Enfin disponible en Europe, grâce à une étonnante formule Europe, 100% naturelle, vous pouvez maintenant dire stop à vos problèmes d’impuissance et à vos troubles de la virilité. Cette formule révolutionnaire agit comme un véritable achat cialis naturel. Ses résultats sont immédiats, sans aucun effet secondaire et vos érections sont durables, quelque soit votre âge. Même si vous avez plus de 70 ans !


J. Plant Physiol. 159. 567 – 584 (2002)  Urban & Fischer Verlaghttp://www.urbanfischer.de/journals/jpp toxicity in higher plants: a critical review
Division of Life Sciences, University of Toronto, 1265 Military Trail, Scarborough, Ontario M1C 1A4, Canada Received December 14, 2001 · Accepted February 22, 2002 Abstract
4 ) toxicity is an issue of global ecological and economic importance. In this review, toxicity, including the occurrence of NH4 in the biosphere, nutrition among wild and domesticated species, symptoms and pro- posed mechanisms underlying toxicity, and means by which it can be alleviated. Where possible,nitrate (NO – 3 ) nutrition is used as point of comparison. Particular emphasis is placed on issues of cellular pH, ionic balance, relationships with carbon biochemistry, and bioenergetics of primary NH + transport. Throughout, we attempt to identify areas that are controversial, and areas that are in needof further examination.
I. Introduction
universal biological phenomenon, as it has also been ob-served in many animal systems (Petit et al. 1990, Kosenko et al. 1991, 1995, Tremblay and Bradley 1992, Gardner et al.
4 ) is a paradoxical nutrient ion in that, al- though it is a major nitrogen (N) source whose oxidation state 1994), including humans, where it has been implicated in par- eliminates the need for its reduction in the plant cell (Salsac ticular in neurological disorders (Marcaida et al. 1992, Mira- et al. 1987), and although it is an intermediate in many meta- bet et al. 1997, Butterworth 1998, Haghighat et al. 2000, Mur- bolic reactions (Joy 1988), it can result in toxicity symptoms in thy et al. 2000), and also in insulin disorders (Sener and Ma- many, if not all, plants when cultured on NH + laisse 1980). Many research efforts have been directed to- clusive N source (Vines and Wedding 1960, Givan 1979, van ward unraveling the causes and mechanisms of NH4 toxicity der Eerden 1982, Fangmeier et al. 1994, Gerendas et al.
in plants, and while present knowledge is far from complete, a more comprehensive understanding of this phenomenon is least as early as 1882, when Charles Darwin described NH + beginning to emerge. This review will present key findings induced growth inhibition in Euphorbia peplus (cited in from this extensive body of work, with special focus on more Schenk and Wehrmann 1979). Sensitivity to NH + recent developments in the field, and on nitrate (NO ) nutri- tion as a point of comparison. In addition, we offer clarifica-tion of central issues that have been clouded by speculationin the past, and identify several critical areas for further re- * E-mail corresponding author: herbertk@utsc.utoronto.ca II. Ecology of NH +
forest expansion, rather than contraction, has been observed toxicity
(Köchy and Wilson 2001). It is clear that NH + creasing ecological importance, and deserves renewed at- in the biosphere
Nitrogen concentrations in soil solution can range over sev-eral orders of magnitude (Jackson and Caldwell 1993, Nes-doly and Van Rees 1998). In many natural and agricultural 2. Species response gradients
al. 1982, Blew and Parkinson 1993, Pearson and Stewart Ammonium toxicity may be universal, but the threshold at 1993, van Cleve et al. 1993, Bijlsma et al. 2000), and is almost which symptoms of toxicity become manifested differs widely always present to some extent in the majority of ecosystems.
among plant species. Although varying experimental condi- For instance, a survey of boreal and temperate forest ecosys- tions used in different studies make a rigid classification of tems shows forest-floor soil solution [NH + plants into tolerance groups difficult, some broad generaliza- tions are possible. Domesticated plants most sensitive to of 2 mmol/L (based on Vitousek et al. 1982, see also Bijlsma et toxicity (especially in terms of its effect on growth rates) include tomato (Claasen and Wilcox 1974, Magalhaes and often ranging from 2 to 20 mmol/L (Wolt 1994). The relative Huber 1989, Feng and Barker 1992 a – d), potato (Cao and Tibbits 1998), barley (Lewis et al. 1986, Britto et al. 2001 b), determined by a number of factors, of which the accumula- pea (Claasen and Wilcox 1974, Bligny et al. 1997), bean tion of organic matter, soil pH, soil temperature, the presence (Chaillou et al. 1986, Zhu et al. 2000), castor bean (Allen and of allelopathic chemicals, and soil oxygenation status are the Smith 1986, van Beusichem et al. 1988), mustard (Mehrer and most important (Rice and Pancholy 1972, Haynes and Goh Mohr 1989, Vollbrecht et al. 1989), sugar beet (Harada et al.
