strong evidence that the regulatory sig- ing constitutive iron deficiency responses while containing high
nals arise from the shoot (Friend et al., 1990; Lainé et al., 1998; amounts of iron in their tissues (Kneen et al., 1990; Welch and
Scheible et al., 1997b). The importance of NO− 3 accumulation in LaRue, 1990). Reciprocal grafting between dgl or brz and their
the shoot as a root growth-regulating signal was demonstrated parental genotypes indicated that the phenotype of the root is
using tobacco transformants expressing very low levels of ni- determined by the shoot genotype (Grusak and Pezeshgi, 1996).
trate reductase (NR) (Scheible et al., 1997a, 1997b; Stitt and Moreover, split-root experiments carried out on Plantago lance-
Feil, 1999). Under conditions where the low NR lines accumu- olata and Arabidopsis showed that the activity of ferric reduc-
lated high concentrations of NO− 3 in the shoot, the amino acid tase, which reduces Fe+ +
3 into Fe2 in the rhizosphere, allowing
and protein content remained low, but there was a major shift plants to efficiently take it up, is increased in the compartment
in the shoot: root ratio and a marked decrease in lateral root supplied with iron, suggesting a long-distance signaling process
density. (Schmidt et al., 1996; Schikora and Schmidt, 2001). A 31-kDa
Auxin, a major plant growth regulator that is synthesized protein (CmPP36) may be involved in long-distance signaling of
in shoots and transported to roots, plays a key role in shoot- the iron status of the shoot, since it is present in the phloem sap
to-root communication (reviewed by Berleth and Sachs, 2001; of Cucurbita maxima, is similar to cytochrome b5 reductases,
Tanimoto, 2005). The isolation of a number of mutants and and is able to reduce Fe+ +
3 -citrate and Fe3 -EDTA in the presence
+
genes involved in lateral root formation in Arabidopsis (re- of NADH (Xoconostle-Cazares et al., 2000). Similarly, the up-
viewed by Hagen and Guilfoyle, 2002; Liscum and Reed, 2002) take of K+ and sulfate by roots is regulated by demand-driven
and nodal root formation in rice (Inukai et al., 2005; Liu et al., control mediated by K+ recirculation in the phloem and by the
2005) has provided a genetic link to the auxin signaling path- sulfate to glutathione ratio in the phloem, respectively (White,
way. When Arabidopsis seedlings were grown on nutrient media 1997; Herschbach et al., 2000).
with a high sucrose to N ratio, lateral root initiation was dramat- As such, root development proceeds in close coordination
ically repressed (Malamy and Ryan, 2001). In those seedlings, with shoot growth, and the development and function of roots
auxin accumulation was observed in the hypocotyls. Similarly, are under strong control by the shoot through material cycling.
Al-Ghazi et al. (2003) suggested that auxin redistribution oc- Similarly, the shoot and plant development as a whole strongly
curred in phosphate-starved Arabidopsis plants, which also in- depends on root function. In the succeeding sections, we will
duced a decreased number of lateral roots. On the other hand, describe the correlation between roots and shoots specifically
López-Bucio et al. (2002) reported that phosphate-starved Ara- on nutrient uptake and transport from roots to shoots.
bidopsis plants were more sensitive to auxin induction of lateral
roots than control plants. These results suggest that changes in
auxin distribution and sensitivity may play an important role in III. ROOT MORPHOLOGICAL PROPERTIES FOR
the effect of nutrient deprivation on lateral root development. NUTRIENT UPTAKE AND TRANSPORT
It is a prerequisite that for nutrient uptake to occur, the root
2. Regulation of Root Function by the Shoot surface should be in contact with nutrients in the soil, which
Uptake of mineral nutrients by roots has a strong influence on is achieved in three ways: root interception, mass flow and dif-
vegetative and reproductive development of the shoots. Corre- fusion (Marschner, 1995; Barber, 1995; Jungk, 2002). Root in-
spondingly, nutrient uptake needs to be regulated in response to terception results from the growth of roots to the sites where
shoot demand (Engels and Marschner, 1992). The “N demand” nutrients are located. The quantity of nutrients intercepted by
theory states that N deficiency in plant tissues accelerates NO− 3 the growing root equals the amount of nutrients present in a
uptake by the roots while the active synthesis and large accumu- volume of soil identical to the root volume. Mass flow and dif-
lation of amino acids in plants results in repression of NO− 3 up- fusion are the transport of nutrients from the bulk soil to the
take (Imsande and Touraine, 1994). Thus, the activities of NO− 3 root surface. Mass flow is the convective transport of nutrients
uptake and the expression of NO− 3 uptake transporter genes in dissolved in solution from the bulk of soil toward the root, and
the root system are regulated by phloem-borne metabolites orig- its driving force is the water potential gradient resulting from
inating from the shoot (Gansel et al., 2002). However, split-root root absorption of water from soils. Diffusion on the other hand
studies on mungbean found no correlation between rates of NO− 3 is the random movement of nutrient ions based on the principle
uptake and either quantitative or qualitative changes in the amino of thermal movement when an ion concentration gradient exists
acid content of the phloem (Tillard et al., 1998). Therefore, the between the soil and the root (Marschner, 1995; Barber, 1995;
mechanism of how changes in the N status of the shoot are com- Jungk, 2002).
municated to the root is not yet clear. Sucrose, plant hormones, Based on these mechanisms, root morphological properties
proteins and other macromolecules are suggested as candidates greatly affect the acquisition of nutrients by several factors in
for the signals (reviewed by Forde, 2002). various ways. It is important to emphasize that the traits of
The existence of shoot-borne signals regulating the root re- the root that determine its acquisition capacity also depend on
sponse to iron starvation has also been suggested in degener- the nutrient mobility in soil (Yamauchi, 2001), as discussed in the
ative leaflets (dgl) and bronze (brz), two pea mutants present- following sections.
282 H. WANG ET AL.

A. Root Morphology and Architecture foraging for P include a more horizontal basal-root growth an-
Root morphology (e.g., root length and radius) and architec- gle, resulting in shallower roots, and increased adventitious root
ture (e.g., branching pattern) are the primary traits that influ- formation, enhanced lateral root formation and increased root
ence plant resource acquisition (Caldwell, 1987; Barber, 1995; hair density and length. In the root system architecture of Ara-
Yamauchi et al., 1996). bidopsis, Williamson et al. (2001) found that P-deficient condi-
Finer roots can confer greater nutrient uptake per unit root tions resulted in a redistribution of root growth from the primary
mass, as discussed below for root surface area. For example, the root to lateral roots, i.e., a reduction in primary root elongation
nitrate uptake rate by turfgrasses was positively correlated with accompanied by increased lateral root density and elongation.
the fibrous root length, surface, and volume of every diameter Besides the above two static models (fractal geometry and
class. But larger numbers of thick roots (diameter ≥0.5 mm) topology), dynamic models of root system architecture are also
appeared to have no effect on nitrate uptake rate, while increased often used to simulate growing root systems on the basis of
rhizome number appeared to have a negative effect on nitrate simple production rules (Lynch and Nielsen, 1996; Dunbabin
uptake rate (Sullivan et al., 2000). et al., 2002, 2004; Pagès, 2002; Pagès et al., 2004). Root sys-
The root system architecture mentioned above has been stud- tem models simulate root system development in discrete time
ied with various models that conceptualize and analyze root steps. They offer an opportunity to integrate, from the root seg-
architecture. The fractal geometry approach describes root sys- ment to the root system levels, interactions between root systems
tems in the soil space using the fractal dimension D, with its un- and their environment. Somma et al. (1998) used architectural
derlying assumption that the root system is self-similar across a modeling to dynamically predict both uptake of nitrate, a mobile
large range of space scales (Tatsumi et al., 1989; Tatsumi, 2001). nutrient, and the influence of nitrate availability on root growth.
Nielsen et al. (1998) screened for more efficient P-acquiring Water and NO− 3 were supplied through drippers at the soil sur-
genotypes of common bean in the field based on the measure- face. In one scenario, NO− 3 was applied continuously, while in
ment of linear and planar fractal dimensions by tracing root the other, NO− 3 was applied for a finite time at the beginning of
intercepts in vertical planes. The linear fractal dimension in- the simulation. In the former case, simulations showed that N
creased over time in the efficient genotypes, but remained fairly concentrations were higher in the upper part of the soil and that
constant over time in the inefficient genotypes. The planar fractal root density decreased with depth. In the latter case, the NO− 3
dimension increased over time for all genotypes, but was higher plume moved downwards and a greater root density occurred in
in the efficient than the inefficient genotypes at the end of the the central part of the soil. The maximum root length density
experiment. and NO− 3 concentration were shifted, and these were linked to
In topological modeling, the root system is described by a set the relative rates of root growth and downward percolation of
of links (a link connects an apex to one or two branch points) and NO− 3.
some topological parameters, such as the number of links along
the path between an apex and the collar of the root system (Fitter,
2002). Fitter suggested that herringbone topologies would be B. Root Surface Area
more efficient in exploiting mobile nutrients such as nitrate, for A large root surface area is beneficial for relatively high total
which herringbone type root systems produce a few orders of uptake of a nutrient. For example, raya root could exploit Mn
laterals, which are characterized by low growth rates and limited from a greater volume of soil than wheat (Triticum aestivum),
extension from the zone depleted by the parent root. Izumi et al. which is probably related to the fact that the root surface area of
(1997) showed genotypic variation in rice seminal root responses raya was 2.3 times that of wheat (Samal et al., 2003). Similarly,
to different water conditions using a combination of fractal and Vigour 18, a breeding line of wheat with higher root dry matter,
topological analyses. root length density and root surface area, had significantly higher
The process of phosphorus acquisition has been most exten- shoot biomass and N uptake (Liao et al., 2004).
sively studied using topology among nutrient elements. Root The surface area of a root system is significantly affected by
architecture adaptations are important to enhance acquisition of the radii of the roots. Claassen and Steingrobe (1999) suggested
P from topsoil because of the relative immobility of P in soil, that the specific soil volume, out of which a nutrient diffuses to
with the highest concentrations usually found in the topsoil and plant roots, is negatively related to the root radius, indicating that
little movement of P into the lower soil profiles. Ge et al. (2000) a thinner root system has a larger surface area, which may ac-
suggested that shallower root systems of bean plants explored count for the observation that thinner roots increased availability
more P in soil per unit root biomass than deeper systems in the of Zn due to a more thorough exploration of the soil (Dong et al.,
case of homogeneous P distributions in the soil profile. In an 1995).
experiment in soil with a stratified P concentration, with high P The characteristics of Oryza sativa roots required for internal
concentration in the first 10 cm, shallower root systems were able aeration may conflict with the surface area available for absorb-
to acquire more P because of increased foraging of the topsoil ing nutrients and the extent of oxygenation of the rhizosphere.
and less inter-root competition. Lynch and Brown (2001) sug- Kirk (2003) suggested that in a root system consisting of coarse
gested that root characteristics associated with improved topsoil and aerenchymatous primary roots with gas-impermeable walls
 ROOT DEVELOPMENT AND NUTRIENT UPTAKE 283

