*Present address: Department of Plant Sciences, University of Western Ontario, London, Ontario, N6H 5B7, Canada
A comparative kinetic analysis of nitrate and ammonium influx in two early-successional tree species of temperate and boreal forest ecosystems
Article first published online: 25 DEC 2001
Plant, Cell & Environment
Volume 23, Issue 3, pages 321–328, March 2000
How to Cite
Min, X., Siddiqi, M. Y., Guy, R. D., Glass, A. D. M. and Kronzucker, H. J. (2000), A comparative kinetic analysis of nitrate and ammonium influx in two early-successional tree species of temperate and boreal forest ecosystems. Plant, Cell & Environment, 23: 321–328. doi: 10.1046/j.1365-3040.2000.00546.x
- Issue published online: 25 DEC 2001
- Article first published online: 25 DEC 2001
- ammonium fluxes;
- kinetics of nitrate and ammonium uptake;
- lodgepole pine;
- nitrate fluxes;
- nitrogen nutrition;
- trembling aspen
Root NO3− and NH4+ influx systems of two early-successional species of temperate (trembling aspen: Populus tremuloides Michx.) and boreal (lodgepole pine: Pinus contorta Dougl. ex Loud. var. latifolia Engelm.) forest ecosystems were characterized. NO3− and NH4+ influxes were biphasic, consisting of saturable high-affinity (HATS) and constitutive non-saturable low-affinity transport systems (LATS) that were evident at low and relatively high N concentrations, respectively. NO3− influx via HATS was inducible (IHATS); nitrate pre-treatment resulted in 8–10-fold increases in the Vmax for influx in both species. By contrast, HATS for NH4+ were entirely constitutive. In both species, Vmax values for NH4+ influx were higher than those for NO3− uptake; the differences were larger in pine (6-fold) than aspen (1·8-fold). In aspen, the Km for NH4+ influx by HATS was approximately 3-fold higher than for IHATS NO3− influx, while in pine the Km for IHATS NO3− influx was approximately 3-fold higher than for NH4+ influx. The aspen IHATS for NO3− influx appeared to be more efficient than that of pine (Vmax values for aspen being approximately 10-fold higher and Km values being approximately 13-fold lower than for pine). By contrast, only small differences in values for the NH4+ HATS were evident between the two species. The kinetic parameters observed here probably result from adaptations to the N availabilities in their respective natural habitats; these may contribute to the distribution and niche separation of these species.
In most late-successional communities of temperate and boreal forest ecosystems, NH4+ is generally the main source of soil inorganic N (e.g. Van Cleve et al. 1983 ; Chapin, Van Cleve & Tyron 1986; Lavoie, Vezina & Margolis 1992). Natural or artificial disturbances result in increased rates of nitrification, increased [NO3−], and low [NH4+] in the soils (e.g. Likens, Bormann & Johnson 1969; Lodhi & Killingbeck 1980; Van Cleve et al. 1983 ; Walley, Van Kessel & Pennock 1996). Plant species differ greatly in their capacities for the utilization of particular N forms and these adaptations may contribute to the unique spatial and/or temporal distributions of these species (e.g. Bledsoe & Rygiewicz 1986; Chapin, Moilanen & Kielland 1993; Kronzucker, Siddiqi & Glass 1997; Min et al. 1998 , 1999). Thus, at relatively low external [N] ([N]o), i.e. in the range of high-affinity transport systems (HATS; see Glass & Siddiqi 1995), late-successional species e.g. Picea glauca (white spruce) show a clear preference for the utilization of NH4+ over NO3− ( Kronzucker, Glass & Siddiqi 1995a; Kronzucker, Siddiqi & Glass 1995b, c, d; 1996, 1997). By contrast, Populus tremuloides (trembling aspen) and Pseudotsuga menziesii var. glauca (Douglas fir), two early-successional species, have relatively high capacities for NO3− acquisition and can maintain apparently adequate cytoplasmic [NO3−] ([NO3−]cyt) for optimal rates of reduction even at low (0·1 mol m−3) [NO3−]o ( Min et al. 1999 ). In the same study, Pinus contorta var. latifolia (lodgepole pine), another early-successional species, showed a much lower capacity for NO3− uptake at 0·1 [NO3−]o and failed to maintain adequate [NO3−]cyt for optimal rates of reduction ( Min et al. 1999 ). In pine, however, NO3− uptake rates and [NO3−]cyt increased greatly at the higher [NO3−]o (1·5 mol m−3). Interestingly, lodgepole pine is generally associated with fire-disturbed sites where soil [NO3−] may be high ( Klinka et al. 1990 ; Brayshaw 1996).
