Phosphorus Uptake by Plants: From Soil to Cell | Plant Physiology

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Other UPDATE ON PHOSPHORUS UPTAKE

 Phosphorus Uptake by Plants: From Soil to Cell

Daniel P. Schachtman, Robert J. Reid, S.M. Ayling
Published February 1998. DOI: [Link]

Article Figures & Data Info & Metrics Table of Contents

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Copyright © 1998 American Society of Plant
Physiologists
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P is an important plant macronutrient, making up about  Download PDF Tweet

0.2% of a plant's dry weight. It is a component of key  Article Alerts Like 4

molecules such as nucleic acids, phospholipids, and  Email Article

ATP, and, consequently, plants cannot grow without a

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reliable supply of this nutrient. Pi is also involved in
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controlling key enzyme reactions and in the regulation
of metabolic pathways (Theodorou and Plaxton,
Jump to section
1993). After N, P is the second most frequently limiting

 Article
We use cookies macronutrient for plant growth.
on this site to enhance your userThis update focuses
experience. on any link on
By clicking
this page you arePgiving your consent for us to set cookies.  PContinue
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IN SOIL Find
Find out more
more
in soil and its uptake by plants, transport across cell

 Pi UPTAKE ACROSS
membranes, and compartmentation and redistribution
THE PLASMA
within the plant. We will concentrate on P in higher MEMBRANE AND

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Phosphorus Uptake by Plants: From Soil to Cell | Plant Physiology

plants, although broadly similar mechanisms have been TONOPLAST

 MULTIPLE Pi

shown to apply in algae and fungi.
TRANSPORTERS
 COMPARTMENTATION

OF P
P IN SOIL
 REGULATION OF Pi


Although the total amount of P in the soil may be high, it UPTAKE

 P TRANSLOCATION IN

is often present in unavailable forms or in forms that are
WHOLE PLANT
only available outside of the rhizosphere. Few
 MYCORRHIZAE IN P

unfertilized soils release P fast enough to support the UPTAKE
high growth rates of crop plant species. In many  CONCLUSIONS


agricultural systems in which the application of P to the  ACKNOWLEDGMENTS



soil is necessary to ensure plant productivity, the  Footnotes



recovery of applied P by crop plants in a growing  LITERATURE CITED



season is very low, because in the soil more than 80% 

 Figures & Data

of the P becomes immobile and unavailable for plant 

 Info & Metrics

uptake because of adsorption, precipitation, or 

  PDF

conversion to the organic form (Holford, 1997).

We recommend
Soil P is found in different pools, such as organic and
mineral P (Fig.1). It is important to emphasize that 20 to 1. Plant Nutrition 2: Macronutrients (N,
P, K, S, Mg, and Ca)
80% of P in soils is found in the organic form, of which American Society of Plant
phytic acid (inositol hexaphosphate) is usually a major Biologists, Plant Cell

component (Richardson, 1994). The remainder is 2. Insights into Plant Cellular

Mechanisms: Of Phosphate
found in the inorganic fraction containing 170 mineral
Transporters and Arbuscular
forms of P (Holford, 1997). Soil microbes release Mycorrhizal Infection
immobile forms of P to the soil solution and are also Nancy A. Eckardt, Plant Cell

responsible for the immobilization of P. The low 3. Review: Transport and

homeostasis of K & P ($)
availability of P in the bulk soil limits plant uptake. More
Mary Williams, Plantae
soluble minerals such as K move through the soil via
4. Promoter analysis of the barley
bulk flow and diffusion, but P is moved mainly by Pht1;1 phosphate transporter gene
diffusion. Since the rate of diffusion of P is slow (10−12 identifies regions controlling root
expression and responsiveness to
to 10−15 m2s−1), high plant uptake rates create a zone
phosphate deprivation.
around the root that is depleted of P. Petra H D Schünmann et al., Plant
Physiol

 1. Response of spring wheat to NPK

and S fertilization. The content and Annotate
uptake of macronutrients and the
value of ionic ratios Highlight
Hanna Klikocka et al., Open
Chemistry

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Phosphorus Uptake by Plants: From Soil to Cell | Plant Physiology

2. Effect of Elevated CO2 on the

Growth and Macronutrient (N, P
and K) Uptake of Annual
Wormwood (Artemisia annua L.)
ChunwuZHUa et al., Pedosphere

