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Plant Physiol. (1998) 116: 91-99
Tomato Phosphate Transporter Genes Are Differentially Regulated
in Plant Tissues by Phosphorus1
Chunming Liu2,
Umesh S. Muchhal2,
Mukatira Uthappa,
Andrzej K. Kononowicz, and
Kaschandra G. Raghothama*
Department of Horticulture, Purdue University, West Lafayette,
Indiana 47907-1165 (C.L., U.S.M., M.U., K.G.R.); and Department of
Plant Cytochemistry and Cytogenetics, University of Lodz,
90-237 Lodz, Poland (A.K.K.)
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ABSTRACT |
Phosphorus
is a major nutrient acquired by roots via high-affinity inorganic
phosphate (Pi) transporters. In this paper, we describe the
tissue-specific regulation of tomato (Lycopersicon esculentum L.) Pi-transporter genes by Pi. The
encoded peptides of the LePT1 and LePT2
genes belong to a family of 12 membrane-spanning domain proteins and
show a high degree of sequence identity to known high-affinity Pi
transporters. Both genes are highly expressed in roots, although there
is some expression of LePT1 in leaves. Their expression is markedly
induced by Pi starvation but not by starvation of nitrogen, potassium,
or iron. The transcripts are primarily localized in root epidermis
under Pi starvation. Accumulation of LePT1 message was also observed in
palisade parenchyma cells of Pi-starved leaves. Our data suggest that
the epidermally localized Pi transporters may play a significant role
in acquiring the nutrient under natural conditions. Divided root-system
studies support the hypothesis that signal(s) for the Pi-starvation
response may arise internally because of the changes in cellular
concentration of phosphorus.
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INTRODUCTION |
Phosphorus availability is considered one of the major
growth-limiting factors for plants in many natural ecosystems (Barber et al., 1963 ). Plants have developed several adaptive mechanisms to
overcome Pi stress (Marschner, 1995). Changes in the root growth and
architecture (Anghinoni and Barber, 1980; Lynch, 1995), increased production of phosphatases and RNases (Duff et al., 1989; Goldstein, 1992; Loffler et al., 1992; Green, 1994; Bariola et al., 1995), and
altered activity of several enzymes of the glycolytic pathway (Duff et
al., 1989) are among the well-characterized responses to Pi deficiency
in plants. In addition, an increase in the phosphate uptake rate of
roots and cell cultures following phosphate starvation has been
observed in several plant species (Clarkson and Scattergood, 1982; Drew
et al., 1984; Katz et al., 1986).
Phosphate is acquired by plants in an energy-mediated co-transport
process driven by a proton gradient generated by plasma membrane
H+-ATPases (Epstein, 1976; Ullrich-Eberius et
al., 1981, 1984; Sakano, 1990). The kinetic characterization of the
Pi-uptake system by whole plants (Ullrich-Eberius et al., 1984) and
cultured cells (Furihata et al., 1992) indicates a high-affinity
transport activity operating at low concentrations (micromolar range)
and a low-affinity activity operating at higher concentrations
(millimolar range). In cultured cells of Catharanthus roseus
the low-affinity system is expressed constitutively, whereas the
high-affinity system is regulated by the availability of phosphorus
(Furihata et al., 1992). When cells grown in Pi-rich medium were
transferred to Pi-depleted medium, the high-affinity uptake activity
increased significantly within 2 d. The enhanced uptake appears to
be in part due to the increased synthesis of a carrier system in
response to Pi starvation (Drew and Saker, 1984; Shimogawara and Usuda, 1995). Phosphorus stress in microorganisms is known to result in
transcriptional activation of high-affinity Pi transporters and
phosphatases (Torriani-Gorini et al., 1994). High-affinity phosphate
transporter genes have been cloned and characterized from fungi (Bun-ya
et al., 1991; Harrison and van Buuren, 1995; Versaw, 1995) and recently
from plants (Muchhal et al., 1996; Kai et al., 1997; Leggewie et al.,
1997; Smith et al., 1997). All of the characterized Pi transporter
proteins are predicted to have a common structure containing 12 membrane-spanning domains, which are separated into two groups of 6 by
a charged hydrophilic region.
In this paper we report the characterization of two tomato
(Lycopersicon esculentum L.) phosphate transporters and
regulation of their expression by phosphorus. To our knowledge, this is
the first report showing an enhanced accumulation of phosphate
transporter transcripts in root epidermis under Pi starvation. We also
provide evidence for the regulation of the gene expression by internal signals during phosphate starvation.