The concentration-dependent differences in the capacities for N utilization among the early-successional species described above prompted us to undertake more detailed kinetic analyses of the NO3− and NH4+ influx systems of these species. In aspen and lodgepole pine, NO3− and NH4+ influxes were biphasic, as in several other species ( Glass & Siddiqi 1995). A high-affinity transport system (HATS) was saturable and operated at low external N concentration, while at higher [N]o a linearly concentration-dependent, low-affinity transport system (LATS) was evident. There were substantial differences between the two species in the characteristics of these transport systems. Since the aim of the present study was to characterize the NO3− and NH4+ transport systems of the tree species per se, plants used in the present studies were grown in hydroponic systems free of mycorrhizal associations ( Min et al. 1998 , 1999; see also Kronzucker et al. 1997 ).
MATERIALS AND METHODS
Seeds of trembling aspen (Populus tremuloides Michx., seedlot 40959) and lodgepole pine (Pinus contorta Dougl. ex Loud. var. latifolia Engelm., seedlot 3847) were obtained from the Tree Seed Centre, Ministry of Forests, Surrey, British Columbia, Canada. Seeds were germinated in styroblocks in a 2:1 (v/v) peat/perlite mixture, containing dolomite at the rate of 4·3 kg m−3. Seedlings were maintained in the peat/perlite mixture in a greenhouse for approximately 3 months. They were then transferred to hydroponic tanks (40 L capacity) containing aerated modified 0·1 strength Johnson’s solution with the desired NO3− or NH4+ concentration, provided as Ca(NO3)2 or (NH4)2SO4 ( Min et al. 1999 ). The nutrient solutions were buffered at pH 6·4–6·8 by adding excess powdered CaCO3. The hydroponic tanks, containing the seedlings, were maintained in a controlled environment room at 20 ± 2 °C, 70% relative humidity and 16 h light/8 h dark period. Light was provided at 250 μmol m−2 s−1 at plant level by fluorescent tubes with spectral composition similar to sunlight (Vita-Lite, Duro-Test, Fairfield, NJ, USA).
NO3− and NH4+ pre-treatments
Plants were grown in low N (a pulse of 25 mmol m−3) for the first 15 d, and then transferred to solutions without N or containing 0·1 mol m−3 NO3− or NH4+ for 5 d prior to influx measurements. We have observed that both NO3− and NH4+ fluxes had reached steady values within 4–5 d of pre-treatment with NO3− and NH4+, respectively ( Kronzucker et al. 1996 ; Min et al. 1998 , 1999). The reason for restricting the N supply to the 5 d prior to influx determinations was that we detected appreciable formation of NO2− in the culture solutions when 0·1 mol m−3 NH4+ was present for 10 d or more. This probably resulted from the activity of nitrifying organisms carried over from the peat/perlite growth medium. Thus, a 5 d pre-treatment with 0·1 mol m−3 NH4+ provided a means of avoiding NO2− accumulation without sacrificing apparent steady-state conditions ( Min et al. 1999 ).
Production and purification of 13NO3− and 13NH4+
The radiotracer 13N (half-life = 9·96 min) was produced as 13NO3− by proton irradiation of H2O at the TRIUMF Cyclotron on the campus of the University of British Columbia, Vancouver, Canada. In the case of 13NO3− experiments, radio-contaminants were removed as described by Kronzucker et al. (1995a) , except that 5 cm3 of 0·1 mol m−3 (instead of 2·5 mmol m−3) Ca(NO3)2 were used to elute residual 13NO3− from the SEP-PAC Alumina-N cartridge ( Min et al. 1998 ). Briefly, 18F was removed by passing the sample through a SEP-PAC Alumina-N cartridge (Waters, Milford, Massachusetts, USA) twice. The sample was then alkalinized by adding KOH and boiled for 2·5 min to volatilize 13NH3. Subsequently, 13NO2− was oxidized by adding H2SO4 and H2O2 and boiling for another 2·5 min. The solution was cooled to room temperature, neutralized and excess H2O2 reduced by adding catalase.