3. Heuristic Anomaly Detection Model

of Industrial Control System Based
Fig. 1. Download figure | Open in new tab | Download powerpoint on Combined Neural Network
TANG Zhang-Guo et al., Journal of
Plant acquisition of soil P.
Sichuan University (Natural
Science Edition)

Plant root geometry and morphology are important for 4. A comparison of arsenic mobility in
Phaseolus vulgaris, Mentha
maximizing P uptake, because root systems that have
aquatica, and Pteris cretica
higher ratios of surface area to volume will more rhizosphere
effectively explore a larger volume of soil (Lynch, Jiřina Száková et al., Open Life
Sciences
1995). For this reason mycorrhizae are also important
for plant P acquisition, since fungal hyphae greatly Powered by
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(Smith and Read, 1997). In certain plant species, root
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limitations. These specialized roots exude high amounts and related cookies across the
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which acidify the soil and chelate metal ions around the
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roots, resulting in the mobilization of P and some
micronutrients (Marschner, 1995).
In this issue

Pi UPTAKE ACROSS THE PLASMA MEMBRANE AND

TONOPLAST

The uptake of P poses a problem for plants, since the

concentration of this mineral in the soil solution is low
but plant requirements are high. The form of P most
readily accessed by plants is Pi, the concentration of
which rarely exceeds 10 μm in soil solutions (Bieleski,
1973). Therefore, plants must have specialized Plant Physiology
transporters at the root/soil interface for extraction of Pi Vol. 116, Issue 2
Feb 1998

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Phosphorus Uptake by Plants: From Soil to Cell | Plant Physiology

from solutions of micromolar concentrations, as well as Table of Contents

other mechanisms for transporting Pi across About the Cover

Index by author
membranes between intracellular compartments, where
the concentrations of Pi may be 1000-fold higher than in
the external solution. There must also be efflux systems
that play a role in the redistribution of this precious View this
resource when soil P is no longer available or adequate. article with
LENS
The form in which Pi exists in solution changes
according to pH. The pKs for the dissociation of H3PO4
into H2PO4 −and then into HPO4 2− are 2.1 and 7.2,  Similar Articles

respectively. Therefore, below pH 6.0, most Pi will be

present as the monovalent H2PO4 −species, whereas
H3PO4 and HPO4 2− will be present only in minor
proportions. Most studies on the pH dependence of Pi
uptake in higher plants have found that uptake rates are
highest between pH 5.0 and 6.0, where H2PO4
−dominates (Ullrich-Eberius et al., 1984: Furihata et
al., 1992), which suggests that Pi is taken up as the
monovalent form.

Under normal physiological conditions there is a

requirement for energized transport of Pi across the
plasma membrane from the soil to the plant because of
the relatively high concentration of Pi in the cytoplasm
and the negative membrane potential that is
characteristic of plant cells. This energy requirement for
Pi uptake is demonstrated by the effects of metabolic
inhibitors, which rapidly reduce Pi uptake. The precise
mechanics of membrane transport are still not clear,
although cotransport of Pi with one or more protons is
the favored option based on the following observations.

The addition of Pi to starved roots results in both

depolarization of the plasma membrane and
acidification of the cytoplasm (Ullrich and Novacky,
1990). The depolarization indicates that Pi does not
enter simply as H2PO4 − or HPO4 2−, both of which
would lead to membrane hyperpolarization. From these
results it is likely that Pi is co-transported with positively
charged ions. Cotransport of Pi with a cation involving a

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Phosphorus Uptake by Plants: From Soil to Cell | Plant Physiology

stoichiometry of more than 1 C+/H2PO4 −or more than 2

C+/HPO4 2−would result in a net influx of positive
charge and hence lead to the observed membrane
depolarization. The cytoplasmic acidification associated
with Pi transport would suggest that the cation is H+, but
acidification would occur regardless of the nature of the
cation if the transported species were H2PO4 −, since it
would undergo a pH-dependent dissociation in the
cytoplasm to HPO4 2− and H+. To verify H+cotransport
requires simultaneous or at least comparable
measurements of Pi influx and the change induced in
cytoplasmic pH. Estimates of the cytoplasmic buffering
capacity would then allow calculation of the Pi-
associated H+ flux, from which the stoichiometry could
be deduced.