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MATERIALS AND METHODS |
Tomato (Lycopersicon esculentum L.) plants were grown
in an aeroponic growth facility similar to the one described by Liu et
al. (1997). Tomato seeds of the variety OS4 were germinated in seedling
trays filled with Ready Earth plug mixture (Scotts, Marysville, OH).
When plants reached the four-leaf stage (20 d after sowing), they were
removed from the growing medium, and roots were washed free of medium
and transferred to aeroponics. In aeroponic culture roots were sprayed
with a fine mist that consisted of one-half-strength Hoagland solution
(Jones, 1982) for 3 s every 10 min. Phosphorus-starvation
treatments were initiated 1 week after the plants were transferred to
aeroponics. For divided root-system studies, tomato plants were grown
in aeroponics for 1 week as described above. Three aeroponic plants
were transferred to an aerated hydroponic solution containing either
250 or 0 µm Pi. The roots of three more plants were
separated into two sections, and each section of the roots was placed
in an adjacent container with aerated nutrient solution containing
either 250 or 0 µm Pi. Leaves and roots from P+ (250 µm Pi) and P (0 µm Pi) and
divided-root-system plants were harvested separately, frozen in liquid
nitrogen, and stored at 70°C.
RNA Isolation
Total RNA was isolated from roots and leaves of tomato plants by
hot-phenol extraction and lithium chloride precipitation (Pawlowski et
al., 1994). Poly(A+) RNA was isolated by the
oligo(dT)-cellulose batch-binding method (Sambrook et al., 1989).
cDNA Library Construction and Screening
A cDNA library representing the mRNA isolated from tomato roots
starved for phosphate for 5 d was constructed in the
XhoI-EcoRI site of the Uni-ZAP-XR vector
(Stratagene), according to the manufacturer's instructions. The two
Arabidopsis thaliana cDNA clones (AtPT1 and AtPT2) encoding
the phosphate transporters (Muchhal et al., 1996) were
radiolabeled by random priming (DECAprimeII, Ambion, Austin, TX) and
used for screening the tomato cDNA library according to standard
procedures (Sambrook et al., 1989). Hybridizations for screening were
carried out in a solution containing 50% (v/v) formamide at 38°C.
Final washing of the filters was done with 1× SSC and 0.2% (w/v) SDS
at 60°C for 30 min. Two sets of cDNA clones were obtained from this
screening. Based on the insert size and restriction mapping, one
full-length representative from each of these sets was used for further
analysis. The sequence of these two clones was determined on both
strands by the dideoxy method using Sequenase (United States
Biochemical). The Genetics Computer Group (University of Wisconsin,
Madison) software package was used for sequence analysis and database
searches.
Northern Blots
Ten micrograms of total RNA was electrophoretically separated on
1% denaturing formaldehyde agarose gels and blotted onto a BA-S
nitrocellulose membrane (Sambrook et al., 1989). The nitrocellulose filters were hybridized overnight with a
32P-labeled probe (106
cpm/mL) in a solution containing 50% formamide, 5× Denhart's solution, 0.1% (w/v) SDS, 6× SSPE, and 100 µg/mL denatured
salmon-sperm DNA at 42°C. Filters were washed twice in 2× SSC and
0.2% SDS at room temperature for 10 min, twice in 1× SSC and 0.2%
SDS at 50°C for 15 min, and twice in 0.1× SSC and 0.2% SDS at
62°C for 20 min before autoradiography.
Southern Blots
High-molecular-weight genomic DNA was isolated from young leaves
of tomato, as described by Dellaporta et al. (1983). Ten micrograms of
genomic DNA was digested with restriction enzymes, electrophoretically
separated through 0.8% agarose gels, denatured, and transferred to a
supported nitrocellulose membrane (Sambrook et al., 1989). The
hybridization and washing conditions were the same as those described
above for northern blots.