Influx of NO3− or NH4+ was measured from modified 0·1 strength Johnson’s nutrient solution containing appropriate concentrations of 13N-labelled NO3− or NH4+. Seedlings were transferred from hydroponic tanks to a non-radioactive solution, identical in composition (except for isotope) to the uptake solution, for 5 min; they were then transferred to 13N-labelled uptake solution for 10 min. Immediately following isotope loading, roots were dipped into a non-radioactive solution for 5 s, and then transferred to a non-radioactive solution, which was otherwise identical to the uptake solution, for 2 min to remove 13NO3− and for 3 min to remove 13NH4+ from the free space ( Kronzucker et al. 1995a , d). Following desorption, roots were excised from shoots, spun for 45 s in a low-speed centrifuge to remove surface solution, and fresh weights determined. Radioactivities of the shoots and roots were measured with a Packard-γ-counter (Minaxi, Auto-gamma 5000) and NO3− and NH4+ fluxes thus determined were expressed as μmol g−1 root fresh weight h−1.
All experiments were performed 3–5 times; within each experiment, each treatment was replicated 3–4 times.
RESULTS AND DISCUSSION
Kinetic analyses ( Figs 1–4) revealed that in both trembling aspen and lodgepole pine, influxes of NO3− and NH4+ are mediated by distinct high- and low-affinity transport systems (HATS and LATS, respectively). This is consistent with earlier reports regarding the uptake of NO3−, NH4+ and several other ions, in other species ranging from unicellular organisms to higher plants (e.g. Epstein 1976; Serra et al. 1978 ; Kochian & Lucas 1982; Siddiqi et al. 1990 ; Aslam et al. 1992 ; Wang et al. 1993b ; Kronzucker et al. 1995b , 1996; see also Glass & Siddiqi 1995 and Crawford & Glass 1998 for reviews). Below approximately 0·5 mol m−3, saturable NO3− and NH4+ influxes occurred via their respective HATS ( Figs 1 & 2), while at high [N]o, NO3− and NH4+ influxes occurred via their respective LATS. The latter showed no indication of saturation, being linearly dependent on [N]o up to 40 mol m−3 [N]o ( Figs 3 & 4). However, both HATS and LATS showed substantial quantitative differences between the two species, between the two ions and between N-pre-treated and untreated plants, as discussed below.
HATS for NO3− and NH4+ uptake
Consistent with the data for other species ( Glass & Siddiqi 1995 for review), NO3− influx into the roots of trembling aspen and lodgepole pine by HATS was inducible. In plants grown at 0·1 mol m−3 NO3− (induced), Vmax values for NO3− influxes were 8-fold (pine) to 10-fold higher (aspen) than those of non-induced plants, i.e. plants grown without NO3− ( Fig. 1, Table 1). Fluxes measured in non-induced plants at low external [NO3−] result from the activities of constitutive high-affinity transport system (CHATS; Aslam et al. 1992 ; King et al. 1992 ). It has been argued that CHATS is genetically distinct from the inducible high-affinity transport system (IHATS), and their simultaneous existence in induced barley and white spruce seedlings has been demonstrated ( Aslam et al. 1992 ; Kronzucker et al. 1995b ; Glass & Siddiqi 1995). Indeed, Wang & Crawford (1996) have identified a mutant of Arabidopsis thaliana (chl8) that appears to be defective in this CHATS activity
|Vmax (μmol g−1 h−1)||Km (mmol m−3)|
|Minus N||Plus N||Minus N||Plus N|
|Aspen||0·305 ± 0·013||3·00 ± 0·10||3·43 ± 1·14||11·69 ± 1·90|
|Pine||0·042 ± 0·003||0·354 ± 0·080||5·91 ± 1·37||153·4 ± 59·2|
|Aspen||9·88 ± 1·27||5·53 ± 0·86||59·5 ± 15·1||45·1 ± 17·5|