1978, Lodhi 1978, Dijk and Eck 1995). Typically, low pH, low 1968, Breteler 1973), strawberry (Claussen and Lenz 1999), temperature, accumulation of phenolic-based allelopathic citrus species (Dou et al. 1999), marigold (Jeong and Lee compounds, and poor oxygen supply inhibit many nitrifying 1992), and sage (Jeong and Lee 1992). NH + microorganisms (cf. Stark and Hart 1997), resulting in higher creasingly predominant N source in the soils of many natural rates of net ammonification than net nitrification (Vitousek et ecosystems as they go through the process of succession, al. 1982, Gosz and White 1986, Olff et al. 1993, Eviner and Chapin 1997). Soils exhibiting these conditions tend to be successional, including angiosperms such as poplars (Pear- son and Stewart 1993), and gymnosperms such as Douglas- cessional (Smith et al. 1968, Rice and Pancholy 1972, Lodhi fir (Krajina et al. 1973, Gijsman 1990 a, b, Oltshoorn et al. 1991, 1978, Klingensmith and van Cleve 1993).
de Visser and Keltjens 1993, Gorison et al. 1993, Min et al.
Human intervention in the nitrogen cycle is presently add- 2000), Scots pine (Vollbrecht et al. 1989, Elmlinger and Mohr ing more reduced nitrogen to the biosphere as the result of in- 1992), and western red cedar (Krajina et al. 1973). Wild her- tensive agricultural activities, which can lead to runoff from baceous plants particularly sensitive to NH + fields and deposition via the atmosphere (Vitousek 1994, Vi- Arnica montana and Cirsium dissectum (de Graaf et al. 1998), tousek et al. 1997, Bobbink 1998, Bobbink et al. 1998, Valiela eelgrass (van Katwijk et al. 1997, Hauxwell 2001), and broom- et al. 2000). Deposition of ammonium that has been trans- ported long distances can be significant, and N input has Plants that are the most highly adapted to NH + more than doubled since the 1950s in many areas, especially gen source include such domesticated species as rice (Ha- in Europe (Pearson and Stewart 1993, Falkengren-Grerup and rada et al. 1968, Sasakawa and Yamamoto 1978, Wang et al.
Lakkenborg-Kristensen 1994, Bobbink 1998, Bobbink et al.
1993 a, b), blueberry and cranberry (Greidanu et al. 1972, In- 1998, Goulding et al. 1998). Moreover, it has been estimated gestad 1973, Peterson et al. 1988, Troelstra et al. 1995, Claus- that human-related N fixation has actually exceeded that from sen and Lenz 1999), and onion and leek (Gerendas et al.
combined natural sources (Vitousek 1994). This additional N 1997, cf. Abbes et al. 1995 for onion). Wild plants in this cate- input has led to the N saturation of many natural ecosystems gory include the heather Calluna vulgaris (de Graaf et al.
and has affected species composition; in at least one case, a 1998), the sedge Carex (Lee and Stewart 1978, Falkengren- local species extinction was documented as a consequence Grerup 1995), many proteaceous plants (Smirnoff et al. 1984), some temperate angiosperm trees (e.g. oak, beech, horn- phenomena as important as large-scale forest decline have beam – Clough et al. 1989, Pearson and Stewart 1993, Truax et al. 1994, Rennenberg 1998, Rennenberg et al. 1998, acidification (van Breemen et al. 1982, Nihlgard 1985, van Bijlsma et al. 2000; eucalypts – Garnett and Smethurst 1999, Dam et al. 1986, van Dijk and Roelofs 1988, van Dijk et al.
Warren et al. 2000, Garnett et al. 2001) and late-successional 1989, 1990). By contrast, it is interesting to note that, when the conifers (spruce species – Marschner et al. 1991, Kronzucker bulk of the nitrogen deposited is as NO – et al. 1997; hemlock – Krajina et al. 1973, Smirnoff et al. 1984).
members are highly variable in their N-source adaptation (Ha- nounced can suffer toxicity symptoms, given a high enough rada et al. 1968, Gigon and Rorison 1972, Sasakawa and Ya- application of ammonium. For instance, rice plants can un- mamoto 1978, Findenegg 1987, Magalhaes and Huber 1989, dergo leaf oranging (Liao et al. 1994) and growth suppression Adriaanse and Human 1993, Cramer and Lewis 1993, Falken- (our unpublished results) under excessive NH + gren-Grerup and Lakkenborg-Kristensen 1994, Falkengren- particularly at low K+, and their growth potential is not fully re- Grerup 1995, Gerendas and Sattelmacher 1995). Moreover, alized unless nitrate is co-provided with ammonium (see sec- we hypothesize that a species’ adaptation to the succes- deposition has also been implicated in the sional stage of an ecosystem, and thus N-speciation domi- decline of some forests of red spruce, although this tree is nance in the native soil habitat (Vitousek et al. 1982), might be more important than family affiliation (see Kronzucker et al.