conducting O2 to short, fine and gas-permeable laterals should gential and radial walls of underlying cortical cells, while roots
provide the greatest absorbing surface per unit root mass in rice. of Fe-deficient plants were characterized by a high percentage
He further suggested that with this architecture and typical rates of extra hairs with two tips.
of root respiration, rates of O2 loss to the soil could allow a plant Comparing these results with those in soil experiments, the
to absorb more NO− +
3 due to the nitrification of NH4 to NO3 .
−
impact of root hairs may not be detectable in solution culture
or nutrient-sufficient medium, where nutrient ions freely diffuse
to the root surface. Suzuki et al. (2003) found that in solution
C. Root Hairs culture, there was no significant difference in the amount of
Root hairs are tubular extensions of epidermal cells that have phosphate uptake per unit root dry weight between progeny of
their origin in protoderm cells, including specialized protoderm the rice cultivar Oochikara and a root-hairless mutant, rh2.
cells called trichoblasts (Peterson and Farquhar, 1996). An esti- Si is a beneficial element for higher plants (Epstein, 1999;
mated 77% of the total root surface area of cultivated crops is oc- Ma et al., 2001b). By using two mutants of rice defective in the
cupied by roots hairs forming the major point of contact between formation of root hairs in nutrient solution, Ma et al. (2001a)
the plant and the rhizosphere (Parker et al., 2000; Bibikova and found that root hairs had little contribution to Si uptake. Similar
Gilroy, 2002). Thus, root hairs are the active and principal zone results were also obtained by Bates and Lynch (2000a, 2000b)
of absorption of nutrient ions. They are assumed to have a higher with root hair defective mutants of Arabidopsis.
influx per unit area than that of the root axis (Gahoonia and Ahn et al. (2004) found that among the K+ transporter
Nielsen, 1998). According to the calculation of Claassen and KT/KUP genes in Arabidopsis, ten KT/KUPs were expressed
Steingrobe (1999), root hairs are more efficient than the root in root hairs, but only five were expressed in root tip cells. This
cylinder in drawing advantage from the laws of diffusion. Since also suggests an important role for root hairs in K+ uptake and
feeding roots often have radii between 50 and 150 µm, whereas transport.
the radius of root hairs is less than 5 µm, the specific soil volume
of root hairs is significantly larger than that of roots. IV. PHYSIOLOGICAL MECHANISMS OF NUTRIENT
Root hairs not only extend the absorptive surface of roots, UPTAKE AND TRANSPORT IN ROOTS
but also are able to grow into small pores and into soil particles.
These characteristics allow root hairs to play an important and A. Kinetic Mechanism
suitable role in intercepting and taking up particularly immobile Ions are taken up by the root and move into xylem by travers-
or slowly mobile nutrients such as phosphorus and iron bound ing several layers of plasma membrane. Many studies have
to soil fractions (Jungk, 2001). Wild-type barley (Hordeum vul- shown that ion movement across the cell membrane is highly
gare L.) is able to absorb more P in a low-P field and to produce sensitive to changes in temperature and oxygen concentration,
more shoot biomass than the hairless mutant brb (Gahoonia, metabolic inhibitors, and light and carbohydrate availability,
et al., 2001; Gahoonia and Nielsen, 2003). The formation and strongly suggesting that nutrient uptake and transport in roots
growth of root hairs are assumed to be induced or triggered by P- are an energy-dependent process. This hypothesis was supported
limited conditions (Reid, 1981; Jungk et al., 1990; Jungk, 2001). by kinetic studies initiated by Epstein and coworkers (Epstein
When the P supply was improved, root hair length and number et al., 1963; Epstein, 1972, 1976). They introduced the concept
were inversely related to the P concentration in rape, spinach, of membrane-bound transporters or carriers and suggested the
and tomato plants (Jungk, 2001). Similarly, the root hair den- multiphasic nature of transport systems. Now it is commonly
sity of Arabidopsis was also highly regulated by P availability, accepted that in many cases, there are two types of plasma mem-
increasing significantly in roots exposed to conditions of low P brane carriers in roots; high-affinity transport systems (HATS)
availability (Ma et al., 2001c). Ma and coworkers suggested that and low-affinity transport systems (LATS) that are specific for
the larger number of root cortical cells and smaller root epider- most inorganic ions and that follow a saturation kinetic model.
mal cell size in P-deficient roots might result in an increase in the These carriers are considered to function at low and high exter-
number of trichoblasts and increased likelihood of trichoblasts nal ion concentrations, respectively (Epstein, 1976; Marschner,
to form hairs. Grierson et al. (2001) reviewed at least 40 genes 1995; Glass, 2002).
in Arabidopsis that affect root hair initiation and development. For NO− 3 , kinetic studies indicate that roots have at least three
Many of these may be responsive to P deficiency. distinct uptake systems. The high-affinity systems for NO− 3 in-
Peculiarities of root-hair development induced under Fe de- clude the well-known inducible high-affinity transport system
ficiency differ from those produced under ordinary conditions (iHATS) and the constitutively expressed high-affinity system
or P deficiency (Bell et al., 1988; Landsberg, 1996). Forma- (cHATS). The iHATS is strongly induced by the external NO− 3
tion of root hairs and swelling of root tips are induced during supply, while the cHATS just operates at low external NO− 3 con-
latent Fe deficiency before significant growth reduction occurs centration in the range of 0.2 mM, even without prior NO− 3 sup-
(Landsberg, 1996). Müller and Schmitt (2004) found that the in- ply (Glass and Siddiqi, 1995). The cHATS has the higher affinity
crease in root hair density in P-deficient Arabidopsis plants was for NO− 3 (K m about 6–20 µM) than the iHATS (K m about 13–
mainly achieved by the formation of extra hairs over both tan- 79 µM) (Forde and Clarkson, 1999), but the iHATS has a much
284 H. WANG ET AL.