In agreement with our earlier results ( Min et al. 1998 , 1999), at low [NO3−]o, aspen seedlings showed a much higher capacity for NO3− uptake than the pine seedlings: Vmax for influxes in aspen were approximately 9-fold (IHATS) and approximately 7-fold (CHATS) higher than pine in induced and non-induced plants, respectively. Further, the Km for NO3− influx was approximately 13-fold higher in pine than in aspen. This implies that both at high and low [NO3−]o, aspen would absorb NO3− by HATS activity more effectively than pine. Furthermore, the two species differed with respect to the concentration ranges of their respective HATS for NO3− influx. In both induced and non-induced aspen seedlings, NO3− influx was saturable up to 0·2 mol m−3 [NO3−]o and LATS was evident at ≥ 0·5 mol m−3 [NO3−]o ( Fig. 1a). In non-induced pine, on the other hand, influx was saturable only up to 0·05 mol m−3 [NO3−]o and a linear system was evident at approximately 0·05 mol m−3 [NO3−]o ( Fig. 1b). In non-induced barley seedlings also, a linear LATS was evident at low [NO3−]o ( Siddiqi et al. 1990 ). In aspen, exposure to NO3− caused the Km for NO3− influx to increase approximately 3-fold ( Table 1). However, this decrease of affinity is more than compensated by the increase of Vmax. In pine, the decrease of affinity associated with induction was much larger (approximately 26-fold) probably having a significant impact upon influx. Aslam et al. (1992) and Kronzucker et al. (1995b) also reported an increase in Km of a similar magnitude following induction in barley and white spruce, respectively. An examination of Fig. 1(b) suggests, however, that the observed Vmax and Km values for NO3− influx by HATS in the induced pine seedlings may have been over-estimated, because of the relatively high contribution to measured fluxes from the LATS. This presumes that influx by LATS was similar in induced and non-induced plants ( Fig. 3b; see also Siddiqi et al. 1990 ). By virtue of a high LATS contribution to total NO3− uptake, the difference between induced and non-induced plants is less in pine ( Fig. 1b). Indeed, this may account for the fact that average tissue [NO3−] in induced and non-induced pine seedlings were similar ( Min et al. 1998 ) and [NO3−]cyt in 0·1 mol m−3 NO3−-grown plants was also very low ( Min et al. 1999 ).
In contrast to NO3− influx, NH4+ influx was not inducible ( Fig. 2, Table 1). Whereas in pine both Vmax and Km of HATS for NH4+ influx were similar between NH4+-pre-treated and untreated plants ( Fig. 2b, Table 1), in aspen NH4+ pre-treatment reduced (down-regulated) Vmax to approximately 50% ( Glass & Siddiqi 1995) but had little effect on Km ( Fig. 2a, Table 1). This down-regulation of NH4+ influx has been demonstrated to result from effects of root glutamine, acting upon AMT1 transcript level in Arabidopsis thaliana ( Rawat et al. 1999 ). Consistent with our earlier results ( Min et al. 1999 ), aspen showed a higher capacity for NH4+ uptake than pine, but the differences (2·7-fold between N-treated plants) were not as large as the corresponding differences in NO3− influx by HATS (≥ 10-fold).
Clearly, at low [NO3−]o (HATS range), aspen has a high capacity for both NO3− and NH4+ uptake (Vmax 3·0 and 5·53 μmol g−1 h−1, respectively). By contrast, pine appears to have a much lower capacity for NO3− uptake than NH4+ uptake (Vmax 0·354 and 2·07 μmol g−1 h−1, receptively). Indeed, in pine, the differences between NO3− uptake and NH4+ uptake increased with decreasing [N]o; the Km for NO3− uptake was approximately 3-fold higher than that for NH4+ ( Table 1). Several other coniferous species show the same preference for NH4+ over NO3− (e.g. Boxman & Roelofs 1988; Marschner, Häussling & George 1991; Kronzucker et al. 1997 ). In aspen, by contrast, the Km for NH4+ uptake was approximately 4-fold higher than that for NO3− uptake. We have suggested that, in pine, unlike aspen, NO3− uptake from 0·1 mol m−3 [NO3−]o was not adequate to maintain a [NO3−]cyt that is optimal for metabolism ( Min et al. 1999 ). By comparison, [NH4+]cyt at 0·1 mol m−3 [NH4+]o were similar between the two species ( Min et al. 1999 ). The same study established that at higher [NO3−]o (1·5 mol m−3) fluxes and [NO3−]cyt of the two species were similar ( Min et al. 1999 ).