In Situ Localization of Tomato Phosphate Transporter
Transcripts
Roots of tomato plants grown in aeroponics were sprayed with
nutrient solutions with Pi (250 µm) or without Pi for
5 d. Root and leaf samples were harvested and fixed in
a solution containing 3.7% (v/v) formaldehyde, 5% (v/v) acetic acid,
and 50% (v/v) ethanol (Niu et al., 1996). Fixed tissue samples were dehydrated in an ethanol dilution series and embedded in wax
(Paraplast, Fisher Scientific). Ten-micrometer sections cut with a
microtome were transferred to Super-Frost Plus slides (Fisher
Scientific) and incubated at 42°C overnight. Sense and antisense
probes representing LePT1 and LePT2 were transcribed by T3 or T7
RNA polymerase (Ambion) from linearized pBluescript- SK
containing the cDNA. The probes were labeled with digoxigenin following
the procedure described by the manufacturer (Boehringer Mannheim).
Tissue-section pretreatment and in situ hybridization were performed as
described by Niu et al. (1996). Successive sections from roots obtained
from three plants were used for hybridizing with sense and antisense
probes. After color development for 16 to 24 h, sections were
photographed using an Optiphot microscope (Nikon).
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RESULTS |
Structure and Organization of the Tomato Pi Transporters
Two full-length cDNA clones, LePT1 and LePT2, encoding the tomato
phosphate transporters were isolated from a phosphate-starved root
library using a mixture of Arabidopsis AtPT1 and AtPT2 cDNA clones
(Muchhal et al., 1996; Mukatira et al., 1996) as heterologous probes.
LePT1 is 2023 bp long and contains an open reading frame encoding a
538-amino acid polypeptide (58.7 kD), whereas LePT2 is 1826 bp long and
encodes a 528-amino acid polypeptide (7.8 kD). The open reading frames
of LePT1 and LePT2 are flanked by 151 and 37 bp of untranslated
sequence at the 5 end and by 258 and 205 bp of untranslated sequence,
including the poly(A+) tail, at the 3 end. The LePT1 and
LePT2 polypeptides are 80% identical in their amino acid sequence. The
two polypeptides share the greatest degree of similarity with the
recently characterized phosphate transporters (Fig.
1) from potato (Solanum
tuberosum L.; Leggewie et al., 1997), Arabidopsis (Muchhal et al.,
1996; Smith et al., 1997), and Catharanthus roseus (Kai et
al., 1997). Based on the amino acid sequence identity, LePT1 is more
similar to potato STPT1 and Arabidopsis to AtPT2, whereas LePT2 is more similar to STPT2 and AtPT1. Phylogenetically, the phosphate
transporters from plants and fungi belong to a closely related family,
even though the similarity between the plant transporters is
significantly higher than that between plants and fungal transporters
(Muchhal et al., 1996).
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| Figure 1.
A, Alignment of the deduced amino acid sequence of
LePT1 and LePT2 with that of A. thaliana (AtPT1 and
AtPT2), potato (STPT1 and STPT2), and C. roseus (PIT1)
phosphate transporters. Identical amino acids are indicated by
asterisks and conserved substitutions are indicated by dots. The
membrane-spanning domains of LePT1 and LePT2 as predicted by TopPred
(Claros and von Heijne, 1994) are underlined and their numbering is
indicated by roman numerals (I-XII). The open and boxed sequences are
consensus sites for phosphorylation by casein kinase II, and boxed and
shaded sequences are consensus sites for phosphorylation by protein
kinase C. B, Summary of the percentage of amino acid identity between
tomato and other plant phosphate transporters.
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Hydropathy plots of the deduced polypeptides suggest that both tomato
transporters are integral membrane proteins that consist of 12 membrane-spanning regions, a common feature shared by proteins responsible for transport of substrates as diverse as sugars, ions,
antibiotics, and amino acids (Griffith et al., 1992; Henderson, 1993;
Marger and Saier, 1993). The position and spacing of these membrane-spanning regions in tomato transporters are very similar to
those in other Pi transporters (Fig. 1). Based on secondary structure
analyses, both the N and C termini of the polypeptides are predicted to
be on the cytoplasmic side of the plasma membrane. The amino acid
domains for protein kinase C- and casein kinase II-mediated
phosphorylation are present in similar conserved regions, as seen with
Arabidopsis Pi transporters (Muchhal et al., 1996).
Full-length LePT1 and LePT2 cDNA probes hybridized with two or three
distinct bands on Southern blots (Fig. 2)
of tomato genomic DNA digested with different restriction enzymes,
suggesting the presence of a small gene family.
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| Figure 2.
Southern-blot analysis of tomato genomic DNA
digested with PstI (P), HindIII (H), or
EcoRI (E). Blots were hybridized with 32P-labeled cDNA fragments specifically recognizing LePT1
and LePT2 genes. DNA markers are indicated in kilobases.
