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Plant Physiol. (1999) 119: 1041-1046
Nitrate-Ammonium Synergism in Rice. A Subcellular
Flux
Analysis1
Herbert J. Kronzucker*,
M. Yaeesh Siddiqi,
Anthony D.M. Glass, and
Guy J.D. Kirk
Department of Plant Sciences, University of Western Ontario,
London, Ontario, Canada N6A 5B7 (H.J.K.); International Rice Research
Institute, P.O. Box 933, 1099 Manila, Philippines (H.J.K., G.J.D.K.); and Department of Botany, University of British Columbia, Vancouver,
British Columbia, Canada V6T 1Z4 (M.Y.S., A.D.M.G.)
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ABSTRACT |
Many reports have shown that plant
growth and yield is superior on mixtures of
NO3 and NH4+ compared
with provision of either N source alone. Despite its clear practical
importance, the nature of this N-source synergism at the cellular level
is poorly understood. In the present study we have used the technique
of compartmental analysis by efflux and the radiotracer 13N
to measure cellular turnover kinetics, patterns of flux partitioning, and cytosolic pool sizes of both NO3 and
NH4+ in seedling roots of rice (Oryza
sativa L. cv IR72), supplied simultaneously with the two N
sources. We show that plasma membrane fluxes for
NH4+, cytosolic NH4+
accumulation, and NH4+ metabolism are enhanced
by the presence of NO3, whereas
NO3 fluxes, accumulation, and metabolism are
strongly repressed by NH4+. However, net N
acquisition and N translocation to the shoot with dual N-source
provision are substantially larger than when NO3 or NH4+ is
provided alone at identical N concentrations.
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INTRODUCTION |
Although higher plants have the capacity to utilize organic N
(Näsholm et al., 1998 ), the major sources for N acquisition by
roots are considered to be NO3
and NH4+ (Haynes and Goh, 1978).
Plants vary substantially in their relative adaptations to these two
sources of N (Kronzucker et al., 1997). Although
NH4+ should be the preferred N
source, since its metabolism requires less energy than that of
NO3 (Bloom et al., 1992), only
a few species actually perform well when
NH4+ is provided as the only N
source. Among the latter are boreal conifers (Kronzucker et al., 1997),
ericaceous species (Pearson and Stewart, 1993), some vegetable crops
(Santamaria and Elia, 1997), and rice (Wang et al., 1993; Kronzucker et
al., 1998). Most agricultural species develop at times severe toxicity
symptoms on NH4+ (Cox and
Reisenauer, 1973; Findenegg, 1987); thus, superior growth in these
species is seen on NO3
(Rideout et al., 1994). However, when both N sources are provided simultaneously, growth and yield are often enhanced significantly compared with growth on either
NH4+ or
NO3 alone. The effect is
particularly well documented in corn (Below and Gentry, 1987; Smiciklas
and Below, 1992; Adriaanse and Human, 1993) and wheat (Cox and
Reisenauer, 1973; Heberer and Below, 1989; Chen et al., 1998), but it
has also been reported in several other species (Hagin et al., 1990;
Cao and Tibbits, 1993; Gill and Reisenauer, 1993), including rice (Ta
and Ohira, 1981; Ta et al., 1981). Yield increases of 40% to 70% have
been observed in solution culture (Weissman, 1964; Cox and Reisenauer,
1973; Heberer and Below, 1989), although, commonly, somewhat smaller enhancements are obtained in soil culture and under field conditions (Hoeft, 1984; Hagin et al., 1990). Several hypotheses pertaining to the
enhanced growth and yield response on mixed N medium have been advanced
(Lewis et al., 1982; Findenegg, 1987; Gill and Reisenauer, 1993), but
mechanistic examinations of these effects have been lacking. In the
present study we have used compartmental analysis with the short-lived
radiotracer 13N to examine the reciprocal effects
of NH4+ and
NO3 on each other in root
tissue of intact rice plants with respect to N-flux partitioning and
storage capacity at the subcellular level.