LATS for NO3− and NH4+ uptake
In aspen, NO3− influx by the LATS was higher in induced than non-induced seedlings even after subtracting the Vmax for HATS ( Fig. 3a). By contrast, in pine, NO3− pre-treatment had no effect on influx by LATS ( Fig. 3b). The latter pattern conforms to that observed in several other species where LATS for NO3− has been shown to be constitutive, e.g. barley ( Siddiqi et al. 1990 ; Glass et al. 1990 ) and white spruce ( Kronzucker et al. 1995b ). In the cases of barley and white spruce, NO3− influx by LATS (after subtracting the Vmax for HATS) was higher in non-induced plants than plants grown with NO3−, indicating some down-regulation of LATS by accumulated N. Likewise, Touraine & Glass (1997) demonstrated that LATS activity in roots of Arabidopsis thaliana was partially down-regulated by growth on NH4NO3 but not by growth on KNO3. In contrast to the apparent constitutive nature of LATS at the physiological level, Tsay et al. (1993) demonstrated that the NRT1 gene (formerly CHL1), considered to encode the LATS in this species, was inducible by exposure to NO3−. Notwithstanding the apparent (but relatively small) increase of LATS activity associated with provision of NO3− in aspen, it is unclear whether this represents a real ‘induction’ phenomenon or simply an expression of increased growth arising from improved N supply.
Interestingly, while the HATS capacity of pine for NO3− was low (see above), the capacity of its LATS for NO3− uptake was substantial ( Fig. 3). Although NO3− influxes by LATS were still higher in aspen than pine ( Fig. 3a,b; Table 2), the differences were only approximately 2-fold or less compared to ≥ 10-fold differences for the HATS. This high LATS activity in pine may represent an important adaptation for colonizing sites which have high soil [NO3−].
|Comparison||Slope||y intercept||Slope||y intercept|
|LATS (+ HATS)|
|Pine: –N versus +N||NS||NS||NS||*|
|Aspen: –N versus +N||*||***||NS||*|
|–N: pine versus aspen||NS||***||NS||**|
|+N: pine versus aspen||NS||***||NS||**|
|LATS (– HATS)|
|Pine: –N versus +N||NS||**|
|Aspen: –N versus +N||**||**|
|–N: pine versus aspen||**||NS|
In the case of NH4+, both species showed higher LATS fluxes in NH4+-pre-treated than untreated plants, although the differences in pine were relatively small ( Fig. 4a,b). This is consistent with the results reported for rice ( Wang et al. 1993b ) and Arabidopsis ( Rawat et al. 1999 ). Lower fluxes in untreated plants in the rice studies were attributed to an N-deficiency ( Wang et al. 1993b ). In the study by Kronzucker et al. (1996) , however, fluxes by LATS of untreated white spruce seedlings were higher than those of NH4+-pre-treated seedlings. It may be that in the latter, N-deficiency was not as severe as in the relatively fast-growing aspen.
As noted earlier, we have characterized the kinetics of NO3− and NH4+ uptake in aspen and lodgepole pine seedling roots without any confounding effects of mycorrhizae. We emphasize that the lack of mycorrhization does not detract from the ecological significance of the present study for the following reasons. (a) NO3− uptake is not affected significantly by the presence of mycorrhizae ( Rygiewicz et al. 1984 ; Plassard et al. 1993 ) and therefore their presence is not likely to improve the NO3− acquisition capacity of lodgepole pine. (b) In the case of NH4+, roots of both species show relatively high capacities for NH4+ uptake even from low external concentrations although the presence of mycorrhizae may further enhance NH4+ uptake capacity. In fact, in the case of NH4+, its exclusion rather than its enhanced abstraction may be ecologically more important, especially in the light of potential toxicity of the ion ( Kronzucker et al. 1995d , 1996; Gerendas et al. 1997 ; Min et al. 1999 ). Moreover, mycorrhization is inhibited with increasing nutrient status of soil including that of NH4+ (e.g. Haug 1990; Marschner et al. 1991 ; de Graaf et al. 1998 and references therein).