(Holldampf and Barker 1993). Substantial variations in NH + tolerance can also be seen amongst closely-related species(Monselise and Kost 1993), within species (Feng and Barker1992 a, Magalhaes et al. 1995, Schortemeyer et al. 1997), and III. Symptoms and proposed mechanisms
at different developmental stages (Vollbrecht et al. 1989).
Such differences, as well as differences in experimental sys-tems (for instance, NH + 1. Visual symptoms
of other nutrients, light intensity, temperature, and standards of comparison in terms of growth on other N sources and The reported symptoms of NH4 toxicity range widely, and choice of contrasting species), have led to some apparent contradictions in the literature (compare, for instance, van 0.1 to 0.5 mmol/L (Schenk and Wehrmann 1979, Peckol and den Driessche 1971 and Krajina et al. 1973, for conifers).
Rivers 1995, van Katwijk et al. 1997). Figure 1 shows, in the While there is no perfect resolution of this question, some sensitive species barley, two of the most dramatic of these studies have managed to compare a large number of species symptoms: the chlorosis of leaves, and the overall suppres- within a consistent framework. Smirnoff et al. (1984) used sion of growth (Kirkby and Mengel 1967, Kirkby 1968, Gigon constitutive levels and inducibility of nitrate reductase as an and Rorison 1972, Breteler 1973, Holldampf and Barker 1993, indicator of N-source adaptation, identifying certain families Gerendas et al. 1997). Yield depressions among sensitive as extreme nitrate specialists (Chenopodeaceae, Rosaceae, species can range from 15 to 60 % (Woolhouse and Hardwick Urticaceae) and ammonium specialists (Ericaceae, Pinaceae, 1966, Chaillou et al. 1986), and even death can result (Gigon Proteaceae). Falkengren-Grerup (1995) classified 23 plant and Rorison 1972, Magalhaes and Wilcox 1983 a, b, 1984 a, b, species into three tolerance groups, while in an approach Pearson and Stewart 1993, de Graaf et al. 1998). Other visual using 276 parameter combinations (‘‘species’’), Bijlsma et al.
symptoms often include a lowering of root : shoot ratios (Hay- (2000) identified five response categories based upon spe- nes and Goh 1978, Atkinson 1985, Blacquière et al. 1987, Box- man et al. 1991, Wang and Below 1996, Bauer and Berntson other studies, it emerges that certain plant families tend to be 1999), although the reverse effect has been observed for some species (Gigon and Rorison 1972, Troelstra et al. 1985).
piled tentatively, albeit not exhaustively, in Table 1. Notably A decrease in the fine : coarse root ratio is also part of thesyndrome (Haynes and Goh 1978, Boxman et al. 1991), butthis can be accompanied by stimulation in root branching(Ganmore-Neumann and Kafkafi 1983). Symptoms not so rea- Table 1. Tentative assignment of plant families according to their ten-
dily visible, but equally important, can include a decline in dency towards tolerance or sensitivity to NH + mycorrhizal associations (Boxman et al. 1991, Lambert and Weidensaul 1991, van Breemen and van Dijk 1998, van der Eerden 1998, Boukcim et al. 2001, Hawkins and George2001). Finally, seed germination and seedling establishment Rosenau 1966, Megie et al. 1967, Barker et al. 1970, West- wood and Foy 1999), a feature of high ecological signifi- 2. Ionic balance and biochemical responses
Chemical changes in the plant induced by NH + clude the well-documented total tissue depression, com- Figure 1. a, 8-day-old seedlings of barley (Hor-
deum vulgare L. cv. «Klondike»), hydroponically cultured in ammonium (two pairs at left) or in nitrate (two pairs at right). Nitrogen concentrations in solu- tion were as indicated. [K+] in all solutions was 0.023 mmol/L. b, Barley seedlings cultured as in
Figure 1, but only with ammonium, at a concentra- tion of 10 mmol/L (left, held in researcher’s right hand) or 0.1 mmol/L (right, held in researcher’s left growth suppression in roots, and, especially, shoots at high ammonium concentrations.