Pi uptake across the plasma membrane in animal cells

normally involves cotransport with Na+. Na-energized,
high-affinity Pi uptake systems have also been found in
cyanobacteria and green algae. In some organisms,
such as Saccharomyces cerevisiae, both Na+- and H+-
dependent Pi uptake systems have been described
(Roomans et al., 1977). Dependence of Pi uptake on
Na+ has not yet been demonstrated in higher plants, but
this may be partly because few studies have actually
tested this possible mode of energized Pi uptake.

Transfer of Pi from the cytoplasm to the vacuole

involves a different set of thermodynamic parameters to
those applying to the plasma membrane, mainly
because of the millimolar concentrations in the
cytoplasm and vacuole compared with the micromolar
concentrations in the soil. Few estimates of cytosolic
and vacuolar Pi concentrations are available. However,
when maize was grown at Pi concentrations similar to
those found in soils (i.e. 10 μm), the root cell
cytoplasmic Pi concentration was estimated to be
higher than the vacuolar concentration (Lee and
Ratcliffe, 1993). Soybean leaf cell cytoplasmic Pi
concentrations were also found to be higher than

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concentrations in the vacuole when plants were grown

in solutions containing 50 to 100 μm Pi (Lauer et al.,
1989). Since the membrane potential of the vacuole is
usually slightly positive with respect to the cytoplasm
under these realistic conditions, Pi transfer to the
vacuole need not be energized.

In plants supplied with higher concentrations of P, Pi

appears to be close to electrochemical equilibrium
across the tonoplast. In one of the few studies in which
tonoplast transport has been examined, Pi uptake into
vacuoles isolated from P-sufficient barley leaves was
shown to follow a monophasic, almost linear
concentration dependence up to at least 20 mm, and
was independent of ATP supply (Mimura et al., 1990).
However, in vacuoles isolated from Pi-starved cells, Pi
uptake rates were found to be much higher and ATP
dependent, despite the fact that the lower Pi
concentrations in the vacuoles would favor passive Pi
accumulation. This suggests the de-repression or
activation of a second transporter in the tonoplast in
response to Pi starvation.

The concentration dependence of Pi uptake in vacuoles

from Pi-starved cells has not been reported; a biphasic
response would support the presence of a second
transporter that might play an important role in
maintaining Pi homeostasis when the Pi supply is
limited. The process of vacuolar Pi mobilization
following Pi starvation is likely to require energy-
dependent transport across the tonoplast, the
mechanism of which is not understood, although an
H+/H2PO4 −symport would be thermodynamically
feasible. There is clearly a great deal more to
understand about the specific mechanisms of vacuolar
Pi transport in higher plants and the role these
mechanisms play in buffering cytoplasmic Pi
concentration.

MULTIPLE Pi TRANSPORTERS

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The question of whether there are several Pi

transporters with different functional characteristics in
plant cell membranes or only one transporter with
characteristics that vary with internal Pi status or
external concentration has been addressed using
kinetic analysis of uptake. In this type of analysis a
transporter's affinity (K m) for a particular mineral is
estimated by measuring the rate of uptake at different
external concentrations of an ion. Results from kinetic
studies have been variously interpreted to support the
existence of only one uptake system in barley roots
(Drew and Saker, 1984) or up to seven in maize roots
(Nandi et al., 1987). The most common interpretation of
these kinetic studies is that two Pi uptake systems exist,
one with a high affinity and activity that is either
increased or de-repressed by Pi starvation, and one
with a lower affinity and activity that is constitutive.
Estimates of theK m for high-affinity uptake range from 3
to 7 μm, whereas for low-affinity transporters theK m
estimates are more variable, from 50 to 330 μm in
several different tissues and plant species (Ullrich-
Eberius et al., 1984; McPharlin and Bieleski, 1987;
Furihata et al., 1992).

Recent advances in the molecular biology of putative

plasma membrane and tonoplast Pi transporters
confirm that plants have multiple transporters for Pi.
Thus far, four different transporter genes have been
cloned from Arabidopsis, three from potato, and two
from tomato. Putative plasma membrane or tonoplast
phosphate transporters in higher plants were cloned by
probing the database of translated expressed sequence
tags with fungal phosphate transporter peptide
sequences. This approach identified at least three
expressed sequence tags from randomly sequenced
Arabidopsis cDNAs with translational products that were
similar to the fungal phosphate-transporter proteins.
Using the expressed sequence tags, full-length clones
have been isolated from cDNA and genomic libraries

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(Muchhal et al., 1996; Leggewie et al., 1997; Smith et

al., 1997). One putative phosphate transporter gene
was expressed in tobacco cells (Mitsukawa et al.,
1997). High-affinity Pi uptake was detected in the cells
in which this gene was overexpressed, demonstrating
that at least one member of this gene family encodes a
high-affinity plasma membrane Pi transporter.