It should be pointed out that the [NO3−]o and [NH4+]o we have used for kinetic determinations in the present study, as well as in our recently published studies ( Kronzucker et al. 1995a , b, c, d; 1996, 1997; Min et al. 1998 , 1999), are ecologically relevant. In temperate and boreal forest ecosystems, exchangeable soil NH4+–N concentrations range from 1·5–100 mg kg−1 (e.g. Vitousek et al. 1982 ); free NH4+, which may vary with soil type, is estimated to be approximately 10% of the exchangeable value, translating into approximately 0·054–3·5 mol m−3 (based on an average 20% water content). These estimates agree well with the few published values for free NH4+ concentrations in forest soil solutions (e.g. Vogt & Edmonds 1982; Gijsman & De Willigen 1991). Nitrate-N concentrations generally range from undetectable levels to approximately 12 mg kg−1 soil (e.g. Vitousek et al. 1982 ). In contrast to NH4+, however, NO3− is not bound and therefore these figures closely approximate the free NO3− concentrations. Generally, in late-successional coniferous forests, soil N is dominated by NH4+, while NO3− may be extremely low (e.g. Lodhi & Killingbeck 1980; Kronzucker et al. 1997 and references therein). Following disturbance, soil [NH4+] and [NO3−] may vary from low micromolar to several millimolar ( Vitousek et al. 1982 ; Prescott 1997), depending on a host of environmental and biotic factors, even among clear-cut sites. However, it is well established that during the first few years after clear-cut, when seedling establishment takes place, rates of nitrification increase and NH4+/NO3− ratios decline ( Lodhi & Killingbeck 1980; Vitousek et al. 1982 ; Gijsman & De Willigen 1991; Truax et al. 1994 ). For example, in a clear-cut, Truax et al. (1994) found soil [NH4+] and [NO3−] to be approximately 0·05 and 1·3 mol m−3, respectively, yielding an NH4+/NO3− ratio of 0·038. Where total inorganic N is low, it is likely that [NO3−] may be in the micromolar range, and [NH4+] may be almost negligible (see e.g. Vitousek et al. 1982 ). In the case of fire disturbance, however, both [NO3−] and [NH4+] may increase; but rates of nitrification also increase and NH4+/NO3− ratios still decline (e.g. Raison 1979).
In summary, aspen represents a generalist species with respect to soil N, equally capable of thriving on low and high NO3− or NH4+. By contrast, kinetic parameters for N acquisition in lodgepole pine identify it as a specialist species particularly well adapted to high soil N concentrations characteristic of forest soils after fire ( Raison 1979; Klinka et al. 1990 ; Brayshaw 1996), and at some such sites it may persist as an edaphic climax species (e.g. Pfister & Daubenmire 1975, Lotan & Critchfield 1990). The exclusion of species such as aspen and lodgepole pine from late-successional stands where soils are dominated by NH4+ (e.g. Kronzucker et al. 1997 ) may possibly be related to toxicity associated with high soil [NH4+] ( Givan 1979; Magalhaes et al. 1992 ) and/or other environmental factors that remain to be resolved.
We wish to thank the following: Dev Britto, Anshuman Kumar, Mamoru Okamoto, John Vidmar and Degen Zhuo, of the Department of Botany, University of British Columbia, for assistance during the experiments involving 13N, Mike Adam, Tamara Hurtado and Tom Ruth of the TriUniversities Meson Facility (TRIUMF), University of British Columbia campus, for production of the isotope. 13N was provided as a gift by TRIUMF. Financial support to R.D.G. and A.D.M.G. by Forest Renewal British Columbia (FRBC) and the Natural Sciences and Engineering Research Council of Canada is gratefully acknowledged.