greater capacity for NO− 3 uptake; in barley, the Vmax for iHATS
saturation of protoplasmic constituents that decreased further
activity following induction with 100 µM NO− 3 was over 25
uptake, but recently, it is believed that plants require internal
times higher than the cHATS activity (Siddiqi et al., 1991). The levels of particular ions that are controlled by a homeostatic
third system is a low-affinity system, which operates when the process (Marschner, 1995; Glass, 2002).
external NO− 3 concentration reaches values of >1 mM (Siddiqi
A typical example is the cytosolic free calcium concentra-
et al., 1990; Glass et al., 1992). tion, which is maintained at the submicromolar level, and is
Influx of ions via HATS is rapidly downregulated or upreg- affected primarily by balancing cytoplasmic Ca2+ influx and
ulated in response to a respective increase or decrease of the efflux. Small variations in these levels trigger physiological re-
external ion concentration. Efflux of ions also rises as inter- sponses mediated via Ca2+ -binding proteins as signals (Sanders
nal ion concentrations rise in response to increasing external et al., 1999, 2002). A voltage-independent cation (VIC) channel
ion concentration. In contrast, ion efflux falls as internal ion identified in the plasma membrane of wheat (Triticum aestivum)
concentration declines, when the ion concentrations of exter- root cells provides perpetual Ca2+ influx into root cells; thus, it
nal solutions are reduced (Glass, 2002). For example, it appears may affect cytosolic Ca2+ homeostasis (White et al., 2002a).
that two different transport systems mediating root Zn2+ uptake More detailed information will be further described in section
are a high-velocity, low-affinity system (K m = 2–5 µM) and V-D.
a low-velocity, high-affinity system (K m = 0.6–2 nM) that is The K+ concentration in the cytosol of the plant cell is main-
probably the dominant transport system under low soil Zn con- tained at approximately 80–100 mM, except under K+ starva-
ditions (Hacisalihoglu et al., 2001). As a consequence to these tion. This range of K+ concentration in the cytoplasm is sug-
effects, net uptake (influx minus efflux) via HATS declines as gested to be a strict requirement for protein synthesis from
external Zn2+ ion concentration increases. However, the decline mRNA (Leigh, 2001). Membrane transport of K+ plays an im-
of ion influx is generally much larger than the increase of efflux portant role in the homeostasis of plants subjected to K depletion
(Kronzucker et al., 1999) and under these conditions, Zn2+ ion in the environment. The change of membrane potential, turgor
influx via LATS assumes a greater importance. pressure and ABA signal may regulate K+ transport process
Ion fluxes via the HATS result from thermodynamically ac- (Leigh, 2001). However, Kronzucker et al. (2003) suggested that
tive fluxes against electrochemical gradients of ions (Glass, strict K+ homeostasis does not occur in the cytosol. The data
2002). It has been suggested that the proton gradient across the from 42 K radiotracer experiments showed that the concentration
plasma membrane serves as the source of free energy for these of K+ in the cytosol of root cells of intact barley (Hordeum
active fluxes (Glass, 2002). vulgare L.) seedlings was held at the minimum of two physi-
Ion uptake via the LATS is thought to be a passive process ological set points, coinciding with two fundamentally distinct
for cations but an active process for anions such as NO− 3 or
modes of K+ transport. Both a pathological (NH+ 4 -induced) and
Pi . These conclusions arise from the application of the Nernst a nonpathological (K+ -dependent) homeostasis in the magni-
equation, using measured electrical potentials across the plasma tude of the cytosolic K+ pool might be involved in parallel in
membrane, together with estimates of external and cytoplasmic the inherent plasticity of cellular K+ fluxes.
ion concentrations (Glass, 2002). Santa Maria and Cogliatti (1988) estimated the amount of
Zn using Zn65 isotope and found that 8% of the root Zn
was in the cytoplasm and 76% in the vacuole, while the rest
B. Nutrient Ion Homeostasis was in the cell wall. Vacuolar ion accumulation may play an
Plants are exposed to a diverse range of nutrient ion con- important role in regulating and maintaining the requirement
centrations, which can vary by several orders of magnitude. It for a particular ion concentration, in some cases alleviating
is crucial for plants to maintain the required concentrations of the potential for toxic effects of excess ion accumulation. In
essential nutrient ions for optimal biochemical and physiologi- view of the fact that the cellular activity of free Zn2+ is very
cal functioning, while at the same time minimizing the damage low, the question of how Zn gets distributed in the cell be-
from nonessential ions. The complex homeostatic mechanisms comes very important. Metallothionein is a cellular protein
may be regulated or controlled by combined processes of up- reservoir for Zn and could deliver Zn to sites where it is re-
take, transport, distribution, and detoxification (Grusak et al., quired. Therefore, metallothionein could be a chaperone, func-
1999; Reid, 2001; Clemens, 2001; Mimura, 2001; Schmidt, tioning either as a Zn donor or acceptor (Maret and Vallee,
2003). 1998).
As early as 1906, Brezeale found that the removal of a partic- Another possible component of Zn homeostasis could be in-
ular nutrient from complete nutrient solution could lead to the volved in the regulation of the expression of transporter genes
uptake of one nutrient by wheat plants to increase by up to four associated with Zn nutrition by changes in cellular Zn status.
times when it was supplied again later. Hoagland and Broyer Lasat et al. (2000) showed that in Thlaspi arvense, a Zn trans-
(1936) also discovered that there are upper limits for nutrient porter was expressed in roots only in response to Zn deficiency.
accumulation in the roots of barley plants. Those phenomena Ramesh et al. (2003) also showed differences in the level of Zn
were once thought or explained to be osmotic effects or salt transporter gene expression in rice plants under Zn deficiency.
 ROOT DEVELOPMENT AND NUTRIENT UPTAKE 285

The OsZIP3 transcript could be detected in both roots and shoots (acetic, ascorbic, benzoic, citric, ferulic, malic, and oxalic acids,
under Zn-depleted conditions. The OsZIP1 transcript was of etc.), and phenolic compounds. Some of these compounds, es-
lower abundance and its expression was only induced in roots pecially the phenolics, influence the growth and development of
and shoots, while the OsZIP2 transcript was visible in roots surrounding plants and soil microorganisms (Uren, 2000; Bertin
and, to a lesser extent, in shoots after the plants were deprived et al., 2003).
of Zn. Root exudates are released in three major ways from living
Various techniques have been developed for the quantifica- root systems; either through diffusion, ion channels, and vesicle
tion of cellular pool sizes of ions in plant roots, which is believed transport. Low molecular weight organic compounds are gener-
to be essential for understanding the homeostasis mechanism. ally released via a passive process (diffusion) due to the steep
For example, cytosolic nitrate concentration has been estimated concentration gradients between the cytoplasm of intact root
by different methods, including microelectrodes (van der Leij cells and the soil. Some chemicals such as specific carboxylates
et al., 1998), determinations of NR activities (King et al., 1992), (e.g. citrate, malate, oxalate), which are normally exuded in high
tracer influx profiles (Presland and McNaughton, 1984), nuclear concentrations, cannot easily diffuse through root membranes.
magnetic resonance (Belton et al., 1985), and compartmental In these cases, anion channels mediate the controlled release
analysis by tracer efflux (CATE) (Britto and Kronzucker, 2001, of these products by roots. High molecular weight compounds
2003; Siddiqi and Glass, 2002). However, the results of differ- generally may be transported from endoplasmic reticulum (ER)-
ent measurements of nitrate pools in compartments of plant root originating vesicles that fuse with the cell membrane and are
cells have been controversial, because cytoplasmic/cytosolic released to the apoplast (Neumann and Römheld, 2000, 2002;
NO− 3 concentration can vary several-fold, from 0.01 to 0.1 mm Bertin et al., 2003; Walker et al., 2003).
at the lower level, or even be at undetectable levels, to 50 mM Through diverse mechanisms, root exudates play a funda-
at the higher level when measured by various methods (Britto mental role in mineral nutrition of plants and are believed to be
and Kronzucker, 2001, 2003; Siddiqi and Glass, 2002). Further mediators of mineral acquisition in low-nutrient environments
quantification of reliable methods remain to be tested. (Dakora and Phillips, 2002). They either contain some signals
or act as regulators for microbial growth and function. For ex-
ample, phenolics and aldonic acids in root exudates can serve as
C. Rhizosphere and Root Exudation major signals to Rhizobiaceae bacteria that form root nodules in
The zone of soil of about 0 to 2 mm away from the surface of which N2 is reduced to ammonia. Flavonoid compounds can in-
living roots is significantly influenced by them, and is referred duce spore germination or hyphal growth, and also affect devel-
to as the rhizosphere. The rhizosphere can be defined as the opment of mycorrhizal fungi (Dakora and Phillips, 2002), which
volume of soil influenced by root activity; hence, the physical, are crucial for phosphate uptake and root elongation (Marschner,
chemical and biological characteristics within this zone differ 1995).
drastically from those of bulk soil (Marschner, 1995; Neumann Some root exudates directly control rhizosphere processes
and Römheld, 2000, 2002). to enhance nutrient uptake and assimilation. For example, or-
An actively growing root system, including lateral roots and ganic acids from root exudates can solubilize unavailable soil Ca,
root hairs, releases large quantities of root exudates. In young Fe and Al phosphates (Dakora and Phillips, 2002; Jones et al.,
plants, root exudates are quite significant and may represent up to 2003). Extracellular enzymes from root exudates can mediate the
30% of total dry matter production (Bertin et al., 2003). The ex- release of P from organic compounds thereby making them read-
udates are composed of carbon-containing compounds derived ily available for plant root uptake and utilization. Several types
from photosynthetic products and noncarbon-containing com- of compounds such as organic acids and phytosiderophores in-
pounds such as H+ , inorganic ions, water, and electrons (Uren, crease iron availability through chelation. These acids in the root
2000). Root exudates can also be grouped into high molecular exudates can markedly lower rhizosphere pH, which effectively
weight and low molecular weight compounds. The amount and mobilizes some nutrients in soils (Kirk, 1999, 2002; Dakora and
composition of root exudates varies among plant species, culti- Phillips, 2002; Neumann and Römheld, 2002; Tanimoto, 2005,
var, age, and stress factors (Uren, 2000; Bertin et al., 2003). High for physiology of apoplast acidification).
molecular weight compounds include carbohydrates (polysac-
charides, mucigel), enzymes, fatty acids, tannins, flavonoids,
growth regulators, nucleotides, steroids, terpenoids, alkaloids, V. ROOT NUTRIENT TRANSPORT SYSTEMS
and polyacetylenes. Vitamins are also released in large quanti- AND THEIR MOLECULAR BIOLOGY
ties. Many of these compounds are involved in either primary Three main types of transport proteins accommodate nutrient
or secondary plant metabolic processes, and also in plant de- transport systems in the plasma membrane of plants: ion pumps,
fense. On the other hand, a variety of low molecular weight or- channels, and transporters (or carriers) (Figure 1) (Chrispeels
ganic compounds include sugars (arabinose, fructose, glucose, et al., 1999; Taiz and Zeiger, 2002). Ion pumps mediate the diffu-
maltose, mannose, oligosaccharides), amino acids (arginine, as- sion of ions using ATP directly as an energy source to pump ions
paragine, aspartic, cysteine, cystine, glutamine), organic acids across membranes, usually against a potential energy gradient.
286 H. WANG ET AL.

FIG. 1. Overview and classification of various transport systems possibly present in the membrane of plant roots (Refer to Taiz and Zeiger, 2002; Reid and
Hayes, 2003).