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MATERIALS AND METHODS |
Plant Growth Conditions
Rice (Oryza sativa L. cv IR72) seeds were
surface-sterilized in 5% NaOCl for 10 min, rinsed with deionized
water, and left to imbibe in aerated deionized water at 30°C in a
water bath for 48 h. The partially germinated seeds were then
placed onto plastic mesh mounted on Plexiglas discs (Atohaas Americas
Inc., Philadelphia, PA) and the discs were transferred to 40-L
hydroponic Plexiglas tanks located in walk-in, controlled-environment
growth chambers. Growth chambers were maintained at 30°C ± 2°C, 70% RH, and set to a 12-h/12-h photoperiod. A photon flux of
approximately 500 µmol m2
s1, measured at plant level (with a light meter
[LI-189, Li-Cor, Lincoln, NE] and quantum sensor [LI-190SA,
Li-Cor]), was provided by fluorescent lamps (1500, F96T12/CW/VHO, 215 W, Philips, Eindhoven, The Netherlands).
Nutrient Solutions
Seedlings were cultivated for 3 weeks in hydroponic medium
contained in 40-L Plexiglas tanks. Deionized, distilled water and reagent-grade chemicals were used in the preparation of all nutrient solutions. N was provided either as 100 µM
NH4+ (in the form of
(NH4)2SO4),
as 100 µM NO3
(in the form of Ca(NO3)2),
or as 100 µM
NH4NO3. Other nutrient salts added were as follows: 1 mM
K2SO4, 2 mM
MgSO4, 1 mM
CaCl2, 300 µM
NaH2PO4, 100 µM Fe-EDTA, 9 µM
MnCl2, 25 µM
(NH4)6Mo7O24, 20 µM H3BO3,
1.5 µM ZnSO4, and 1.5 µM CuSO4. Nutrient solutions in
tanks were continuously mixed via electric circulating pumps (model
IC-2, Brinkmann). Continuous infusion of nutrient stock solution via
peristaltic pumps (Technicon Proportioning Pump II, Technicon
Instrument, Tarrytown, NY) allowed steady-state control of nutrient
concentrations in the tanks. Solutions were checked daily for
[K+] using a spectrophotometer (model 443;
Instrumentation Laboratory, Lexington, MA). The solution pH was
maintained at 6.5 ± 0.3 by addition of powdered
Ca(CO3)2. pH was monitored
daily using a microprocessor-based, pocket-size pH meter (pH Testr2
model 59000-20, Cole Parmer, Chicago, IL).
[NH4+]o
was measured (using a Philips PU 8820 UV/visible spectrophotometer) according to the method described by Solorzano (1969).
[NO3]o
was measured spectrophotometrically by the method of Cawse (1967).
Compartmental Analysis
The radiotracer 13N (half-life = 9.98 min) was produced by the cyclotron facility (Tri-University Meson
Facility) at the University of British Columbia. Proton irradiation of
a water target was used to generate 13N, a
procedure that provides chiefly
13NO3
with high radiochemical purity (Kronzucker et al., 1995b). The irradiated solutions were supplied in sealed 20-mL glass vials, with a
starting activity of 700 to 740 MBq. At this activity sufficient counts
were present in both eluates and plant samples following loading
periods of up to 60 min and a total elution period of 22 min (see
below). Procedures for the removal of radiocontaminants and conversion
of 13NO3
to 13NH4+
were as described in detail elsewhere (Kronzucker et al., 1995a, 1995b,
1995c). A volume of 20 to 100 mL of
13N-containing "stock" solution was prepared
in a fume hood and was transferred into the controlled-environment
chambers where experiments were carried out. All uptake solutions were
premixed and kept behind lead shielding. The chemical composition of
the labeling solutions was identical to that of the growth solutions in
the hydroponic tanks (see above). The protocol for efflux experiments was essentially as described elsewhere (Kronzucker et al., 1995b, 1995d, 1995e). Roots of intact rice seedlings were immersed for 60 min
in 120-mL darkened plastic beakers containing the
13NO3-
or
13NH4+-labeled
solution. Steady-state conditions with respect to all nutrients were
maintained throughout growth, loading, and elution. The duration of the
loading period was chosen on the basis of the half-lives of exchange
for the cytoplasmic compartment, i.e. approximately 14 min for
NH4+ and 16 min for
NO3. Therefore, 60 min of
exposure to tracer should ensure that cytoplasmic specific activity
approximate 95% of that in the loading solution (Kronzucker et al.,
1995e). Following loading with 13N, seedlings
were transferred to efflux funnels (Wang et al., 1993), and the roots
were eluted with 20-mL aliquots of nonradioactive solution after
varying time intervals. These time intervals ranged from 5 s to 2 min over an experimental duration of 22 min. Eluates from a total of 25 time intervals were collected separately, and the radioactivities of
each eluate were determined in a gamma-counter (Minaxi  , Auto-
5000 series, Hewlett-Packard), measuring the 511-keV positron-electron
annihilation radiation generated by recombination of ambient electrons
and  + particles emitted from
13N. After the final elution seedling roots were
excised from the shoots, the roots were spun in a low-speed centrifuge
for 30 s to remove surface liquid, and the fresh weights of roots
and shoots were determined. The plant organs were then introduced into
20-mL scintillation vials, and the radioactivities of roots and shoots were determined.