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LePT1 and LePT2 Transcripts Are Induced by Phosphate Starvation in
Roots
The expression of LePT1 and LePT2 in tomato plants grown either in
the presence of 250 µm phosphate or no phosphate was
compared by northern-blot analysis of total RNA isolated from different tissues. Both probes hybridized to approximately 2-kb transcripts (Fig.
3). Their expression was markedly
increased in plants grown under Pi-limiting conditions. LePT1 is
primarily expressed in roots, with a small amount of the message also
detectable in leaves (Fig. 3), stems, and petioles (data not shown) of
tomato plants subjected to Pi starvation. LePT2 is expressed only in
the roots. The relative abundance of both of the messages was similar
in the Pi-starved roots. An increase in the transcript level of both of
the genes was detected within 24 h of Pi starvation in roots (Fig.
4). The transcript levels continued to
increase with increased duration of Pi starvation, and reached a
maximum after 5 d. These results indicate that expression of LePT1
and LePT2 responds to changing nutritional conditions.
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| Figure 3.
Northern-blot analysis of the expression of tomato
phosphate-transporter genes. Total RNA from roots (R) or leaves (L) of tomato plants grown aeroponically and misted with a solution containing 250 µm (+) or no () phosphate was hybridized with a
labeled probe from either LePT1 or LePT2. An ethidium bromide-stained
gel picture indicating uniform loading and integrity of RNA samples is
shown at the bottom.
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| Figure 4.
Expression of LePT1 and LePT2 transcripts during
Pi starvation. Northern blot of total RNA isolated from the roots of
plants misted with nutrient solutions containing either 250 µm (+) or no () phosphate for the indicated periods. A
picture of the gel showing uniform loading of RNA is shown.
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To investigate the expression of LePT1 and LePT2 in response to
deficiency of other nutrients, tomato plants grown in aeroponics were
subjected to starvation of three other nutrients, nitrogen, potassium,
and iron. After 5 d a visible retardation in growth was noticed in
the Pi- and nitrogen-starved plants, but no visible difference in
growth was observed in the plants starved of potassium and iron. The
LePT1 and LePT2 transcript levels increased greatly in Pi-starved
plants but remained low in the roots of plants subjected to the other
three nutrient-starvation treatments (Fig.
5). Although we have not tested the
effect of starvation of other essential nutrients, the data suggest a
strong correlation between LePT1 and LePT2 expression and Pi
starvation.
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| Figure 5.
Effect of different nutrient starvation on the
expression of LePT1 and LePT2 transcripts. The roots of tomato plants
grown in aeroponics were sprayed with nutrient solutions deficient in phosphate (P), potassium (K), nitrogen (N), or iron (Fe) and a control
solution containing all necessary nutrients (C) for 5 d. Total RNA
isolated from the roots of these plants was analyzed by northern
blotting. A picture of the gel showing uniform loading of RNA is
shown.
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LePT1 and LePT2 Expression Is Dependent on the Availability of Pi
in the Medium
To define the Pi concentration at which the phosphate- transporter
genes are expressed, tomato plants were grown in the presence of
different concentrations of phosphorus. After 5 d of treatment the
roots were harvested for isolation of RNA. Increased expression of both
LePT1 and LePT2 was detected in the roots of plants provided with 100 µm Pi or less (Fig. 6),
suggesting a correlation between the amount of phosphorus present in
the medium and the level of LePT gene expression. It appears that
expression of LePT1 is relatively more sensitive to Pi concentration
changes than that of LePT2.
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| Figure 6.
Effect of different concentration of Pi on the
expression of LePT1 and LePT2 transcripts. Northern blot of total RNA
isolated from roots of tomato plants sprayed with nutrient solution
containing the indicated micromolar concentration of Pi for 5 d. A
picture of the gel showing uniform loading of RNA is shown.
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The regulation of LePT1 and LePT2 expression by phosphorus availability
was further examined by resupplying Pi to the plants that were Pi
deficient and strongly expressing the genes. When 250 µm
Pi was resupplied to these plants, transcript levels of both genes
decreased within 24 h (Fig. 7) and
reached a significantly low level within 2 d. These observations
suggest the existence of a fine coordination between gene expression,
presumed to lead to the synthesis of more transporters and increased
uptake, and the availability of phosphorus in the soil.
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| Figure 7.