For example, a H+ -ATPase can pump H+ ions to produce poten- metabolites. Their activity can be investigated by studying the
tial energy in the form of pH and electrical potential gradients electric currents associated with the flow of ions. Transporters
for driving many other secondary transport processes (Sze et al., transport nutrient ions by utilizing gradients of electrical poten-
1999). Ion channels are selective pores with protein structures tial or concentration generated by the H+ -ATPases (Tanner and
that span membranes and enable the diffusion of ions down po- Caspari, 1996; Taiz and Zeiger, 2002). Anion transporters are
tential energy gradients, allowing transport of nutrient solutes common symporters that normally obtain the necessary energy
by passive diffusion (Hedrich and Schroeder, 1989; Taiz and by simultaneously co-transporting an H+ ion down its electro-
Zeiger, 2002). Flow through a single ion channel is usually rapid, chemical potential gradient. Antiporters, also called exchang-
about 106 –107 ions per channel per second. Channels are not ers, obtain energy by the simultaneous transport of a secondary
static pores but dynamic molecules whose function can be reg- chemical species in the opposite direction to the primary sub-
ulated in response to stimuli, including voltage, pH, and various strate. Transporters play their function at slower rates than ion
 ROOT DEVELOPMENT AND NUTRIENT UPTAKE 287

channels, about 102 –104 ions per channel per second. The orig- differences in the physiological role of these channels between
inal studies suggested that transporters were distinct from chan- the two plant species.
nels, but later some researchers concluded that transporters could Contrary to NH+ −
4 , NO3 taken up by roots need to be reduced
function like ion channels under certain conditions (Cammack in roots or in leaves by NR and nitrite reductase before its as-
and Schwartz, 1996; Fairman et al., 1995; Gassmann et al., similation into organic compounds (Forde and Clarkson, 1999;
1996). Faure et al., 2001). NO− 3 can enter into the vacuole where it acts
Many plant molecular biology studies have been reveal- as a general osmoticum or serves as an N reservoir (der Leij
ing more genes associated with plant nutrient transport sys- et al., 1998). All these processes require the transport of NO− 3
tems. An excellent database of transporter genes and a database or nitrite through different cellular membranes.
of plant nutrient transporter proteins are available on two It is assumed from thermodynamic calculations that NO− 3
websites, http://tcdb.ucsd.edu/tcdb and http://plantst.sdsc.edu. influx is an active process (Glass and Siddiqi, 1995). A number
Dunlop and Phung (2002) and Reid and Hayes (2003) have re- of reviews dealing with various aspects of NO− 3 transport have
viewed and summarized the main groups of transport proteins been published recently (Daniel-Vedele et al., 1998; Crawford
for various nutrients. These transport systems are found in var- and Glass, 1998; Forde, 2000, 2002; Williams and Miller, 2001;
ious organs in plants. In this review, we mainly describe recent Glass et al., 2001; Orsel et al., 2002).
molecular information on the families of nutrient transport sys- Molecular research has identified two main NO− 3 transporter
tems in plant roots (Figure 1). gene families, referred to as NRT1 and NRT2 (Forde, 2000;
Williams and Miller, 2001). Both families contain several mem-
bers. No primary sequence homology is found between them,
A. Nitrogen but they share the same structural topology, with 12 trans-
Plants acquire NH+ −
4 and NO3 , two N sources, through dif- membrane domains, distributed in two sets of six helices con-
ferent transport systems for growth and development. nected by a cytosolic loop (Forde, 2000; Orsel et al., 2002).
The first NH+ 4 transporter genes (AMT) were identified The NRT1 transporter was originally assumed to be involved
from yeast (Saccharomyces cerevisiae) and Arabidopsis (Marini in LATS (Huang et al., 1996; Touraine and Glass, 1997), but it
et al., 1994; Ninnemann et al., 1994). In 1996, Lauter et al. appears also to be involved in high-affinity NO− 3 uptake and is
found that three NH+ 4 transporters were preferentially expressed a dual-affinity NO− 3 transporter, involved in multiple phases of
in root hairs of tomato and suggested an important role of these NO− 3 uptake (Wang et al., 1998; Liu et al., 1999). NRT2 genes
genes in uptake of N. Six putative NH+ 4 transporter genes have are responsible for a major contribution to the HATS. NRT2
so far been identified in the Arabidopsis genome. mRNA increases rapidly upon first supplying NO− −
3 to NO3 -
Gazzarrini et al. (1999) showed that high-affinity NH+ 4 up- starved roots and subsequently decreases when the NO3 level is−

take in roots was regulated at the transcriptional level by the maintained (Krapp et al., 1998; Zhuo et al., 1999; Vidmar et al.,
physiological status of the plant and by substrate affinities of in- 2000b).
dividual expressed members of the AMT1 gene family. The three The NRT2 gene family consists of seven members in Ara-
AMT1 transporters, AtAMT1;1, AtAMT1;2, and AtAMT1;3, bidopsis thaliana. Glass et al. (2002) grouped these NRT2 genes
isolated from Arabidopsis showed different affinities for NH+ 4 into three categories: 1) NRT2.1 and NRT2.2, which are tran-
when expressed in roots. Transcript levels of AtAMT1;1, which siently upregulated upon provision of NO− 3 and subsequently
possesses an affinity in the nanomolar range, steeply increased downregulated; 2), NRT2.3, NRT2.5 and NRT2.6, which are
with NH+ 4 uptake in roots under low N conditions, whereas those constitutively expressed; and 3) NRT2.4 and NRT2.7 which
of AtAMT1;3 increased slightly, with AtAMT1;2 being more con- are immediately down-regulated upon NO− 3 exposure. More-
stitutively expressed. Shelden et al. (2001) also indicated a pre- over NRT2.1 and NRT2.2 are by far the most highly expressed
eminent role for AtAMT1;1 in NH+ 4 uptake across the plasma among NRT2 genes in Arabidopsis roots. However, Nazoa et al.
membrane of NO− 3 -fed and N-deprived root cells. Expression (2003) found that the NRT2.1 gene appeared to be expressed
of the AtAMT1;1 gene in Arabidopsis roots increased approx- predominantly not only in roots, but also in leaf hydathodes.
imately four-fold in response to N deprivation. This coincided Furthermore, NRT2.1 expression increased rapidly during early
with a similar increase in high-affinity NH+ 4 uptake by these vegetative growth, peaked prior to floral stem emergence, and
plants. In contrast, the expression of AtAMT1;2 in roots was decreased to very low levels in flowering and silique-bearing
insensitive to changes in N nutrition. plants. In Nicotiana plumbaginifolia, NRT2 transcripts are more
Voltage-insensitive cation channels (CICC) in roots also abundant in the epidermal and endodermal cells close to the root
have a high permeability to NH+ 4 . The selectivity sequence tip, and in the epidermis and lateral root primordia in the ma-
of nonselective cation channels studied with planar lipid bi- ture part of the root (Krapp et al., 1998). From roots of wheat
layers obtained from wheat (Davenport and Tester, 2000) was (Triticum aestivum), Zhao et al. (2004) isolated TaNRT2.3, a
NH+ + +
4 >K >Na , but in Arabidopsis, the result obtained in a high-affinity NO− 3 transporter, which is closely related to other
patch-clamp study showed K+ >NH+ +
4 >Na (Demidchik and NRT2 proteins from plants and is a polypeptide with 507 amino
+
Tester, 2002). The two different NH4 conductances may reflect acids and 12 transmembrane domains.
288 H. WANG ET AL.