The proteins encoded by these genes contain large

regions that are identical to each other (Table I). The
gene family appears to be clustered in the Arabidopsis
genome with at least three members (APT1, APT2,
andAtPT4) mapping to a specific region of chromosome
5 (Lu et al., 1997; Smith et al., 1997). These multiple
Pi-transporter genes are differentially expressed. Some
are strongly up-regulated by Pi starvation, whereas the
expression of others is constitutive (Leggewie et al.,
1997). In the cases of APT1 and APT2, the deduced
amino acid sequences are 99% identical, which
suggests that the proteins have the same functional
characteristics. Although these proteins are almost
identical, the promoter regions are completely different
and may contain specific information that controls the
spatial expression of these genes in different cell types,
such as epidermal or cortical cells in the roots.

Table I.
View inline | View popup
Comparison matrix of phosphate transporter polypeptides

A cDNA encoding a Pi transporter from potato, which is

expressed in roots under conditions of Pi starvation,
was characterized in thepho84 yeast mutant (Leggewie
et al., 1997). TheK m for Pi uptake was 130 μm, much
higher than would be expected if it were involved in Pi
uptake from soils, where concentrations rarely exceed
10 μm. Various reasons were suggested (Leggewie et
al., 1997) for the highK m values, but perhaps the most
interesting is that phosphate transporters may contain a
number of different protein subunits. The normal
function of phosphate transporters may require subunits

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that are absent when this plant cDNA is expressed in

yeast. Genetic evidence from Saccharomyces
cerevisiaeindicates that several proteins containing
putative membrane-spanning domains may interact to
form a Pi-transporter complex (Bun-ya et al., 1991,
1996; Yompakdee et al., 1996). Although the
association between these proteins has not been
directly demonstrated, and one protein (Pho84) has
been shown to be sufficient to catalyze phosphate
transport in proteoliposomes (Berhe et al., 1995), the
genetic evidence supports the idea that phosphate
transporters are comprised of multiple subunits.

In summary, kinetic and molecular data show that

higher plants have multiple transporters for Pi across
cellular membranes. The molecular data show that
there are at least four genes that encode Pi
transporters, and the kinetic data suggests the
presence of two types of transporters with different
affinities for Pi. The recent advances in the molecular
biology of these transporters provide powerful tools for
understanding how their function is integrated into plant
physiological processes. More work will be required to
gain a comprehensive picture of the location (cellular
and subcellular) and precise function of the multiple
phosphate transporters in plants.

COMPARTMENTATION OF P

Maintenance of stable cytoplasmic Pi concentrations is

essential for many enzyme reactions. This homeostasis
is achieved by a combination of membrane transport
and exchange between various intracellular pools of P.
These pools can be classified in a number of different
ways. First, according to their location in physical
compartments such as the cytoplasm, vacuole,
apoplast, and nucleus. The pH of these compartments
will determine the form of Pi. The second pKa for
H3PO4 is 7.2, so Pi in the cytoplasm will be
approximately equally partitioned between the ionic

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forms H2PO4 −and HPO4 2−, whereas in the more acidic

vacuole and apoplast, H2PO4 −will be the dominant
species. Second, by the chemical form of P, such as Pi,
P-esters, P-lipids, and nucleic acids. The proportion of
the total P in each chemical form (except P in DNA)
changes with tissue type and age and in response to P
nutrition. Third, according to physiological function, as
metabolic, stored, and cycling forms.

Our knowledge of the distribution of P into metabolic

pools and physical compartments comes from three
types of studies. Before 1980, information about P
compounds and their distribution within tissues was
derived from the analysis of isolated organelles or from
the partitioning of the radioactive tracer 32P between
different chemical fractions (Bieleski, 1973). Other
information came from studies on the rate at which32P
is incorporated into or lost from tissues, commonly
referred to as compartmental analysis (Macklon et al.,
1996). A major advance in mapping intracellular pools
came with the application of NMR spectroscopy in plant
tissues. This technique allowed analysis in vivo of Pi
and other important P-metabolites (Ratcliffe, 1994), as
well as the monitoring of time-dependent changes in the
amounts of these compounds. Figure2 shows a
typical31P-NMR spectrum, such as is observed from
samples of root tips or suspension-cultured cells, and
indicates where the observed compounds are found
within the cell.