3 -fed plants, of essential cations such as potas- grown on NO3 (Kirkby 1968, Haynes and Goh 1978, Allen sium, calcium, and magnesium (Kirkby 1968, Salsac et al.
and Smith 1986, Allen and Raven 1987, van Beusichem et al.
1987, van Beusichem et al. 1988, Boxman et al. 1991, Holl- 1988, Goodchild and Givan 1990, Leport et al. 1996), while dampf and Barker 1993, Troelstra et al. 1995, Gloser and Glo- amino acid concentrations increase (Margolis 1960, Harada ser 2000). This decline in cations other than NH + et al. 1968, Kirkby 1968, Magalhaes and Wilcox 1984 a, b, panied by an increase in tissue levels of inorganic anions Rosnitschek-Schimmel 1985, Chaillou et al. 1986, 1991, Allen such as chloride, sulfate and phosphate (Kirkby 1968, Cox and Raven 1987, Blacquière et al. 1988, Majerowicz et al.
and Reisenauer 1973, van Beusichem et al. 1988). In addition, 2000). It is important to point out that almost no information is tissue levels of non-amino dicarboxylic acids, such as malic available on the intracellular localization of these changes in ion concentration (see Speer et al. 1994, Speer and Kaiser 1994), and much more work is necessary to resolve whether 4 -rich soils are typically low in pH (Vitousek et what is concluded from total tissue analyses also pertains to, in particular, the cytosolic compartment. Even large changes Intracellular pH disturbance has also been proposed to be in total tissue contents, given the enormous capacity of the vacuole to sequester metabolites, including malate, and also McQueen and Bailey 1991), but this possibility has been waste products (Martinoia et al. 1981, Martin 1987, Kaiser et largely dismissed by studies using NMR and fluorescent dyes al. 1989, Siebke et al. 1992, Heber et al. 1994, Yin et al.
(Bligny et al. 1997, Kosegarten et al. 1997, Wilson et al. 1998, 1996 a, Dietz et al. 1998, Oja et al. 1999, Blumwald 2000, And- Gerendas and Ratcliffe 2000). However, because cellular ni- reev 2001), may not have direct bearing on growth, fitness, trogen-pH relations in plants have long been clouded by in- and mortality. Until these questions are resolved, a causative correct and piecemeal speculation, this subject deserves a more detailed treatment. It has become a textbook argument ficult, if not impossible, to determine.
(Salisbury and Ross 1992, Marschner 1995) that cytosolic pH Although the uptake of many inorganic cations is reduced must increase with nitrate feeding and decrease with ammo- nutrition, the uptake of NH4 itself is so high that nium feeding, unless buffered by a cellular pH-stat mecha- 4 -fed plants generally take up an excess of cations rela- nism. In support of this argument, the two-step reduction of tive to anions (Kirkby 1968, Clark 1982, van Beusichem et al.
to NH4 (via nitrate and nitrite reductases) is usually cited, as it involves a transfer of 10 protons and 8 electrons.
external medium (Mevius and Engel 1931, Runge 1983, Fin- Because of this imbalance, nitrate reduction is a proton-con- denegg 1987, Goodchild and Givan 1990, Schubert and Yan suming process overall. Starting with water, the ultimate 1997), suggesting that proton efflux from the plant is one source of both H+ and e– (in the Hill reaction of photosynthe- means of compensating for the charge imbalance. By con- sis – note that this applies to roots as well as shoots, in the 3 -fed plants cause a net alkalinization of the me- long run), the two partial reactions for this redox transfer, and dium (Dijkshoorn 1962, Runge 1983, Goodchild and Givan 1990, Schubert and Yan 1997), probably in response to the excess uptake, in this case, of anions relative to cations (how- ever, for both N sources, differences in proton uptake and ex- trusion along the longitudinal root axis, and between the rhi- zoplane and bulk solution, demonstrate that the actual situta- tion is considerably more complicated – see Henriksen et al.
NH4 assimilation, on the other hand, involves the release of 1992, Taylor and Bloom 1998). Indeed, van Beusichem et al.