B. Phosphorus under Pi -sufficient conditions but with highest concentrations

Transport of inorganic phosphate (Pi ) through plant mem- in root hairs. However, in situ hybridization studies demon-
branes is mediated by a number of families of transporter pro- strated that the LePT1 mRNA was detectable in peripheral cell
teins. There are two main types of P transport systems, named layers such as rhizodermal and root cap cells, suggesting cell-
Pht1 and Pht2. Pht1 transporters can be divided into two sub- specific expression of LePT1 in the root. Under Pi -deprivation
families, those that are expressed in both the root and the shoot conditions, a marked increase in transcript abundance was de-
and those that are specifically expressed in roots during P depri- tected in the central cylinder of the root proximal to the root
vation (Bucher et al., 2001). There are nine members of the Pht1 tip (Daram et al., 1998). However, Liu et al. (1998) found that
family in the Arabidopsis genome. Members of this family are LePT1 mRNA was detectable in both root and shoot tissues of
suggested to be H2 PO− + +
4 /H symporters by utilizing the H gra- tomato, and transcript levels increased in both tissues upon Pi
+
dient at the plasma membrane to drive H /Pi symport activity. starvation. In contrast, LePT2 mRNA was detectable exclusively
Most of the genes of the Pht1 family that are expressed in roots in roots, and its concentration was strongly enhanced during Pi
are upregulated in P-stressed plants. Two members of the Pht1 deprivation.
family have also been isolated from cluster roots of white lupin Chiou et al. (2001) confirmed the predominantly transcrip-
(Lupinus albus) (Smith et al., 2003). Pht1 transporters presum- tional regulation and the rhizodermal localization of another
ably play a major role in P acquisition from the soil solution member of the Pht1 family, MtPT1 from Medicago truncatula.
into the root (Bucher et al., 2001). Members of the Pht1 family Enhanced Pi transporter gene expression under P limiting con-
are assumed to be high-affinity Pi transporters (Bucher et al., ditions leads to an increased number of transport sites and thus
2001) because a Km value of 3.1 µM was measured in cul- most likely to an increase in Vmax of Pi uptake on a root area ba-
tured tobacco cells expressing the gene encoding PHT1 from sis. Liu et al. (2001) characterized a high-affinity type Pi uptake
Arabidopsis (Mitsukawa et al., 1997). gene (LaPT1) from cluster roots of white lupin (Lupinus albus)
The first genes encoding putative plant Pi transporters were that shows highly intensified expression in P-deficient plants.
isolated from Arabidopsis (Muchhal et al., 1996; Leggewie The transcript was expressed strongly under P-deficient condi-
et al., 1997; Mitsukawa et al., 1997; Smith et al., 1997). Re- tions (both non-proteoid roots and proteoid roots) but became
cently, a nomenclature for Pht1 proteins in Arabidopsis based low to non-detectable under P-sufficient conditions. In potato
on the sequences present in the whole Arabidopsis genome has (Solanum tuberosum), three high-affinity transporters, StPT1,
been proposed (Poirier and Bucher, 2002; Rausch and Bucher, StPT2 and StPT3, have been cloned and sequenced (Leggewie
2002) and includes all nine Pht1 proteins, numbered Pht1;1 et al., 1997; Rausch et al., 2001). StPT1 mRNA is present not
to Pht1;9 (http://ukcrop.net/perl/ace/tree/Mendel-CPGN?name only in roots but also to a lesser extent in the source leaves,
=Pht1&class=GeneFamily). In contrast to the nine different flowers and tubers. Although amounts of StPT1 mRNA in the
Pht1 genes detectable in the Arabidopsis genome, in plant root increase in response to P depletion, a low level of constitu-
species like Medicago, tomato (Lycopersicon esculentum) and tive expression can also be detected throughout the plant. StPT2
potato (Solanum tuberosum), a relatively low number of Pht1 mRNA, however, is only detected by northern blots in roots
transporter genes have been identified (Rausch and Bucher, after P depletion (Gordon-Weeks et al., 2003) while StPT3 is
2002; Poirier and Bucher, 2002). only detected in roots colonized by mycorrhizae (Rausch et al.,
All the members of the Pht1 family of plant Pi transporters ex- 2001).
hibit high sequence similarity. The putative proteins are similar The first member of the Pht2 family of plant Pi transporters,
in size, contain 12 putative transmembrane domains (TMs) and ARAth;Pht2;1, was cloned from an Arabidopsis cDNA library
have both their N- and C-termini oriented towards the inside of (Quigley et al., 1996; Daram et al., 1999). The predicted Pht2;1
the cell (Raghothama, 1999; Smith, 2001). Another typical fea- protein with its 12 transmembrane (TM) subunits is structurally
ture is a large hydrophilic loop between TM6 and TM7, resulting similar to the members of the Pht1 family, but distinct in se-
in the characteristic 6 + 6 configuration of many transporter pro- quence and have a large hydrophilic loop between TM8 and
teins belonging to the major facilitator superfamily (Pao et al., TM9 (Daram et al., 1999). Pht2;1 from Arabidopsis thaliana is
1998). Misson et al. (2004) showed that Pht1;4 was mainly ex- predominantly expressed in the shoot. It is now suggested that
pressed in roots of Arabidopsis grown in a medium with limited Pht2;1 is involved in loading of above-ground organs, especially
inorganic phosphate (Pi) supply, primarily in the epidermis, the leaves, with P (Bucher et al., 2001). A chloroplastic localization
cortex and the root cap. The expression of Pht1;4 was also ob- of Pht2;1 protein has been demonstrated in Arabidopsis (Ferro
served at the lateral root branch points on the primary root and et al., 2002; Versaw and Harrison, 2002).
in the stele of lateral roots, implying that Pht 1;4 may play a However, it is proposed that there is a third family
role in phosphate absorption and translocation from the growth (Pht3) of Pi transporter genes, the members of which are
medium to the different parts of the plant. highly conserved within the mitochondrial transporter fam-
Two Pi transporters, LePT1 and LePT2, have been studied ex- ily. Further sequence information about plant mitochon-
tensively. Transcript levels of LePT1 in tomato (Lycopersicon drial Pi transporters can be found at http://ukcrop.net/perl/
esculentum) seedlings were detectable in all vegetative organs ace/tree/Mendel-CPGN?name=Pht3&class=GeneFamily).
 ROOT DEVELOPMENT AND NUTRIENT UPTAKE 289

C. Potassium independent cation currents when added to the cytosolic side of

Transmembrane movement of K+ is catalyzed by channel and Arabidopsis root protoplast patches.
transporter proteins, and energized by the negative membrane K+ -uptake transporters isolated from bacteria are named
potential of plant cells. In addition, transporters may use H+ and KUP and high-affinity K+ transporters from fungi are named
in some cases Na+ gradients or ATP hydrolysis to energize K+ HAK. The homologues, called KUP/HAK/KT transporters, are
translocation (Mäser et al., 2002). also present in plants, which make a large family with 13 mem-
In the early 1990s, two K+ channels were identified in Ara- bers in Arabidopsis (Mäser et al., 2001) and at least 17 mem-
bidopsis, which was regarded as the first mineral ion transport bers in rice (Bãnuelos et al., 2002). Little is known about the
system analyzed at the molecular level. Over the past few years, structure of these transporters (Mäser et al., 2002; Véry and
a large number of genes encoding K+ transport systems have Sentenac, 2003). Those gene candidates for K+ transporters
been identified with the advancement of molecular approaches in in the KUP/HAK/KT family are involved in the process of
association with electrophysiological analyses. These transport root K+ uptake and transport. For example, AtKUP3 (Kim
systems are found in roots, guard cells, and growing pollen tubes et al., 1998), AtKUP4 (Rigas et al., 2001) and AtHAK5 (Rubio
in various plants (Véry and Sentenac, 2003). There are at least et al., 2000) from Arabidopsis and barley (Hordeum vulgare
seven major families of K+ transport membrane proteins that L.) HvHAK1 (Santa Maria et al., 1997) are expressed in roots.
have varying selectivity and permeability to K+ in Arabidop- Ten AtKT/KUPs are expressed in root hairs, but only five are
sis plant roots (Mäser et al., 2001, 2002; Véry and Sentenac, expressed in root tip cells (Ahn et al., 2004). The expression of
2003). AtKUP3 and HvHAK1 is induced by K+ starvation (Santa Maria
Shaker-type K+ channels are made up of four subunits ar- et al., 1997; Kim et al., 1998). HvHAK1, AtKUP1, AtKUP4
ranged around a central pore. The hydrophobic core of each and AtHAK5 exhibit high-affinity K+ uptake in yeast (Sac-
subunit consists of six TM domains, the fourth with a rep- charomyces Cerevisiae) (Rigas et al., 2001; Rubio et al., 2000;
etition of basic residues acting as a voltage sensor (Mäser Santa Maria et al., 1997) and in transgenic Arabidopsis cells
et al., 2002; Véry and Sentenac, 2003), thereby controlling (Kim et al., 1998) and roots (Rigas et al., 2001; Gierth et al.,
channel gating. They can be subdivided into two subfami- 2005).
lies; depolarization-activated outward-rectifying K+ channels In terms of transcript levels, two AtKUPs are up-regulated in
(KCO) and hyperpolarization-activated inward-rectifying K+ Arabidopsis roots by K+ deprivation (Kim et al., 1998). In rice
channels (KIRC). In Arabidopsis, there are 9 genes encoded roots and shoots (Bãnuelos et al., 2002) and in roots of barley
by the Shaker family. In roots, an AKT1 channel, belonging to (Hordeum vulgare L.), wheat (Triticum aestivum) (T.B. Wang
KIRC, mediates root K+ uptake when the external concentra- et al., 1998) and tomato (Lycopersicon esculentum) (Wang et al.,
tion is in the micromolar range, demonstrating that a channel 2002), several KUP/HAK/KT genes were up-regulated in re-
can contribute to high-affinity K+ uptake (Hirsch et al., 1998). sponse to K+ deprivation. Ahn et al. (2004) found that in Ara-
Moreover, it is insensitive to inhibition by NH+ 4 (Spalding et al., bidopsis plants, AtHAK5 was the only gene in this family that was
1999). Another channel, stelar K+ outward rectifier (SKOR), is up-regulated upon K+ deprivation and rapidly down-regulated
expressed in stelar tissues of the root (Gaymard et al., 1998), with resupply of K+ .
which may mediate K+ release into the xylem sap. Two-pore High-affinity K+ transporters (HKT) are likely to be present
K+ channels are composed of subunits with two P-loops each in all plant species, but in Arabidopsis thaliana only one member
(Mäser et al., 2002). The first-identified gene, KCO1, encod- (AtHKT1) has been detected (Mäser et al., 2001, 2002; Véry and
ing a two-pore K+ channel, was characterized in Arabidopsis, Sentenac, 2003). It was suggested that Arabidopsis AtHKT1 fa-
and was activated by cytosolic Ca2+ (Czempinski et al., 1997). cilitates Na+ homeostasis in plant and through this function reg-
Its contribution to root K+ uptake and transport remains to be ulates K+ nutrient status (Uozumi et al., 2000; Rus et al., 2004).
investigated. To date, the family of two-pore K+ channels in HKT transporters are hypothesized to have a core structure with
Arabidopsis includes 6 members. eight TM subunits and four P-forming domains, with the four
Cyclic-nucleotide-gated channels (CNGCs) are gated by P-loops lining a central P (Véry and Sentenac, 2003). The HKT1
cyclic nucleotides such as cGMP or cAMP (Broillet and gene could be expressed in the root cortex of wheat (Schachtman
Firestein, 1999; Mäser et al., 2002) and are further modulated and Schroeder, 1994) by K+ starvation (Wang et al., 1998).
by calcium and calmodulin (CaM) (Köhler et al., 1999). The A family of cation/proton antiporters, composed of six puta-
CNGCs structure is related to that of the Shaker family (Henn tive K+ /H+ antiporters has been identified in Arabidopsis (Mäser
et al., 1995) but without the high K+ selectivity motif in the P- et al., 2001, 2002). Their tissue and subcellular localization are
domain (Finn et al., 1996). The family of CNGCs in Arabidopsis still unknown (Véry and Sentenac, 2003). They may play im-
consists of 20 genes (Mäser et al., 2001, 2002). CNGCs seem to portant roles in K+ homeostasis by loading K+ into vacuoles or
be permeable to monovalent cations and Ca2+ , but very little is other acidic compartments (Mäser et al., 2001, 2002).
known about plant CNGC ion selectivity, localization, or func- In addition, a K+ -permeable, low-affinity cation transporter
tion (Véry and Sentenac, 2003). Maathuis and Sanders (2001) (LCT), has been identified in both roots and leaves of wheat.
found that cGMP and cAMP inhibited nonselective, voltage- Nonselective cation conductance has been described in vivo in
290 H. WANG ET AL.