Data Analysis
All experiments were repeated five to eight times, with two
replicates per experiment. Data from several experiments were pooled
(n  10) for calculations of means and
SE. Symbols and calculation of fluxes were as
follows:  co, efflux from the cytoplasmic compartment at time 0 divided by the specific activity of
13N in the loading solution;
net, net flux, obtained from the accumulation of 13N in the plants at the end of the loading
period (60 min); oc, unidirectional influx,
calculated from net + co; xylem, flux of
13N to the shoot at the end of the elution
period; and vac./ass., combined flux to N
assimilation and the vacuole, resulting in net  xylem. Half-lives of exchange and pool
sizes were determined as described in detail elsewhere (Siddiqi et al.,
1991; Kronzucker et al., 1995a, 1995b, 1995c, 1995e).
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RESULTS AND DISCUSSION |
For both NO3 and
NH4+, compartmental analyses by
efflux revealed exchange with three subcellular compartments (Fig.
1), identified as a surface film (I), a
binding component in the cell wall (II), and the cytoplasm (III), in
keeping with previous studies in which detailed compartment identity
tests were carried out using membrane perturbation, ion-exchange
series, and metabolic modifiers (Siddiqi et al., 1991; Kronzucker et
al., 1995e). The short isotopic half-life of 13N
(9.98 min) made it impossible to trace vacuolar exchange in our study.
Half-lives of exchange for the three compartments identified in our
study were approximately 2 s, 30 s, and 16 min, respectively, for NO3, and 2 s, 40 s, and 14 min, respectively, for
NH4+ (data not shown). These
half-lives were very similar to those reported for N exchange in other
studies (Wang et al., 1993; Kronzucker et al., 1995e, 1997), with no
significant differences in the presence of the other ion. Cytoplasmic
NO3 exchange, however,
exhibited half-lives that were about two to three times as long as
those observed for other species (compare Devienne et al., 1994;
Kronzucker et al., 1995a). The relatively long half-life for cytosolic
exchange of NO3 in rice may be
seen as an indication of a relatively small negative feedback upon
NO3 influx by cytoplasmic
NO3, in keeping with a high
cytosolic accumulation capacity and efficiency of uptake for
NO3 in this species (H.J.
Kronzucker, A.D.M. Glass, M.Y. Siddiqi, and G.J.D. Kirk, unpublished
results). It is surprising to find such high capacity and efficiency
for NO3 capture in rice, which
traditionally has been assumed to prefer NH4+-N (compare Wang et al.,
1993; Kronzucker et al., 1998). Notwithstanding the substantial
rates of both NO3 influx and
net flux, we found a strong inhibitory effect of
NH4+ on the latter (Table
I). Such repression of
NO3 uptake by
NH4+ has been documented in many
species (Jackson et al., 1976; MacKown et al., 1982; Lee and Drew,
1989; Aslam et al., 1997; Colmer and Bloom, 1998), although there has
been an ongoing debate about whether the effect is primarily upon
influx or efflux (Kronzucker et al., 1999).
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| Figure 1.
Representative semilogarithmic plots for the rate
of release of 13NO3 [log
(cpm released) g1 h1] versus time
of elution for roots of intact cv IR72 rice seedlings maintained at 100 µM [NO3]o with
NH4+ ( ) or without
NH4+ ( ). Plots include linear regression
lines for the three phases of efflux (I, surface film; II, cell wall;
III, cytoplasm). Regression lines are dashed for the
+NH4+ treatment and solid for the control
(phase I overlapped). See text for derivation of compartmental
parameters.