protons (Kirkby 1968, Raven and Smith 1976, Smith and (1988) showed that the cumulative number of protons ex- Raven 1979), although this release results neither from NH4 creted by Ricinus communis plants grown on NH + days closely approximated the excess cation uptake, while mary assimilatory reaction sequence catalyzed by GS (4) and the ‘‘hydroxyl’’ ions excreted (not distinguishable from pro- GOGAT (5) themselves, as can be seen when the partial imated the excess anion uptake. The ammonium response, glutamate + ATP → glutamine + ADP + Pi and the resulting acidification of the rhizosphere under both 2-oxoglutarate + glutamine + H+ + 2e– → 2 glutamate field and laboratory conditions, is often considered to be onefundamental cause of NH + ATP + 2e– → glutamate + ADP + Pi from toxicity symptoms has often been observed when While proton-neutral, however, this reaction sequence consu- growth solutions are pH-buffered (Gigon and Rorison 1972, mes two electrons (in reaction 5), which leads, again, to an Findenegg 1987, Vollbrecht and Kasemir 1992, Dijk and Eck imbalance between proton and electron consumption. Inter- 1995, Dijk and Grootjans 1998). However, in some cases the estingly, however, in this case the proton/electron imbalance relief is only partial (Gigon and Rorison 1972, Breteler 1973), is the mirror image of that noted for reactions 1– 3 in the and in many other instances is absent (Kirkby 1968, Cox and reduction of NO – to NH +. Therefore, because NO – reduc- Reisenauer 1973, Pill and Lambeth 1977, Blacquière et al.
tion is almost always coupled to NH + assimilation, NO – 1987, 1988, van Beusichem et al. 1988), so it is more likely assimilation as outlined above is, overall, a pH-neutral pro- that plants that benefit from pH-buffering are not suffering cess. This important conclusion is not usually drawn (cf.
4 -toxicity per se, but rather from externally acidic Gerendas and Ratcliffe 2000); nor is it usually considered that conditions as a superimposed, but essentially separate, the production of each dicarboxylic carbon skeleton (2-oxo- stress (see Goodchild and Givan 1990). Nevertheless, it glutarate) for N assimilation involves the generation of two protons, as summarized in the following equation: ance, and therefore it is no coincidence that most, if not all, ofthe NH + 4 -tolerant plants listed above are also acid-tolerant (see, for instance, Yan et al. 1992). This is not surprising, When C metabolism is included in the analysis, then, equa- et al. 1992, Heber et al. 1994, Yin et al. 1996 a, Dietz et al.
1998, Oja et al. 1999), and its significance in the context of assimilation generates 2 H+, and thus both NH4 toxicity should not be discounted. Moreover, the plas- processes impose a net acid load on the plant cell. Further- ma-membrane H+ ATPase is well known to respond to both more, it is crucial to this issue, but rarely considered, that in inorganic N sources (Troelstra et al. 1985, Siddiqi and Glass addition to purely biosynthetic processes, the primary trans- 1993, Yamashita et al. 1995, Venegoni et al. 1997).
across the plasma membrane into the plant cell In light of these considerations, changes in the amino acid is mechanistically tied to a symport of 2H+ (McClure et al.
or organic acid profiles of plants under NH + 1990, Glass et al. 1992, Siddiqi and Glass 1993, Meharg and Blatt 1995, Mistrik and Ullrich 1996, Glass and Crawford 1998, Givan 1990) and even observed under conditions where NH4 does not suppress growth (van Beusichem et al. 1988, occur by an electrogenic uniport (Raven and Farquhar 1981, Chaillou et al. 1991), are unlikely to be directly related to the Smith 1982, Ullrich et al. 1984, Wang et al. 1994, Howitt and manifestation of the toxicity syndrome.
Udvardi 2000, von Wirén et al. 2000, Cerezo et al. 2001).
When the above primary transport and assimilation functions 3. Energetics and primary NH + acquisition
are summed, it emerges that the plant cell experiences an intracellular H+ appearance of 4 moles of H+ per mole of N Clearly, an understanding of ammonium toxicity in plants is taken up and assimilated, regardless of whether N is supplied contingent upon an understanding of the mechanisms of pri- or NO3 . However, the analysis is further compli- mary entry of NH4 into plant cells. An ongoing debate plagu- cated by the intracellular buildup of NO – ing the discussion has been whether NH4 or its conjugate been transported but not metabolized; these pools magnify base, NH3 (ammonia), is the chemical species entering the the contribution of proton fluxes associated with primary NO – plant from the external medium via the plasma membrane.
transport, but have no comparable effect with NH + There is no doubt that, under conditions of high external pH, Another complication is the larger buildup of organic trations large enough to facilitate its entry via passive diffu- nutrition (see above), although it has been suggested that, sion (Yin et al. 1996 b, Kosegarten et al. 1997, Wilson et al.