wheat roots, showing mediation of low-affinity transport of all 3H+ /1Ca2+ (Blackford et al., 1990). Eleven genes encoding pu-
monovalent ions and Ca2+ (Schachtman et al., 1997). tative H+ /Ca2+ -antiporters (AtCAX) have been identified in the
genome of Arabidopsis thaliana (Hirschi, 2001; Mäser et al.,
2001). The transporters AtCAX1, AtCAX2 and AtCAX4 are lo-
D. Calcium cated at the tonoplast (Hirschi, 2001; Cheng et al., 2002, 2003).
Ca2+ may traverse the root either through the cytoplasm of The AtCAX1 antiporter exhibits both a high affinity and high
cells linked by plasmodesmata (the symplast) or through the specificity for Ca2+ . By contrast, the AtCAX2 transporter is a
spaces between cells (the apoplast) (White, 2001). The apoplas- high-affinity, high-capacity H+ /heavy metal cation antiporter.
tic pathway is relatively nonselective among divalent cations and The cation specificity of other AtCAXs is still unknown, but
localizes in the root tip where the tight barrier of the Casparian may be determined by a specific stretch of nine amino acids
band and suberized endodermal cells are not well developed termed the Ca2+ domain (Shigaki et al., 2002).
(White, 2001; White et al., 2002a, 2002b). Thus, the symplastic Ca2+ influx to the cytosol is catalyzed by calcium-permeable
pathway allows the plant to control the rate and selectivity of channels, which can be classified into the following three types
Ca2+ transport to the shoot (Clarkson, 1984, 1993; White, 2001). based on their voltage dependence: depolarization-activated
Ca2+ efflux from the cytosol to either the apoplast or intracel- (DACC), hyperpolarization-activated (HACC) and voltage-
lular organelles against its electrochemical gradient requires ac- independent (VICC) cation channels (White, 2000; Miedema
tive transport. This is catalyzed by Ca2+ -ATPases and H+ /Ca2+ - et al., 2001; Sanders et al., 2002). Each type of channel is perme-
antiporters (Sze et al., 2000; Hirschi, 2001). able to a wide range of both monovalent and divalent cations in
Plant Ca2+ -ATPases that belong to P-type ATPases, con- addition to Ca2+ . Most DACCs are activated significantly at volt-
tain two distinct families, type IIA and type IIB (Evans and ages more positive than about −150 to −100 mV (White, 1998).
Williams, 1998; Geisler et al., 2000; Sze et al., 2000; Axelsen HACCs have been identified in root cells (Kiegle et al., 2000;
and Palmgren, 2001; Garciadeblas et al., 2001). The first family Véry and Davies, 2000; Foreman et al., 2003) and cells of other
(the P-type ATPase IIA family) lacks an N-terminal autoregula- plant organs (Pickard and Ding, 1993; Blumwald et al., 1998;
tory domain. Four members of this family, termed AtECAs1 to Stoelzle et al., 2003; Perfus-Barbeoch et al., 2002). They are ac-
4, have been identified in the Arabidopsis genome (Axelsen and tivated at voltages more negative than about −100 to −150 mV,
Palmgren, 2001). They are likely to be present in the plasma but increasing the concentration of Ca2+ in the cytosol shifts
membrane, tonoplast and the ER/Golgi apparatus. In tomato their activation potential to more positive voltages in root hairs
(Lycopersicon esculentum), two transcripts of a type IIA Ca2+ - (Véry and Davies, 2000).
ATPase (LeLCA1) were observed in phosphate-starved roots Many distinct VICCs are present in the plasma membrane
that correlated with two distinct protein isoforms (120 and 116 of plant cells that differ in cation selectivity, voltage depen-
kDa) located in the plasma membrane and tonoplast of root cells, dence and pharmacology (White et al., 2002a; Demidchik et al.,
respectively (Navarro-Avino et al., 1999). The second family of 2002a, 2002b). They are likely to provide a weakly voltage-
plant Ca2+ s-ATPases (the P-type ATPase IIB family) is charac- dependent Ca2+ influx to cells under physiological ionic con-
terized by an autoinhibitory N-terminal domain that contains ditions (White and Davenport, 2002; Demidchik et al., 2002a).
a binding site for Ca-CaM plus a serine-residue phosphory- It has been suggested that Ca2+ influx through VICCs, which
lation site. Their catalytic activity can be modulated by the are open at physiological voltages and are generally insensitive
concentration of Ca2+ in the cytosol either through activation to cytoplasmic modulators, is required to balance the perpetual
upon binding CaM or by inhibition following phosphorylation Ca2+ efflux through Ca2+ -ATPases and H+ /Ca2+ -antiporters to
by Ca2+ -dependent protein kinases (Hwang et al., 2000). Since maintain cytosolic Ca2+ homeostasis in an unstimulated plant
CaM binding sites are generally quite diverse, each type IIB cell. Furthermore, VICCs appear to be the only Ca2+ -permeable
Ca2+ -ATPase may have a different affinity for CaM or may bind channel open at the resting potential of most plant cells
a different CaM isoform. Ten members of the type IIB Ca2+ - (Demidchik et al., 2002a, 2002b; White and Davenport, 2002).
ATPase family, termed AtACAs1, 2 and 4 and AtACAs7 to 13, Several highly selective Ca2+ channels activated by cytosolic
have been identified in the Arabidopsis genome (Axelsen and second messengers such as IP3, IP6 or cADPR are present in the
Palmgren, 2001). These have been detected in various cellu- tonoplast (Allen and Sanders, 1997; White, 2000; Sanders et al.,
lar membranes including the plasma membrane (AtACA8), the 2002). In the ER, a variety of voltage-dependent and ligand-
tonoplast (AtACA4), ER (AtACA2) and the plastid inner mem- activated Ca2+ channels have also been found (White, 2000).
brane (AtACA1). More information is available in the review Some candidate genes for Ca2+ channels have been identified
by White and Broadley (2003). in plants (White et al., 2002a). For example, a single candidate
The H+ /Ca2+ -antiporters present in the plasma membrane gene (At4g03560) for depolarization-activated Ca2+ channels
and tonoplast (Evans and Williams, 1998; Sanders et al., 2002) has been identified in Arabidopsis thaliana. It encodes a protein
are suggested to have a lower affinity for Ca2+ than the Ca2+ - with homology to the α1 subunit of animal voltage-dependent
ATPases, and may also transport Mg2+ . The stoichiometry of Ca2+ channels (Hille, 2001). Mäser et al. (2001) isolated a full-
the dominant H+ /Ca2+ -antiporter in the tonoplast is apparently length cDNA encoding a putative Ca2+ channel (AtTPC1) from
 ROOT DEVELOPMENT AND NUTRIENT UPTAKE 291

Arabidopsis that has two conserved homologous domains, both Pfeiffer and Hager (1993) identified a Mg2+ /H+ antiporter on
of which contain six transmembrane segments (S1–S6) and a tonoplast membranes of roots in Zea mays, which previously
pore loop between S5 and S6 in each domain. This cDNA has had been characterized as a Ca2+ /H+ antiporter. But in fact,
the highest homology with the two pore channel (TPC1) re- Mg2+ /H+ antiporters characterized in tonoplast membrane vesi-
cently cloned from rat. In rice, Hashimoto et al. (2004) isolated a cles from Hevea brasiliensis, the latex rubber plant, were able to
cDNA (OsTPC1) that was homologous to AtTPC1. Kadota et al. physically separate Mg from Ca transport (Amalou et al., 1992,
(2004) identified cDNAs for putative voltage-dependent Ca2+ - 1994).
permeable channels, NtTPC1A and NtTPC1B, from suspension-
cultured tobacco BY-2 cells, which are homologous to TPC1
(two-pore channel). White et al. (2002a) proposed that future F. Sulfur
studies should endeavor to determine the electrophysiological The uptake of sulfate from the soil to plant cells is an
characteristics of the putative Ca2+ -permeable channels encoded energy-independent mechanism performed via proton/sulfate
by these gene families and to identify their physiological coun- co-transporters (Leustek et al. 2000; Saito, 2000; Droux, 2004).
terparts. More works need to be focused on physiological con- Members of sulfate transporter families with high affinity and
sequences of downregulation or overexpression of these genes low affinity for sulfate were identified and found to be similar
to elucidate their physiological roles. to those reported in yeast (Saccharomyces cerevisiae) (Thomas
More detailed information about calcium and calcium chan- and Surdin-Kerjan, 1997; Takahashi et al., 2000; Vidmar et al.,
nels in plants can be found in a series of reviews (White, 2000a).
2000; White et al., 2002a; Demidchik et al., 2002b; White and Processes of sulfate transport in plants include transport
Broadley, 2003). across the plasma membrane, intracellular transport from the
root to the shoot, and redistribution via phloem. Before assim-
ilation, sulfate is reduced in the plastids and stored in the vac-
E. Magnesium uole through local transport into the cell (Takahashi et al., 1997,
Relatively little is known of the proteins mediating Mg2+ 1999, 2000; Shibagaki et al., 2002; Yoshimoto et al., 2002,
uptake and transport in plants. However the CorA (cobalt re- 2003).
sistance) family of Mg2+ transporters has been characterized The first isolation of a higher plant sulfate transporter was re-
in Salmonella typhimurium and Escherichia coli (Kehres and ported from a tropical forage legume, Stylosanthes hamata, by
Maguire, 2002). The yeast (Saccharomyces cerevisiae) protein, functional complementation of the yeast (Saccharomyces cere-
MITOCHONDRIAL RNA SPLICING 2 (MRS2), whose struc- visiae) mutant (Smith et al., 1995). In the past several years,
ture is similar to the bacterial CorA family, has been suggested a number of genes for sulfate transporters were isolated from
as a transporter of Mg2+ across the inner mitochondrial mem- various plant species and characterized (Takahashi et al., 2000;
brane (Gardner, 2003). Recently, a novel family of at least 10 Yoshimoto et al., 2002, 2003; Hawkesford, 2003). In the genome
putative Mg2+ transporter genes was identified in Arabidopsis of Arabidopsis thaliana, about 12 sulfate co-transporter-like
(Schock et al., 2000; Li et al., 2001; Gardner, 2003). All ten are genes were identified and divided in four groups (Takahashi
transcribed but direct evidence that proteins encoded by this fam- et al., 2000; Yoshimoto et al. 2003). These subgroups (AtSultr1
ily transport Mg2+ is lacking (Li et al., 2001). From the results to 4) suggest specialized functions for the transport of sulfate
obtained with mrs2 mutant and alr1; alr2 mutant of yeast (Li between tissues and compartments. According to the protein se-
et al., 2001), and with an aorA− ; MgtA− ; MgtB− triple mutant quences and characteristics, the sulfate transporter gene fam-
of Salmonella (Li et al., 2001), it seems that three members of ily consists of five distinct groups (Hawkesford, 2003). The
the plant MRS2 family transport Mg2+ when their genes are ex- members in group 1 are suggested to be able to encode high-
pressed in microbes (Schock et al., 2000; Li et al., 2001). There affinity transporters. In Arabidopsis, SULTR1;1 and SULTR1;2
may also be differences in the cations transported by each MRS2 are mainly expressed in the epidermis and cortex of root tissues,
protein. Like CorA, MRS2 proteins appear to be able to utilize and transcripts accumulate under sulfate deprivation, indicating
several other divalent cations as substrates (Li et al., 2001). The that they may have a specialized function to import sulfate from
MRS2 family is also present in rice and probably in most plants the soil to the roots (Takahashi et al., 2000; Yoshimoto et al.,
(Gardner, 2003). 2002). The members of group 2 are suggested to have a low-
The plant vacuole seems to play a key role in Mg2+ home- affinity sulfate transport activity when they were expressed in
ostasis in plant cells. Mg2+ entry into the vacuole was proposed yeast (Saccharomyces cerevisiae) mutant; however, their precise
to be mediated by Mg2+ /H+ exchangers (Gardner, 2003). The functions in plants are unclear (Hawkesford, 2003). Takahashi
Arabidopsis vacuolar Mg2+ /H+ exchanger, AtMHX, is highly et al. (2000) indicated that SULTR2;1 protein may specifically
transcribed at the vascular membrane, apparently most abun- be localized in the vascular tissues because SULTR2;1 mRNA
dantly at the xylem parenchyma, and functions as an electro- was abundantly expressed, particularly in the roots of sulfur-
genic exchanger of protons for Mg2+ and Zn2+ ions when ex- starved Arabidopsis plants. Kataoka et al. (2004) suggested that
pressed in tobacco cell lines (Shaul et al., 1999; Shaul, 2002). SULTR3;5, a member of group 3, may be an essential component
292 H. WANG ET AL.