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View this table:
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Table I.
Component fluxes for NH4+
and NO3 as determined by compartmental
analysis
Rice plants were grown on 100 µM
NO3, 100 µM
NH4+, or 100 µM
NH4NO3. The bottom row indicates combined N
fluxes in the NH4NO3 treatment. For flux
symbols, see ``Materials and Methods''. Data are means ± SE (n 10).
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Our present study shows that, under steady-state coprovision of the two
N sources, NO3 influx and
efflux are both significantly repressed by
NH4+, compared with plants fed
only with NO3 (Table I).
Influx was repressed by approximately 50% (Colmer and Bloom, 1998) and
efflux by almost 40%, so that
NO3-net acquisition in the
presence of NH4+ was 2.2 times
less than with NO3-only
provision. Thus, it is clear that, under steady-state conditions, the
principal effect of NH4+ on net
NO3 uptake is through its
repressive action on influx, not through enhancement of efflux, which
supports the conclusions by Lee and Drew (1989) and our own group
(Kronzucker et al., 1999; compare Aslam et al., 1997). Also, since
NO3 efflux constituted only
8.7% (with NO3) to 11.4%
(with NO3 plus
NH4+) of
NO3 influx, any effect on
efflux could make only a negligible contribution to net
NO3 acquisition. The same
trend as for NO3 fluxes was
observed for cytosolic NO3
accumulation capacity. Figure 1 shows overlaid efflux plots for NO3 in the presence and
absence of NH4+, with a
significant downward y-axis shift being evident for
NO3 efflux from the
cytoplasmic compartment in the presence of
NH4+. By contrast, half-life for
cytoplasmic exchange, as seen in the slope of the regression line for
compartment III, was not changed. Given this half-life constancy, the
y-axis intercepts for 13N efflux from
compartment III in Figure 1 reflect directly the relative sizes of the
cytoplasmic NO3 pools. As
shown in Figure 2, cytoplasmic
[NO3] was depressed from 36 ± 4.5 mM with
NO3-only provision to 17.8 ± 3.6 mM in the presence of
NH4+.
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| Figure 2.
Cytoplasmic pool sizes (in mM) of
NO3 and NH4+ in roots
of intact cv IR72 rice seedlings in the presence (black bars) or
absence (white bars) of the other N source. Plants were under
steady-state conditions with respect to N treatments. Error bars
indicate SE (n 10).
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In the reverse experimental design, compartmental analysis revealed
unexpected effects of NO3 on
NH4+ fluxes. Cytoplasmic
[NH4+] was not affected
significantly by the presence of
NO3 (Fig. 2). Due to this,
efflux plots for NH4+ with or
without NO3 virtually
overlapped (data not shown). However,
NH4+ influx was increased by
almost 25% when NO3 was
provided at the same time (Table I). Concurrently,
NH4+ efflux was decreased by
NO3 almost 2-fold. As a
result, net NH4+ acquisition was
improved by as much as 50% compared with the NH4+-only control. Under
perturbational conditions, since N-deprived plants were resupplied with
N, a stimulatory effect of NO3
on NH4+ uptake has been recorded
previously for soybean (Rideout et al., 1994; Saravitz et al., 1994).
Here we show that NH4+ uptake is
stimulated substantially as well under steady-state conditions.
Perhaps even more important, however, is the finding that N-flux
partitioning patterns changed significantly when both N sources were
provided compared with either
NH4+ or
NO3 alone. For both
NH4+ and
NO3, if supplied alone,
approximately 50% of incoming N remained in roots, either channeled to
assimilation or to the vacuole, whereas a relatively smaller proportion
was translocated to the shoot, approximately 38% of incoming
13N in the case of
NO3 and 26% in the case of
NH4+. With coprovision of the
other N source, xylem-N translocation increased substantially, to
approximately 49% on NO3 (in
the presence of NH4+) and to
approximately 56% on NH4+ (in
the presence of NO3). Our
compartmental analyses do not allow us to determine the biochemical
profiles of N-translocation compounds, nor can the specific activities
of the respective xylem-loading pools of these compounds be known.