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Fig. 2. Download figure | Open in new tab | Download powerpoint

31P-NMR of carrot cells. The assignments of the labeled

resonances are: 1, several P-monoesters including Glc-6-P and
phosphocholine; 2, cytoplasmic Pi; 3, vacuolar (vac) Pi; 4, γ-P of
nucleoside triphosphates, principally ATP; 5, α-P of NTPs; 6, NDP-
hexose and NAD(P)H; 7, NDP-hexose; and 8, β-P of NTPs.
(Spectrum redrawn from Carroll et al., 1994.)

Separate signals are detectable for Pi and other

soluble-P compounds located in the near-neutral
cytoplasm or in the acidic vacuole (Fig.2). 31P-NMR is
at present the only way to measure directly the
cytoplasmic and vacuolar pools of Pi in vivo. In an NMR
spectrum the intensity of the resonances, reflected in
the peak areas, provides an immediate representation
of the relative amounts of the different soluble-P
fractions present. The peak areas represent the content
of Pi from which concentrations can be derived (see
Lee and Ratcliffe, 1993). NMR studies confirmed that a
small, rapidly turning over pool of Pi (representing 1–5%
of total Pi) is located in the cytoplasm and a larger
storage pool is located in the vacuole (Ratcliffe, 1994).
NMR studies have made a major contribution to our
knowledge of the behavior of the cytoplasmic and
vacuolar pools of Pi within the plant.

REGULATION OF Pi UPTAKE

Cytoplasmic Pi is maintained at constant concentrations

(5–10 mm), more or less independently of external Pi
concentrations, except under severe P depletion (Lee
et al., 1990; Lee and Ratcliffe, 1993; Mimura, 1995).
In contrast, vacuolar Pi concentrations vary widely;
under conditions of P starvation, vacuolar Pi may be
almost undetectable. Pi in the vacuole also increases
more readily than other P fractions in response to
improved P status. However, it does not seem to

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increase above about 25 mm (Lee et al., 1990; Lee

and Ratcliffe, 1993; Mimura, 1995).

When the supply of Pi is limited, plants grow more

roots, increase the rate of uptake by roots from the soil,
retranslocate Pi from older leaves, and deplete the
vacuolar stores of Pi. In addition, mycorrhizal fungi may
more extensively colonize the roots. Conversely, when
plants have an adequate supply of Pi and are absorbing
it at rates that exceed demand, a number of processes
act to prevent the accumulation of toxic Pi
concentrations. These processes include the
conversion of Pi into organic storage compounds (e.g.
phytic acid), a reduction in the Pi uptake rate from the
outside solution (Lee et al., 1990), and Pi loss by efflux,
which can be between 8 and 70% of the influx (Bieleski
and Ferguson, 1983). Any or all of these processes
may be strategies for the maintenance of intracellular Pi
homeostasis.

It is clear from both kinetic and molecular studies that

the capacity to transport Pi across cellular membranes
involves several different transporters and is in some
way regulated by the external supply of [Link] et
al. (1992) showed differential expression of phosphate
transporters using kinetic techniques in which the high-
affinity, but not the low-affinity, system was repressed
by high concentrations of Pi. The expression of certain
members of the putative plasma membrane or tonoplast
phosphate-transporter gene family increases during
periods of Pi starvation. In Arabidopsis at least three
genes encoding phosphate transporters are expressed
in roots and are up-regulated by Pi starvation. Similarly,
in potato one gene was specifically induced in roots and
stolons by starving the plants of Pi, whereas a second
gene was expressed throughout the plant under
conditions of high or low phosphate.

Changes in Pi-transport activity and phosphate-

transporter gene expression show that plant cells
respond to changes in the Pi concentration of the

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external medium or in the vacuole. However, the

intracellular signals and the factors that modify gene
expression in the nucleus while cytoplasmic
concentrations of Pi remain relatively constant are
unknown. Progress at the molecular level may
eventually provide insight into the processes that
regulate phosphate uptake through the isolation of
genes encoding proteins that interact and regulate
phosphate-transport mechanisms.