Expression of LePT1 and
LePT2 genes is reversible upon the resupply of phosphate
to Pi-starved plants. Tomato plants were sprayed with nutrient solution
containing 250 µm (+) or no () Pi. After 5 d the
Pi-starved plants were replenished with 250 µm Pi (R) or
continued to grow in Pi-deficient medium (C) for the indicated time.
Total RNA isolated from the roots of these plants was used for
northern-blot analysis. A picture of the gel showing uniform loading of
RNA is shown.
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Phosphate Transporter Expression Is Likely Regulated by Internal
Signals
The increase in transcript levels of tomato Pi transporters may be
due to a combination of a lack of phosphate supply to roots and/or
depletion of internal Pi reserves. To obtain further insight into the
origin of the signals that regulate expression of the Pi transport
system in plants, one-half of the roots was exposed to a Pi-deficient
solution, and the other half was exposed to a solution with 250 µm Pi. Under these conditions the LePT1 and LePT2
transcript levels remained comparable in the roots exposed to either
250 µm or no Pi (Fig.
8). The accumulation of these transcripts in divided-root plants was similar to those sprayed with
250 µm Pi. Similarly, the transcript levels of LePT1 in
leaves of divided-root plants and Pi+ control plants were also
comparable. The expression of TPSI1, a gene specifically
induced in response to phosphate starvation in tomato (Liu et al.,
1997), was also similar to those of phosphate transporters. These data
suggest that even if Pi is supplied to a portion of the root system,
expression of Pi transporters in other portions of roots exposed to
Pi-deficient conditions do not increase compared with Pi-deficient
plants.
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| Figure 8.
Expression of phosphate transporters and TPSI1 is
regulated by the internal concentration of phosphate in plants. In this divided-root experiment roots of plants were exposed to either 250 µm Pi (C+) or 0 µm (C) Pi. Roots of
another set of plants were separated into two portions, and each
portion was placed in an aerated hydroponic solution containing 250 µm (D+) or 0 µm (D) Pi for 5 d.
Total RNA isolated from roots and leaves of the plants was analyzed by
northern blotting. A picture of the gel showing uniform loading of RNA
is shown.
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LePT1 and LePT2 Are Strongly Expressed in the Epidermis of
Phosphate-Starved Roots
In situ localization of the LePT1 and LePT2 transcripts was done
with digoxigenin-labeled probes to obtain information about tissue-specific expression of the phosphate transporters. In tomato plants grown under phosphorus-deficient conditions, a significant amount of chromogenic product signal for LePT1 and LePT2 transcripts was observed in the root epidermis (Fig.
9). Low levels of LePT1 transcripts in
other cell types, including the central cylinder, was also noticed in
Pi-starved roots. In addition, accumulation of the LePT1 message was
also detected in palisade parenchyma and phloem cells (data not shown)
of leaves under phosphate starvation. The significance of the presence
of higher transcript levels in palisade parenchyma cells in leaves is
not clear. Higher demand for phosphorus by the actively
photosynthesizing palisade parenchyma cells may be one of the reasons
for increased expression of phosphate transporters. These transporters
may be involved in active transport of Pi from neighboring tissues or
in the release of Pi in the apoplastic space into the palisade
parenchyma cells. Expression of LePT2 was not detected in leaf tissue
even under phosphate starvation. In situ localization of the phosphate
transporter message agrees with northern analysis of RNA.
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| Figure 9.
In situ localization of tomato
phosphate-transporter transcripts in roots and leaves. Tissue
localization of the message was done using digoxigenin-labeled LePT1
and LePT2 sense (A and C) and antisense (B and D) RNA probes. Sections
are from roots and leaves of plants grown with (A and B) and without (C
and D) phosphorus for 5 d. ep, Epidermis; cp, cortical parenchyma;
cc, central cylinder; pp, palisade parenchyma; and sp, spongy
parenchyma.
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DISCUSSION |
The uptake system for phosphate and other ions in plants consists
of high- and low-affinity components (Epstein, 1976). Under most
natural conditions in which the concentration of available Pi in soil
is very low (Barber et al., 1963), the transport of Pi by plant cells
proceeds through the high-affinity, energy-dependent proton/phosphate
symport mechanism. At the molecular level the main protein component of
this system, the phosphate transporter, has been recently characterized
from Arabidopsis (Muchhal et al., 1996; Smith et al., 1997), potato
(Leggewie et al., 1997), and C. roseus (Kai et at., 1997).