- 1992) Comparative kinetics and reciprocal inhibition of nitrate and nitrite uptake in roots of uninduced and induced barley (Hordeum vulgare L.) seedlings. Plant Physiology 99, 1124 1133. , , (
- 1986) Ectomycorrhizas affect ionic balance during ammonium uptake by Douglas-fir roots. New Phytology 106, 271 283. & (
- 1988) Some effects of nitrate versus ammonium nutrition on the nutrient fluxes in Pinus sylvestris seedlings: effects of mycorrhizal infection. Canadian Journal of Botany 66, 1091 1097. & (
- 1996) Trees and Shrubs of British Columbia. University of British Columbia Press, Vancouver. (
- 1986) Relationship of ion absorption to growth rate in taiga trees. Oecologia 69, 238 242. , , (
- 1993) Preferential use of organic nitrogen for growth by a non-mycorrhizal arctic sedge. Nature 361, 150 153. , , (
- 1998) Molecular and physiological aspects of nitrate uptake in plants. Trends in Plant Sciences 3, 389 395. & (
- 1976) Kinetics of ion transport and the carrier concept. In Transport in Plants. II. Part B. Tissues and Organs. Encyclopaedia of Plant Physiology, New Series, Volume 2 (eds U. Lüttge & M.G. Pitman), pp. 70 94. Springer Verlag, Berlin. (
- 1997) Physiological and biochemical processes related to ammonium toxicity in higher plants. Zeitschrift für Pflanzenernährung und Bodenkunde 160, 239 251. , , , , (
- 1991) Modelling ammonium and nitrate uptake by a mature Douglas-fir stand from a soil with high atmospheric NHx input. Netherlands Journal of Agricultural Science 39, 3 20. & (
- 1979) Metabolic detoxification of ammonia in tissues of higher plants. Phytochemistry 18, 375 382. (
- 1995) Nitrogen absorption in higher plants. In Nitrogen Nutrition in Higher Plants (eds H.S. Srivastava & R.P. Singh), pp. 21 55. Associated Publishers, New Delhi, India. & (
- 1990) Studies of the uptake of nitrate in barley. II. Energetics. Plant Physiology 93, 1585 1589. , , , (
- 1998) Differential effects of ammonium and nitrate on three heartland species. Plant Ecology 135, 185 196. , , , (
- 1990) Mycorrhization of Picea abies with Pisolithus tinctorius at different nitrogen levels. Agriculture Ecosystems and Environment 28, 167 170. (
- 1992) Studies of the uptake of nitrate in barley. V. Estimation of root cytoplasmic nitrate concentration using nitrate reductase activity – implications for nitrate influx. Plant Physiology 99, 1582 1589. , , (
- 1990) Ecological principles. applications. In Regenerating British Columbia’s Forests (eds D.P. Lavender, R. Parish, C.M. Johnson, G. Montgomery, A. Vyse, R.A. Willis & D. Winston), pp. 55 72. University of British Columbia Press, Vancouver. , , , , , (
- 1982) Potassium transport in corn roots. I. Resolution of kinetics into a saturable and linear component. Plant Physiology 70, 1723 1731. & (
- 1995a) Nitrate induction in spruce. an approach using compartmental analysis. Planta 196, 683 690. , , (
- 1995b) Kinetics of NO3− influx in spruce. Plant Physiology 109, 319 326. , , (
- 1995c) Compartmentation and flux characteristics of nitrate in spruce. Planta 196, 674 682. , , (
- 1995d) Compartmentation and flux characteristics of ammonium in spruce. Planta 196, 691 698. , , (
- 1996) Kinetics of NH4+ influx in spruce. Plant Physiology 110, 773 779. , , (
- 1997) Conifer root discrimination against soil nitrate and the ecology of forest succession. Nature 385, 59 61. , , (
- 1992) Absorption and assimilation of nitrate and ammonium ions by Jack pine seedlings. Tree Physiology 11, 171 183. , , (
- 1969) Nitrification: importance to nutrient losses for a cutover forest ecosystem. Science 163, 1205 1206. , , (