P TRANSLOCATION IN WHOLE PLANT

Recent studies (Mimura et al., 1996; Jeschke et al.,

1997) provide a picture of patterns of Pi movement in
whole plants. In P-sufficient plants most of the Pi
absorbed by the roots is transported in the xylem to the
younger leaves. Concentrations of Pi in the xylem range
from 1 mm in Pi-starved plants to 7 mm in plants grown
in solutions containing 125 μm Pi (Mimura et al., 1996).
There is also significant retranslocation of Pi in the
phloem from older leaves to the growing shoots and
from the shoots to the roots. In Pi-deficient plants the
restricted supply of Pi to the shoots from the roots via
the xylem is supplemented by increased mobilization of
stored P in the older leaves and retranslocation to both
the younger leaves and growing roots. This process
involves both the depletion of Pi stores and the
breakdown of organic P in the older leaves. A curious
feature of P-starved plants is that approximately one-
half of the Pi translocated from the shoots to the roots in
the phloem is then transferred to the xylem and
recycled back to the shoots (Jeschke et al., 1997). In
the xylem P is transported almost solely as Pi, whereas
significant amounts of organic P are found in the
phloem.

A number of mutants that show altered Pi accumulation

in leaves have been identified. These may help us to
understand the processes controlling the allocation of Pi
within the plant. One Arabidopsis mutant (pho1) was

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isolated based on reduced total phosphate

concentrations in the leaf tissue (Poirier et al., 1991)
and was shown to have root Pi uptake rates that were
the same as the wild type, but reduced translocation
rates to the shoot. In thepho1 mutant, it is not known
whether a gene encoding a transporter or regulatory
molecule has been mutated; however, the phosphate-
transporter genes that have been cloned do not map to
thepho1 (or pho2) locus. This mutation highlights the
importance of specialized mechanisms for the transfer
of Pi to the xylem. Another Arabidopsis mutant, pho2,
accumulates P in its leaves to toxic concentrations,
which is indicative of a defect in the regulation of Pi
concentrations in shoots (Delhaize and Randall, 1995)
and illustrates the significance of regulating intracellular
concentrations.

MYCORRHIZAE IN P UPTAKE

There is a general perception that Pi uptake by plants

occurs as a direct consequence of uptake from the soil
by root cells. However, in more than 90% of land plants,
symbiotic associations are formed with mycorrhizal
fungi. In these plants the fungal hyphae play an
important role in the acquisition of P for the plant
(Bolan, 1991; Smith and Read, 1997). Mycorrhizae
can be divided into two main categories:
ectomycorrhizae and endomycorrhizae, of which
vesicular arbuscular mycorrhizae are the most
widespread in the plant kingdom (Smith and Read,
1997). The mycorrhizal symbiosis is founded on the
mutualistic exchange of C from the plant in return for P
and other mineral nutrients from the fungus. Influx of P
in roots colonized by mycorrhizal fungi can be 3 to 5
times higher than in nonmycorrhizal roots (rates of
10−11 mol m−1 s−1; Smith and Read, 1997).

The few published studies of the kinetics of Pi uptake

indicate that mycorrhizal roots and isolated hyphae
have P-uptake systems with characteristics similar to

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those found in nonmycorrhizal roots and other fungi

(Thomson et al., 1990; Smith and Read, 1997). Germ
tubes of the vesicular arbuscular mycorrhizal fungus
Gigaspora margarita have two Pi-uptake systems (K m
2–3 μm and 10,000–11,000 μm) (Thomson et al.,
1990). A recent molecular study (Harrison and van
Buuren, 1995) identified the geneGvPT, which encodes
a high-affinity fungal phosphate transporter (K m = 18
μm) in external hyphae that is similar in both structure
and function to high-affinity transporters in plants (Table
I).