These proteins show significant structural similarity with known
high-affinity phosphate transporters and were able to complement yeast
mutants defective in high-affinity phosphate uptake activity (Muchhal
et al., 1996; Kai et at., 1997; Leggewie et al., 1997). Furthermore,
overexpression of AtPT1 (PHT1) in tobacco cell cultures enhanced cell
growth and Pi uptake under phosphate-limited conditions (Mitsukawa et
al., 1997). The deduced amino acid sequences of LePT1 and LePT2
polypeptides show a high degree of sequence similarity to other plant
phosphate transporters. LePT1 and LePT2 are greater than 95% identical
at the amino acid sequence level to STPT1 and STPT2 from potato,
respectively. This degree of similarity at the primary sequence level
among the members of the Solanaceae family is interesting, considering
the fact that, despite similar functionality, the overall sequence
similarity among phosphate transporters from plants and fungi is not
more than 42% (Muchhal et al., 1996).
The results from expression studies show that both LePT1 and LePT2
transcripts accumulate primarily in roots, and their expression is
highly induced under Pi-deficient conditions. Roots are the organs
involved in nutrient acquisition, and the expression pattern of these
two genes in roots correlates well with their function. A small amount
of LePT1 message was also detectable in the leaves, stem, and petioles
of tomato plants starved of Pi, suggesting a global role for this in
plants. The differential expression of LePT1 and LePT2 in roots and
leaves was similar to that of potato phosphate transporters described
by Leggewie et al. (1997). The induction of LePT1 and LePT2 in response
to Pi starvation correlates well with published reports of increased
phosphate uptake rate of roots and cell cultures subjected to Pi
deprivation (Clarkson and Scattergood, 1982; Drew and Saker, 1984; Katz
et al., 1986). This enhanced Pi absorption following Pi starvation has
been proposed to be associated with a larger capacity for Pi transport,
possibly by the formation of additional carriers for Pi (Anghinoni and
Barber, 1980; Lefebvre and Glass, 1982; Drew et al., 1984; Furihata et
al., 1992; Shimogawara and Usuda, 1995). In this study the transcript
levels of both LePT1 and LePT2 showed a significant increase within
1 d after the transfer to Pi-deficient medium, and reached a
maximum after about 5 d of starvation. Resupplying Pi to tomato
plants starved for 5 d repressed the LePT1 and LePT2 transcripts
back to their uninduced levels within 2 d, suggesting a role for
these two transporters in the uptake of Pi under Pi-limiting
conditions.
Increased transcription of phosphate-transporter genes in Pi-limiting
conditions has been well documented in several microorganisms (Torriani-Gorini et al., 1994). In Saccharomyces cerevisiae,
which, like plants, has both high- and low-affinity Pi uptake systems, transcription of the high-affinity phosphate transporter (PHO84) is
controlled by the availability of Pi in the medium through the action
of several positive and negative regulators constituting the
pho regulon (Youshida et al., 1987; Johnston and Carlson, 1992). By analogy, a similar feedback system for controlling the activity of Pi transporters in response to external Pi availability could be postulated for plants, since their expression appears to be
linked to the availability of Pi. However, the situation here is much
more complex, considering that Pi is a highly mobile element within
plants, and its uptake has to be coordinated with growth requirements
of tissues far away from the point of uptake.
In the divided-roots experiment, in which two halves of the root system
were exposed to different concentrations of Pi (0 and 250 µm), the level of LePT1 and LePT2 expression was similar in both halves. The amount of these transcripts, both in roots and
leaves, was also comparable to that found in the plants provided with
250 µm Pi. The expression pattern of TPSI1
(Liu et al., 1997), another phosphate- starvation-induced gene, also
indicates that tissues of divided-root plants have sufficient
phosphorus to repress phosphate-starvation-induced gene expression.
Furthermore, the total phosphorus content in leaves and roots of
Pi-sufficient (250 µm) plants was comparable to that of
leaves and roots provided with no Pi in divided-root plants (data not
shown). These results suggest that signals for increased uptake of Pi
by roots under starvation are likely due to changes in internal Pi
concentrations. Earlier reports (Lefebvre and Glass, 1982; Drew et al.,
1984) have showed that the supply of Pi to a part of the root system may partly or fully compensate for the deficiency in other parts of the
root system by greater rates of nutrient uptake. In their study a
localized supply of Pi resulted in greater translocation of labeled Pi
to the remainder of the root system exposed to a phosphate-deficient
solution. Higher mobility of Pi in both xylem and phloem may lead to
rapid equilibration of Pi concentration in tissues farther away from
the source of Pi supply. As long as the phosphate requirement of plants
is met, the expression of phosphate transporters in the entire root
system appears to be depressed.