Hence, the xylem-translocation data presented here include not only the
NO3 and
NH4+ species, respectively, but
also N metabolites and, thus, a fraction of the assimilatory flux.
Whereas in the case of NO3
long-distance N translocation increased only in percentage terms, an
absolute increase was seen in the case of
NH4+. It has been suggested that
the inhibition of NO3 uptake
might be accompanied by an inhibition of nitrate reductase in roots
(Smith and Thompson, 1971; Radin, 1975; MacKown et al., 1982);
therefore, the increased proportion of N translocated to the shoot in
the case of NO3 is likely to
be accompanied by a decreased rate of N metabolism and hence a lower
ratio of N metabolites to free
NO3 in the xylem. Since, under
most conditions, NH4+ is not
transported as such in the xylem of rice at appreciable concentrations
(Wang et al., 1993; Kronzucker et al., 1995e), the translocation
increase with NH4+ in the
presence of NO3 must be due to
a stimulation of NH4+
assimilation. A similar
NO3-specific stimulation of
NH4+ assimilation has been
reported elsewhere for radish plants (Goyal et al., 1982; Ota and
Yamamoto, 1989). We propose that the specific induction by
NO3 of the proplastidic
glutamine synthetase/glutamate synthase pathway (Redinbaugh and
Campbell, 1993), in addition to the one localized in the cytoplasm,
opens up an assimilatory flux potential that is not available to plants
grown on pure NH4+. It is
possible that significant portions of N derived from both incoming
NO3 and
NH4+ could be channeled through
this pathway. The increased shoot translocation of N is likely to have
important agronomic consequences. In the case of rice, in excess of
70% of N in the grain at harvesting and more than 50% of N in
photosynthetically active leaves during grain filling are drawn from N
that accumulated in shoot tissue during vegetative growth (Mae et al.,
1985, and refs. therein); on the other hand, the rice root system
during grain filling is subject to senescence.
In summary, our analyses document distinct changes in the pattern of
N-flux partitioning when NO3
and NH4+ are supplied together,
compared with provision of either
NO3 or
NH4+ alone. At least in part,
the frequently observed growth and yield maximization on a combined
N-source diet (see the introduction) can be attributed to an
up-regulation of NH4+ uptake and
metabolism by NO3. Although
uptake, metabolism, and cytosolic accumulation of
NO3 are depressed by as much
as 50% by the simultaneous presence of
NH4+, when contributions to the
N budget from both NO3 and
NH4+ are taken into account (see
Table I), a substantially larger N-acquisition rate is achieved than
would be possible with either NH4+ or
NO3 alone at an identical
external N concentration (i.e. 200 µM in our
experiments). The Michaelis-Menten saturation kinetics of the
individual influx components allow for an increase in influx of
approximately only 12% with an increase in external N from 100 to 200 µM (compare Siddiqi et al., 1990; Kronzucker et al., 1998); by contrast, the combined N intake from the
NO3/NH4+
mixture is approximately 20% and 75% larger than individual fluxes at
200 µM in the case of
NO3 and
NH4+, respectively. It is clear
that this benefit from combined N-source provision must be most
pronounced at higher concentrations of external N, as influx isotherms
are near or at saturation (Siddiqi et al., 1990; Kronzucker et al.,
1995d, 1996). In our study with rice, the additive N-budget advantage
due to the combined influx components was further enhanced by a
reduction in N loss through efflux. In addition, a significant shift in
N partitioning was observed in favor of N allocation to the shoot, with
agronomic consequences that are likely not trivial.
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FOOTNOTES |
1
The work reported in this paper was supported by
funds from the "New Frontier" project grant to the International
Rice Research Institute and by a University of Western Ontario grant to
H.J.K.
*
Corresponding author; e-mail kronzuck{at}julian.uwo.ca; fax
1-604-822-6089.
Received August 19, 1998;
accepted December 8, 1998.
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ACKNOWLEDGMENTS |
For technical help and discussion we thank D.T. Britto, M. Okamoto, D. Zhuo, and the staff at the Tri-University Meson Facility for the particle accelerator.
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Top
Abstract
Introduction