- 1980) Allelopathic inhibition of nitrification and nitrifying bacteria in a ponderosa pine (Pinus ponderosa Dougl.) community. American Journal of Botany 67, 1423 1429. & (
- 1990) Lodgepole pine. In Silvics of North America. Volume 1. Conifers. Agriculture Handbook 654 (eds R.M. Burns & B.H. Honkala), pp. 302 315. USDA Forest Services, Washington DC. & (
- 1992) Evidence of increased nitrogen-15-ammonium assimilation in tomato plants with exogenous alpha ketoglutarate. Plant Science 85, 135 141. , , (
- 1991) Ammonium and nitrate uptake rates and rhizosphere pH in non-mycorrhizal roots of Norway spruce [Picea abies (L.) Karst.]. Trees 5, 14 21. , , (
- 1998) Induction of nitrate uptake and nitrate reductase activity in trembling aspen and lodgepole pine. Plant, Cell and Environment 21, 1039 1046. , , , , (
- 1999) A comparative study of fluxes and compartmentation of nitrate and ammonium in early-successional tree species. Plant, Cell and Environment 22, 821 830. , , , , (
- 1975) Ecology of lodgepole pine (Pinus contorta Douglas). In Proceedings of a Symposium on Management of Lodgepole Pine Ecosystems, pp. 25 46. Washington State University,> Pullman Publishers, WA. & (
- 1993) Nitrate uptake in maritime pine (Pinus pinaster) and the ectomycorrhizal fungus Hebeloma cylindrosporum: effect of ectomycorrhizal symbiosis. Canadian Journal of Botany 72, 189 197. , , , (
- 1997) Effects of clearcutting and alternative silvicultural systems on rates of decomposition and nitrogen mineralization in a coastal montane coniferous forest. Forest Ecology and Management 95, 253 260. (
- 1979) Modification of the soil environment by vegetation fires, with particular reference to nitrogen transformations: a review. Plant and Soil 51, 73 108. (
- 1999) AtAMT1 gene expression and NH4+ uptake in roots of Arabidopsis thaliana: evidence for regulation by root glutamine levels. Plant Journal 17, 563 568. , , , , (
- 1984) Effect of ectomycorrhizae and solution pH on 15N-ammonium uptake by coniferous seedlings. Canadian Journal of Botany 14, 885 892. , , (
- 1978) Nitrate utilization by the diatom Skeletonema costatum. I. Kinetics of nitrate uptake. Plant Physiology 62, 987 990. , , (
- 1990) Studies of the uptake of nitrate in barley. I. Kinetics of 13NO3− influx. Plant Physiology 93, 1426 1432. , , , (
- 1997) NO3− and CLO3− fluxes in the chl1-5 mutant of Arabidopsis thaliana – Does the CHL1-5 gene encode a low-affinity NO3− transporter? Plant Physiology 114, 137 144. & (
- 1994) Nitrate assimilation of raspberry and pin cherry in a recent clearcut. Canadian Journal of Botany 72, 1343 1348. , , , (
- 1993) The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72, 705 713. , , , (
- 1983) Productivity and nutrient cycling in taiga forest ecosystems. Canadian Journal of Forestry Research 13, 747 766. , , , , (
- 1982) A comparative analysis of potential nitrification and nitrate mobility in forest ecosystems. Ecological Monographs 52, 155 177. , , , , (
- 1982) NO3− and NH4+ levels in relation to site quality in Douglas-fir soil and litter. Northwest Science 56, 83 89. & (
- 1996) Landscape-scale variability of N mineralization in forest soils. Soil Biology and Biochemistry 28, 383 391. , , (
- 1993a) Ammonium uptake by rice roots. I. Fluxes and subcellular distribution of 13NH4+. Plant Physiology 103, 1249 1258. , , , (
- 1993b) Ammonium uptake by rice roots II. Kinetics of 13NH4+ across the plasmalemma. Plant Physiology 103, 1259 1267. , , , (
- 1996) Genetic identification of a gene involved in constitutive high-affinity nitrate transport in higher plants. Proceedings of the National Academy of Sciences of the United States of America 93, 9297 9301. & (