Leaf phosphorus status may regulate uptake of Pi by the roots
(Marschner, 1995). The location of regulation of phosphate uptake away
from roots should allow plants to absorb the required amounts of the
nutrient to maintain a physiologically constant concentration in the
cytoplasm. The proposed control of phosphate uptake, directly or
indirectly, by the internal concentration of Pi should lead to a
regulated expression of phosphate-transporter genes in roots despite
wide variations in the availability of phosphorus under natural
conditions. At present the nature of the phosphate-starvation signals
are not clear. There are reports suggesting a role for ethylene in the
phosphate-starvation response (Drew et al., 1989; He et al., 1992).
Temporary deprivation of phosphorus has been shown to decrease
C2H4 production and enhance
the sensitivity of roots to ethylene during aerenchyma formation (Drew
et al., 1989; He et al., 1992). Although no direct evidence is
available at present, it is likely that ethylene may play a role as a
component of the phosphate-starvation response mechanism. Under
phosphate starvation significant amounts of carbohydrates are
translocated from shoots to roots. Even though there is no experimental
evidence for a role for sugar-mediated signals during Pi starvation,
the existence of sugar phosphate molecules in the carbohydrate pools acting as phosphate-starvation signals cannot be ignored.
In situ localization of LePT1 and LePT2 in roots and leaves correlated
with accumulation of message in specific tissues under phosphate
starvation. Localization of transcripts in the epidermis of roots and
pronounced induction of message in response to Pi starvation suggest
that epidermally localized transporters play a significant role in
phosphate acquisition under natural conditions. As Pi moves through the
apoplastic pathway, the exclusion of anions, including Pi, from the
narrow pores in the cell wall could decrease its concentration to the
submicromolar range (Clarkson, 1991). This interaction between Pi and
the apoplastic pathway could be a significant factor in maintaining the
concentration of Pi in a reasonable range for uptake by phosphate
transporters. Under these conditions the epidermis will be exposed to a
relatively higher concentration of phosphorus, as compared with other
tissues away from the surface. Higher expression of Pi transporters in root epidermis is most likely an adaptive mechanism to enhance and
optimize Pi uptake by roots under Pi-deficiency conditions. The
contribution of epidermal uptake of nutrients in general and Pi in
particular under deficiency conditions may be a significant component
of nutrient acquisition by plants. The uptake of
NO3 under low concentration is also suggested to
occur at the epidermis (Rufty et al., 1986). It was elegantly shown by
Rufty et al. (1986) using the induction of NO3
reductase as an indicator of NO3 uptake by different root
tissues. A distinct induction of NO3 reductase activity was noticed in epidermal cells under micromolar concentration. As the concentration of NO3 increased in the
bathing medium, the enzyme activity was also noticed in other cell
types, including the endodermis.
Plants have developed several adaptive mechanisms to cope with limiting
concentrations of Pi available in soils, most of which focus on
increasing the availability of external Pi and efficiency of Pi uptake
and utilization inside. However, in the constantly fluctuating
environment surrounding roots the most important response is fine
tuning of Pi uptake rate relative to the availability of Pi.
Transcriptional regulation of Pi-transporter gene expression, regulated
directly or indirectly by internal Pi, appears to be a very important
part of this control mechanism in roots.
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FOOTNOTES |
1
This research was funded in part by U.S.
Department of Agriculture-National Research Initiative Competitive
Grants Program grant no. 94-37100-0834. This is journal paper no.
15,551 of the Purdue University Agricultural Research Program.
2
The first two authors have contributed equally
to this paper and their names are listed alphabetically.
*
Corresponding author; e-mail ragu{at}hort.purdue.edu; fax
1-765-494-0391.
Received July 24, 1997;
accepted October 1, 1997.
The GenBank accession numbers described in this article are
Af022973 (LePT1) and Af022874 (LePT2).
| |
ACKNOWLEDGMENTS |
We thank Drs. P.M. Hasegawa, Jose M. Pardo, and B.C. Moser for
critically reviewing the manuscript.
| |
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Abstract
Introduction