of the sulfate transport system that facilitates the root-to-shoot binding site involved in the transport pathway (Guerinot, 2000;
transport of sulfate in the vasculature. Mäser et al., 2001; Hall and Williams, 2003).
More detailed information about five groups of sulfur trans- The ZIPs have been shown to be involved in uptake and trans-
porters is available in the review by Hawkesford (2003). port of a variety of micronutrient metals in plants, including Fe,
Zn, and Mn (Guerinot, 2000). About 15 ZIP genes in the ZIP
family have been identified in Arabidopsis (Mäser et al., 2001).
G. Micronutrient Metals ZIP1 and ZIP3 are expressed in the roots of Zn-deficient plants
Some micronutrient metals, such as Fe, Cu, Zn, Mn, and Ni, while ZIP4 is expressed in both shoots and roots (Grotz et al.,
are essential for plant growth and development, although they are 1998). ZIP1, ZIP2 and ZIP3 are inhibited by Cu and Cd, whereas
toxic in excess. A large number of membrane transporters and only ZIP3 is inhibited by Mn and Co (Grotz et al., 1998).
metal-binding proteins have been found to be vital for plant roots Two ZIP genes, LeIRT1 and LeIRT2, have now been cloned
to take up adequate levels and to maintain a nontoxic balance of from tomato (Lycopersicon esculentum) and are both predom-
these metal ions. inantly expressed in roots (Eckhardt et al., 2001). LeIRT1, but
Two principal mechanisms for regulation of cytosolic metal not LeIRT2, is strongly enhanced by iron limitation, and together
concentration exist; sequestration into the vacuole by metal/H+ with particular P and K transporter genes, is also up-regulated
antiport and export across the plasma membrane by a metal- by P and K deficiency in the root medium, suggesting a possible
pumping P-type ATPase (Williams et al., 2000; Hall and co-regulation of the transporter genes for certain essential min-
Williams, 2003). A nonselective cation channel may be a erals (Wang et al., 2002). About thirteen ZIP genes have been
route for low-affinity uptake of micronutrient metals (Fe, Cu, cloned from rice (Gross et al., 2003). OsIRT1 from rice, which
Zn, Mn and Ni) (Demidchik et al., 2002b; Reid and Hayes, has high homology to the IRT1 gene in Arabidopsis, is also pre-
2003). Depolarization-activated cation channels (DACC) and dominantly expressed in roots and is induced by Fe and Cu defi-
hyperpolarization-activated cation channels (HACC) appear to ciency (Bughio et al., 2002). Burleigh et al. (2003) detected a Zn
allow entry of a range of divalent cations including many trace transporter cDNA named MtZIP2 from the model legume Med-
metals. Metal cation antiporters capable of transporting Zn and icago truncatula, which encodes a putative 37 kDa protein with
Mn have been identified in the tonoplast vesicles of oat roots 8-membrane spanning domains and has moderate amino acid
(Gonzalez et al., 1999). identity with the Arabidopsis thaliana Zn transporter AtZIP2p.
Three main groups (ZIP, IRI and Nramp proteins) of trace The MtZIP2 gene could be expressed in roots and stems and
metal transporter systems have been identified. These groups it was upregulated in roots by Zn fertilization. Lopez-Millan
operate when plants are subjected to limiting conditions of one et al. (2004) identified six new members of the ZIP family of
or more micronutrients (Reid and Hayes, 2003). metal ion transporters from the model legume Medicago truncat-
The ZIP designation, which stands for “ZRT, IRT-like pro- ula, and were designated as MtZIP1, MtZIP3, MtZIP4, MtZIP5,
tein,” comes from the names of the first members of this family MtZIP6, and MtZIP7. These six proteins ranged from 350 to 372
that have been identified (Guerinot, 2000; Hall and Williams, amino acids in length and contained eight transmembrane do-
2003). ZRT1 and ZRT2 (Zn-regulated transporters) are the high- mains with highly conserved ZIP signature motif. Most of these
and low-affinity Zn transporters in yeast (Saccharomyces cere- proteins also exhibited a histidine-rich region in the variable se-
visiae), respectively, that are regulated by changes in cellular quence between transmembrane domains III and IV. They also
Zn status (Zhao and Eide, 1996a, 1996b). IRT1 (iron-regulated found that MtZIP1 transcripts were only detected in Zn-deficient
transporter) which was first identified in roots of Arabidopsis roots and leaves. MtZIP3 and MtZIP4 expression was downreg-
(Eide et al., 1996), is regarded as a metal transport protein in- ulated in the leaves of Mn- and Fe-deficient plants and appeared
duced upon Fe deficiency and it may also be permeable to some to be upregulated in both roots and leaves of Zn-deficient plants.
other trace metals such as Zn2+ (Vert et al., 2002; Reid and MtZIP5 was upregulated in leaves under Zn and Mn deficiency.
Hayes, 2003). The expression of MtZIP6 and MtZIP7 was unaffected by the
The ZIP proteins are predicted to have eight potential trans- metal supply, at least in root and leaf tissues.
membrane domains (TM) and have a similar membrane topol- The IRI1 transporter was suggested to play a central role
ogy, in which the amino- and carboxy-terminal ends of the pro- in plant Fe nutrition. IRT1 protein was localized at the plasma
tein are located on the outside surface of the plasma membrane membrane of root epidermal cells. Enhanced IRT1 expression
(Guerinot, 2000). TM3 and TM4, called “variable regions,” have could increase IRT1 density in the plasma membrane of Ara-
large differences in the length of amino acids, which may be bidopsis root cells (Cohen et al., 1998). Research on Arabidop-
the reason why the length of ZIP proteins ranges quite widely sis irt1 have provided more direct evidence that IRT1 is a ma-
from 309 to 476 amino acids. The most conserved portion of jor transporter responsible for Fe uptake and homeostasis in
the ZIP family proteins presents in TM4 and it is predicted to higher plants (Henriques et al., 2002; Varotto et al., 2002; Vert
form an amphipathic helix containing a fully conserved histidine et al., 2002). The Arabidopsis irt1 knockout mutant was ob-
residue. This histidine residue, along with an adjacent (semi) po- tained based on T-DNA insertion. It shows visual Fe-deficient
lar residue, may comprise part of an intramembranous metal ion chlorotic symptoms in shoots, and root Fe uptake and plant Fe
 ROOT DEVELOPMENT AND NUTRIENT UPTAKE 293