mechanistically, malate accumulation might respond to 1998, Gerendas and Ratcliffe 2000, Plieth et al. 2000), and external pH rather than N source (Goodchild and Givan the permeability coefficient for NH3 does appear to suggest 1990). Malate production, however, further increases the that NH3 can readily penetrate some biological membranes 3 -associated H + load, rather than counteracting a pre- (Kleiner 1981, Ritchie and Gibson 1987). This point of view ap- sumed OH–-load, as is commonly invoked in discussions of pears additionally supported by the observation that a tran- the role of malate as a biochemical ‘‘pH-stat’’. We propose an sient cytosolic alkalinization occurs with exposure of plant alternative explanation, that increased net malate synthesis cells to ammonia/ammonium (Kosegarten et al. 1997, Wilson provision is driven by the greater need, relative et al. 1998, Gerendas and Ratcliffe 2000; see also Mirabet et provision, for reduction equivalents in the root, rather al. 1997 and Minelli et al. 2000 for similar analyses in animal than for pH balance. Interestingly, however, the synthesis of tissues). We favor the alternative hypothesis that under malate via PEP carboxylase, though not its accumulation, is normal external pH conditions, the plasma membrane H+- ATPase immediately responds to NH4 exposure (see above).
mer and Lewis 1993, Leport et al. 1996), although this is not Furthermore, it is important to note that soils only rarely exhibit always the case (Goodchild and Givan 1990). It is likely that the increased PEP carboxylase activity serves an anapleuro- quently so low that NH3 is present in such small amounts that tic function in the provision of carbon skeletons for ammonium no appreciable flux into the plant could possibly be sustained (it should be noted that in marine ecosystems, with a pH > 8, is often reduced in the shoot illustrates NH3 might be significant). Moreover, biological membranes in that the resulting cellular acid burden, in the absence of the situ are undoubtedly more complex than simple lipid bilayer opportunity to offload protons to an external medium, poses solubility and permeability models suggest. In the case of no problem for the shoot in normally-functioning plant tissues, 4 , this is dramatically illustrated in the lack of uncoupling contrary to what is often stated (Kirkby 1968, Raven and of photophosphorylation in highly intact chloroplasts (Heber Smith 1976, Salsac et al. 1987). The unloading of the proton 1984, Kendall et al. 1986, Blackwell et al. 1988, Gerendas et burden imposed upon the cytosol by both nitrogen forms may al.1997, Kandlbinder et al. 1997, Zhu et al. 2000; also see be- be alternatively explained by biophysical pH stat mecha- low). Indeed, it is fascinating to speculate what mechanisms nisms involving the pumping of H+ across the tonoplast and plant membranes (especially the tonoplast) use to maintain plasma membranes. The potency and rapidity of pH rectifica- sequestration, against often sizable gradients, of highly mo- tion effected by the tonoplast H+ ATPase is well established in bile, lipophilic materials whose tight compartmentation is crit- the context of many other physiological phenomena (Siebke ical to cell function. Incidentally, Raven and Farquhar (1981), often incorrectly cited to support the idea that NH3 is the prin- nity transport system’’ (LATS) the activity of which, surpri- cipal membrane-permeating species, also conclude forcibly singly, is apparently not downregulated (unlike the high-affi- 4 , and not NH3, is the membrane-permeating spe- nity transport system), but rather produces higher fluxes with cies. A second often-cited paper in this context (Kleiner 1981) increased nitrogen status of the plant (Wang et al. 1993 b, Min in fact provides little evidence in favour of NH3 penetration, et al. 1999, Rawat et al. 1999, Cerezo et al. 2001). The rea- presenting instead an equivocal case for fluxes across higher sons for this lack of regulation are yet to be resolved, but a plant membranes; this uncertainty was due to the lack of ex- plausible explanation involves the likelihood that LATS trans- perimental evidence available at the time. This lack has port is mediated by constitutively-expressed channel-type clearly been superseded by more recent work in the field; the transporters possibly identical or very similar to those whose preponderance of recent experimental evidence supports the normal function is potassium uptake into the plant (Sokolik is the principal chemical species traversing and Yurin 1986, Vale et al. 1988, Schachtmann et al. 1992, plant plasma membranes under most conditions (Walker et al.
White 1996, Nielsen and Schjoerring 1998; see also Mironova 1979 a, b, Smith 1982, Ullrich et al. 1984, Schlee and Komor 1996, Hagen et al. 2000 for similar instances in animal sys- 1986, Wang et al. 1993 b, 1994, Karasawa et al. 1994, Ninne- tems), or belonging to a family of transporters identified as man et al. 1994, Ryan and Walker 1994, Herrmann and Felle ‘‘non-selective cation channels’’ (Davenport and Tester 2000, 1995, Kronzucker et al. 1995 a, 1996, Nielsen and Schjoerring Kronzucker at al. 2001). Given that K+ tissue concentrations 1998, von Wirén et al. 2000, Britto et al. 2001a, b, Cerezo et al.
are reduced significantly under high NH + 2001), and that cytosolic accumulation of NH + 1968), it may not be surprising that potassium channels are by at least three different techniques (NMR, compartmental overexpressed in response to what essentially amounts to a analysis, and micro-electrodes; see Lee and Ratcliffe 1991, K+ starvation condition; the unfortunate side-effect is that it Wang et al. 1993 a, Wells and Miller 2000, respectively, for allows even more uncontrolled influx of NH + examples of each), is substantial enough to indicate that loss ing with, and inhibiting, potassium suppression) into the plant.
via simple diffusion of NH3 is not significantly high.