A number of factors may contribute to the increased

rate of Pi uptake measured in mycorrhizal plants (Smith
and Read, 1997). An extensive network of hyphae
extends from the root, enabling the plant to explore a
greater volume of soil, thereby overcoming limitations
imposed by the slow diffusion of Pi in the soil. Several
studies have shown that the depletion zone around
plant roots, which is caused by plant uptake and the
immobile nature of Pi, is larger in mycorrhizal than in
nonmycorrhizal plants (Bolan, 1991). Mycorrhizal fungi
may also be able to scavenge Pi from the soil solution
more effectively than other soil fungi because C (which
may be limiting in the soil) is provided to the fungus by
the plant. The plant/fungus association could therefore
enable the plant to compete more effectively with soil
microorganisms for the limited amount of available soil
Pi. Mycorrhizal fungi may also be able to acquire P from
organic sources that are not available directly to the
plant (e.g. phytic acid and nucleic acids)
(Jayachandran et al., 1992).

Little is known about the transport of P compounds

within mycorrhizae or the mechanism of P efflux from
the fungus. Pi and organic P (such as polyphosphate)
could be carried within the fungus by cytoplasmic
streaming or by bulk flow to the plant root from external
hyphae located in the soil. The current view is that Pi is
the major form effluxed by the fungus across the

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interfacial membranes. However, there is also evidence

in higher plants that phosphocholine can be broken
down outside cells to release Pi. It is possible that
phosphocholine is also effluxed by the fungus to the
plant; Pi would then be taken up by the plant via an H+
cotransporter, as in nonmycorrhizal roots. Since it is
known that the phosphate transporter cloned from
Glomus versiforme (GvPT) is not expressed in fungal
structures inside the plant, it cannot be a candidate for
the fungal P efflux mechanism. Efflux of P must depend
on a different transporter of unknown structure.

The role of P in the regulation of symbiosis is still poorly

understood, in part because of conflicting experimental
results. In mycorrhizal roots demand for P by the plant
may regulate the activity of P transporters in the fungus,
with efflux from the fungus being the limiting step.
However, NMR studies of ectomycorrhizal roots of
Pinus resinosa (MacFall et al., 1992) showed that
although there was an increase in polyphosphate P in
mycorrhizal roots, the vacuolar Pi content of mycorrhizal
and nonmycorrhizal roots was similar. The mycorrhizal
plants did not accumulate Pi in the vacuoles, which
suggests that the fungus (Hebeloma arenosa) may be
able to limit the efflux of P to the plant.

Mycorrhizal roots are able to take up Pi from solutions

containing up to 100 mm Pi (Smith and Read, 1997),
concentrations far above that likely to be encountered in
the soil. High external Pi concentrations (up to 16 mm)
had little adverse effect on germination and growth of
germ tubes in the vesicular arbuscular mycorrhizal
fungus G. margarita (Tawaraya et al., 1996). These
results suggest that the low levels of colonization seen
in plants growing in soils with high P status may not be
the result of direct regulation of the activity of the fungus
by soil Pi, but, rather, that specific signals from the plant
regulate the activity of the fungus.

CONCLUSIONS

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Phosphorus Uptake by Plants: From Soil to Cell | Plant Physiology

Considering that P is an essential and often limiting

nutrient for plant growth, it is surprising that many
aspects of P uptake and transport in plants are not
thoroughly understood.31P-NMR studies have provided
a picture of where Pi is distributed in a living cell, kinetic
studies have elucidated the general functional
characteristics of plasma membrane and tonoplast Pi
transporters, and molecular studies have confirmed the
presence of multiple genes encoding phosphate
transporters that are differentially expressed. Perhaps
the next important leap in our conceptual understanding
in this area will come from the integration of these
techniques to provide a comprehensive picture of the
function of phosphate transporters and how the control
of their spatial and temporal expression allows the plant
to cope with changing environmental conditions.

A final issue to raise is that the soil Pi concentration has

often been ignored by plant physiologists. It is common
to find experiments in which plants were grown in 1 mm
Pi, which may be 100-fold higher than the Pi
concentrations plants encounter in agricultural or
natural ecosystems. To fully understand how plants
acquire Pi from soils and regulate internal Pi
concentrations, future studies on Pi uptake by plants
must more closely mimic soil conditions, in which the
concentration of Pi is always low and soil microflora
influence both acquisition and mobilization.

ACKNOWLEDGMENTS

We thank Professors F.A. and S.E. Smith for their

critical comments and discussions. We apologize to the
colleagues whose papers were not directly cited
because of space limitations.

Footnotes

* Corresponding author; e-
maildschachtman@[Link]; fax 61–

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Phosphorus Uptake by Plants: From Soil to Cell | Plant Physiology

8–82–32–3297.

Received July 23, 1997.

Accepted October 9, 1997.

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