accumulation are significantly reduced (Varotto et al., 2002; Vert ing herbs, crops and trees (Gupta, 1997; Mendel and Hänsch,
et al., 2002). Another gene, IRT2, from Arabidopsis is also ex- 2002) especially at higher soil pH values. The Mo transporter is
pressed in root epidermal cells under Fe deficiency (Vert et al., still unknown in plants. Molybdate was thought to be transported
2001). More detailed information about the molecular mecha- by another anion transporter (Mendel and Hänsch, 2002). For ex-
nism of Fe uptake and transport by plant roots is available in the ample, P deficiency in tomato (Lycopersicon esculentum) plants
review by Ma (2005). enhanced uptake of radiolabelled molybdate up to five times, so
NRAMPs (natural resistance associated macrophage pro- that uptake of molybdate could occur via the phosphate uptake
teins) are members of a multigene family found across a broad system (Heuwinkel et al., 1992). Sulfate transporters are also
range of organisms, which can transport Mn, Zn, Fe, Ni, Cu, and likely candidates for low-affinity Mo uptake into the cell, be-
Co (Gunshin et al., 1997; Curie et al., 2000; Thomine et al., cause molybdate uptake could be inhibited by large amounts of
2000; Hall and Williams, 2003). They are highly conserved sulfate (Marschner, 1995). The co-transport of molybdate by a
proteins and have 12 predicted transmembrane domains. A se- sulfate transport system was also observed in filamentous fungi
quence motif characterized as a “consensus transport signa- (Tweedie and Segel, 1970).
ture” has been identified in the fourth intracellular loop be- Mutant analysis in the green alga (Chlamydomonas rein-
tween TM8 and 9 (Williams et al., 2000; Hall and Williams, hardtii) revealed two molybdate uptake systems. One system
2003). Six NRAMP genes have been identified in Arabidopsis is a high-affinity, low-capacity transporter which is insensitive
(Williams et al., 2000; Mäser et al., 2001), of which AtNramp1, to tungstate, but can be inhibited by 0.3 mM sulfate. The other
AtNramp3, and AtNramp4 are expressed in roots and the ex- system is a bulk transporter (low-affinity, high-capacity) that
pression is increased by Fe deficiency (Thomine et al., 2000). can be inhibited by tungstate, but not by sulfate (Llamas et al.,
They may be important at intermediate concentrations of Fe 2000).
where IRT1 is not present. NRAMPs have been proposed to
act as metal/H+ symporters (Reid and Hayes, 2003). In tomato, 3. Boron
the NRAMP gene LeNramp1 is suggested to act in mobilizing The mechanism of B uptake is still controversial. Passive up-
Fe in the vascular tissue under conditions of Fe deficiency be- take (the diffusion of boric acid through the plasma membrane)
cause this gene is specifically expressed in roots and localized is currently the most widely accepted mechanism for those plants
in the root vascular parenchyma during Fe starvation (Bereczky with adequate B supply (Dordas and Brown, 2000). However,
et al., 2003). Eight members (OsNRAMP1 to OsNRAMP8) of the an active carrier mediated process is also involved in B uptake
NRAMP family have been reported in rice plants (Gross et al., at low B supply, and is supported by evidence that its uptake
2003). rate can be described by Michaelis-Menten kinetics, and can be
inhibited by application of metabolic inhibitors. A high-affinity
transporter for B may be activated under B deficiency (Brown
H. Micronutrient Anions
et al., 2002).
1. Chloride Investigation using foreign gene expression in Xenopus
Cl− is thought to traverse the root by a symplastic pathway, oocytes indicated that B uptake occurs via passive diffusion
and Cl− fluxes across the plasma membrane and tonoplast of root across the lipid bilayer, facilitated by transport through major
cells are regulated by the Cl− content of the root. A Cl− efflux intrinsic proteins (MIPs). These proteins are types of aquaporins
channel may be responsible for efflux of Cl− at high external Cl− or water channels, found in cell membranes that most commonly
concentrations (e.g., in saline environments) or in depolarized mediate the transport of water (Dannel et al., 2002).
cells. Active Cl− transport across the plasma membrane domi- The Arabidopsis thaliana mutant bor1-1 is sensitive to B
nates Cl− influx to root cells at low Cl− concentrations in the soil deficiency (Noguchi et al., 1997; Takano et al., 2001). Using this
solution, and passive Cl− influx to root cells occurs under more mutant, the BOR1 gene was isolated, which encodes an efflux-
saline conditions. Both active and passive Cl− transports occur type B transporter for xylem loading (Takano et al., 2002).
at the tonoplast. Electrophysiological studies have demonstrated Hayes and Reid (2004) proposed two models for boron ef-
the presence of an electrogenic Cl− /2H+ symporter in the plasma flux to explain the tolerance mechanism in barley (Hordeum
membrane of root-hair cells and Cl− channels mediating either vulgare L.). They suggested B enters rapidly from the external
Cl− influx or Cl− efflux across the plasma membrane. Similarly, medium and accumulates in the cytoplasm as B(OH)3 , which
there is both biochemical and electrophysiological evidence that undergoes pH-dependent conversion to B(OH)− 4 . In model I, the
Cl− channels mediate Cl− fluxes in either direction across the efflux of B(OH)− is driven through an anion-permeable trans-
4
tonoplast and that a Cl− /nH+ antiport mediates Cl− influx to the porter by the negative membrane potential difference and at
vacuole (White and Broadley, 2001). low external pH by the outwardly directed concentration gra-
dient. In model II, B(OH)− 4 efflux occurs by anion-exchange.
2. Molybdenum If the anion is HCO− 3 no charge compensation is needed and
The requirement for Mo is very low in plants. Nevertheless, pH stability will occur through dissociation into OH− and CO2
Mo deficiency has been reported for many plant species includ- in the cytoplasm. Compared with tolerant genotype Sahara,
294 H. WANG ET AL.

B-sensitive genotypes Schooner may lack a capacity to efflux Barber, S. A. 1995. Soil Nutrient Bioavailability (2nd ed). Wiley, New York.
B(OH)−4.
Bates, T. R., and Lynch, J. P. 2000a. Plant growth and phosphorus accumulation
of wild type and two root hair mutant of Arabidopsis thaliana (Brassicaceae).
Am. J. Bot. 87: 958–963.
VI. CONCLUSIONS Bates, T. R., and Lynch, J. P. 2000b. The efficiency of Arabidopsis thaliana
(Brassicaceae) root hairs in phosphorus acquisition. Am. J. Bot. 87: 964–970.
The status of nutrient supply in soils are generally consid- Bell, P. F., Chaney, R. L., and Angle, J. S. 1988. Staining localization of ferric
ered to influence the growth and function of plant root systems reduction on roots. J. Plant Nutr. 11: 1237–1252.
(McMichael and Quisenberry, 1993), but the material cycling in Belton, P. S., Lee, R. B., and Ratcliffe, R. J. 1985. A 14 N nuclear magnetic
whole plants or retranslocation of nutrients from shoots to roots resonance study of inorganic nitrogen metabolism in barley, maize and pea
also play an important role in regulating root development and roots. J. Exp. Bot. 36: 190–210.
Bereczky, Z., Wang, H. Y., Schubert, V., Ganal, M., and Bauer, P. 2003. Differ-
functions. Until now about sixteen mineral elements have been ential regulation of nramp and irt metal transporter genes in wild type and
demonstrated to be essential for plant growth and development. iron uptake mutants of tomato. J. Biol. Chem. 278: 24697–24704.
These elements, except for C, H, and O, are usually taken up from Berleth, T., and Sachs, T. 2001. Plant morphogenesis: Long distance coordina-
soil by roots. Physiological functions of plant root systems are tion and local patterning. Curr. Opin. Plant Biol. 4: 57–62.
primarily determined by the development and function of indi- Bertin, C., Yang, X. H., and Weston, L. A. 2003. The role of root exudates and
allelochemicals in the rhizosphere. Plant Soil. 256: 67–83.
vidual roots, which have dissimilar morphologies expressed by Bibikova, T., and Gilroy, S. 2002. Root hair development. J. Plant Growth Regul.
several parameters such as root surface, length, diameter, num- 21: 383–415.
ber and configuration in soils (Yamauchi, 2001). In addition, Blackford, S., Rea, P. A., and Sanders, D. 1990. Voltage sensitivity of H+ /Ca2+
mechanisms involved in mineral nutrient uptake and transport antiport in higher plant tonoplast suggests a role in vacuolar calcium accu-
have been elucidated on a molecular basis as well in recent years. mulation. J. Biol. Chem. 265: 9617–9620.
Blumwald, E., Aharon, G. S., and Lam, B. C. H. 1998. Early signal transduction
Genes for acquisition and transport of various mineral nutrients pathways in plant-pathogen interactions. Trends Plant Sci. 3: 342–346.
have been identified in model plant systems such as Arabidopsis Britto, D. T., and Kronzucker, H. J. 2001. Constancy of nitrogen turnover kinetics
thaliana and rice, and in other plant species. in the plant cell: Insights into the integration of subcellular N fluxes. Planta.
This progress helps us better understand plant strategies to 213: 175–181.
overcome mineral nutrient stress (Ma, 2005), and offer a real Britto, D. T., and Kronzucker, H. J. 2003. The case for cytosolic NO− 3 het-
erostasis: A critique of a recently proposed model. Plant Cell Environ. 26:
possibility to genetically improve crop productivity in problem 183–188.
soils. There are needs for further functional analysis, precise Broillet, M. C., and Firestein, S. 1999. Cyclic nucleotide-gated channels. Molec-
localization at the organismal and cellular levels and cloning ular mechanisms of activation. Ann. N Y Acad. Sci. 868: 730–740.
of new genes. An integration of studies on nutrient behavior in Brown, P. H., Bellaloui, N., Wimmer, M. A., Bassil, E. S., Ruiz, J., Hu, H.,
soils, and the morphological and physiological functions of root Pfeffer, H., Dannel, F., and Römheld, V. 2002. Boron in plant biology. Plant
Biol. 4:205–223.
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detailed mechanisms of plant nutrient uptake and transport by nisms of phosphorus uptake into plants. J. Plant Nutr. Soil Sci. 164: 209–217.
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