Perhaps for this reason, plants that are susceptible to NH4 The low NH3-permeability of the plasma membrane is fur- toxicity display extraordinarily high plasma membrane fluxes ther substantiated by the observation that dramatic increases in both directions (Feng et al. 1994, Nielsen and in the inwardly-directed NH3 gradient are accompanied by Schjoerring 1998, Rawat et al. 1999, Min et al. 1999, Britto et al.
2001b, Cerezo et al. 2001). Given that such fluxes can be well direction (i.e. efflux to the external medium); for example, 4 -assimilation capacity of the plant, either Kronzucker et al. (1995 a) showed a 8-fold reduction in the gradient accompanied by a 105-fold increase in efflux.
Kaiser 1994, Wieneke and Roeb 1997, Husted et al. 2000), Clearly, this runs against the idea that NH and/or increased efflux of NH4 from the plant must ensue.
significant role in trans-plasma-membrane N fluxes under Taking into consideration plasma membrane electrical po- normal conditions. There has been some debate about the medium and in the cytosol, a thermodynamic analysis reveals that it lies in the low to medium millimolar range (see Kron- zucker et al. 1995 a, Britto et al. 2001 a, and references transport into the plant is a passive process, therein). This agreement is found in spite of uncertainties relating to cellular heterogeneity (Henriksen et al. 1992, Taylor must be energetically active. Indeed, passive efflux transport and Bloom 1998) which affect all these methods, and which points to the need for system verification (Kronzucker et al.
much higher than measured by any technique to date (e.g. at 1995 b). One exception to the agreement in the above esti- an external concentration of 10 mmol/L, a realistic membrane mates consists of a short communication which did not report potential of –120 mV would require a minimum, but unlikely, measurements per se, but rather used an indirect cytosolic concentration of 1mol/L in order for passive efflux to method of analyzing 31P- and 13C-NMR signals (Roberts and occur). Although there is a debate about cytosolic concentra- tions of NH4 (which need to be distinguished from vacuolar range (2 – 438 µmol/L). A more recent study found cytosolic concentrations), and therefore about the magnitude of concentrations in barley and rice plants to be several the gradient against which such active efflux transport must hundred millimolar, at the exceptionally high external concen- work, all studies with the exception of one (Roberts and Pang 1992) have shown that cytosolic [NH4 ] can be in the millimo- values, it should be noted, were found under conditions lar range (see Britto et al. 2001 a). Along with detection of substantial (millimolar) NH4 in the xylem stream (van Beusi- high, were nevertheless at, or below, concentrations pre- chem et al. 1988, Schjoerring et al. 2002), studies of plant- dicted by the Nernst equation (see below).
Schjoerring et al. 2000), and the inescapability of large uptake into the plant is a ‘‘low-affi- endogenous cellular NH4 production associated with protein turnover under virtually all growth conditions, including excessive root respiration, that does not contribute to growth growth on nitrate (Blackwell et al. 1987, Jackson et al. 1993, or maintenance (but rather to wasteful processes such as Feng et al. 1998), such cellular measurements belie the wide- ly-held notion that free ammonium does not accumulate in plant tissues (Kafkafi and Ganmore-Neumann 1997, Tobin and It is noteworthy that ammonium toxicity is frequently more Yamaya 2001 – but cf. Husted et al. 2000). Using measured pronounced at high light intensity (Goyal et al. 1982 a, b, Ma- concentrations and membrane potentials in galhaes and Wilcox 1983 a, 1984 a, Zornoza et al. 1987, Zhu et barley, Kronzucker et al. (2001) showed that the active efflux al. 2000, Bendixen et al. 2001). At first glance, this observa- process is highly inefficient, which helps explain the high tion may appear to contradict the idea that increased carbon respiratory rates commonly, but not always (de Visser and Lambers 1983, Cruz et al. 1993), measured with NH + pectation might be that increased photosynthetic activity at tion in many plants (Haynes and Goh 1978, Matsumoto and higher light intensities could supply more carbon to the root.
Tamura 1981, Barneix et al. 1984, Blacquière and de Visser Indeed, it may be that the light optimum under NH + 1984, Cramer and Lewis 1993, Rigano et al. 1996; see also 3 ) nutrition is shifted to a higher intensity, to compen- Kosenko et al. 1991, Martinelle and Haggstrom 1993, Hagen sate for increased carbon utilization for respiration and amino et al. 2000, Hagighat et al. 2000 a, b for similar examples in acid production (a subject worthy of further study; see Givan 1979 and references therein; also see below for a discussion the glutamine synthetase inhibitor methionine sulfoximine of root energy demands associated with NH + (Britto et al. 2001 b). Consistent with this respiratory increase ever, as in the case of plants suffering toxicity in a medium is a decline in cellular ATP levels (Kosenko et al. 1991, Rigano that is not pH-buffered, negative high-light effects are most et al. 1996, Hagen et al. 2000, Hagighat et al. 2000 a, b). How- likely to be an instance of the consequences of superim- ever, this is not a necessary outcome (e.g. Lang and Kaiser posed stresses. What is important here is that, in addition to 1994), as increased energy utilization can occur in plant cells the events occurring at the root level, plants susceptible to without concomitant declines in ATP or ATP/ADP ratios (Yan et toxicity typically are afflicted by reduced rates of net photosynthesis (Takács and Técsi 1992, Claussen and Lenz Based on the root respiratory increase with NH + 1999, cf. Raab and Terry 1994). More specifically, the decline and the decrease in root : shoot ratio, some workers have sug- in CO2 fixation (Puritch and Barker 1967, Ikeda and Yamada gested that an excessively high carbon sink strength in root 1981, Mehrer and Mohr 1989) has been attributed to a decline in rubisco and NADP-dependent glyceraldehyde-3-phos- meyer et al. 1997, see Kronzucker et al. 1998 for additional phate dehydrogenase (Mehrer and Mohr 1989), impaired references), is in part responsible for ammonium toxicity.
NADP reduction (Vernon and Zang 1960) or changes in Indeed, sugar and starch content of plants generally chloroplast ultrastructure (Takács and Técsi 1992, Dou et al.
decrease with ammonium treatment (Kirkby 1968, Matsumoto 1999). It is important to reiterate here that uncoupling of plas- et al. 1971, Breteler 1973, Lindt and Feller 1987, Lewis et al.
tidic energy gradients by NH3, sometimes cited as the funda- 1989, Magalhaes and Huber 1989, Mehrer and Mohr 1989, Kubin and Melzer 1996), although some exceptions have experiments with isolated chloroplasts (Krogmann et al. 1959, been observed (Blacquière et al. 1987, Lang and Kaiser Puritch and Barker 1967, Crofts 1967, Izawa and Good 1972, 1994). Contrarily, it has been suggested that tolerance to Krause et al. 1982) has no basis in intact or suitably isolated might be directly related to the capacity of the root glu- systems (Heber 1984, Kendall et al. 1986, Blackwell et al.
tamine synthetase/glutamate synthase (GS-GOGAT) enzyme 1987, 1988, Gerendas et al. 1997, Kandlbinder et al. 1997, Zhu et al. 2000, Bendixen et al. 2001, our unpublished results).
in the plant is itself toxic (Givan 1979, Magalhaes and In recent studies Zhu et al. (2000) and Bendixen et al.
Huber 1989, Monselise and Kost 1993, Fangmeier et al. 1994, (2001) examined the possibility of direct effects of NH + Tobin and Yamaya 2001). However, it must be pointed out that the photosystems of Phaseolus vulgaris. Somewhat surpri- singly, chlorophyll fluorescence analysis revealed no signifi- very high GS capacity (Magalhaes and Huber 1989), can cant differences in energy quenching (qE) or photoinhibition accumulate substantial amounts of free NH + (as manifest in Fv/FM ratios) between NO3 - and NH4 -grown and vacuole, even at modest external concentrations (Wang plants (cf. Vanselow 1993, who did observe such differences et al. 1993 a, Kronzucker et al. 1999 a, Britto et al. 2001 b).
in Dunaliella). However, significant depression in the ability of These findings cast doubt on both the root-carbon-sink hypo- 4 -grown plants to engage the violaxanthin-zeaxanthin cy- thesis, and the metabolic-detoxification hypothesis. Clearly, cle for photoprotection was observed (Bendixen et al. 2001), per se in the plant cell is not necessarily toxic, and car- an effect due to the decline in ascorbate consistent with lower reduced carbon availability (see above), and with increased limiting only when capacity of the shoot to deliver photoassi- uronic acid levels (Kirkby 1968). Despite lack of fluorescence milate via the phloem is impaired, and/or under conditions of data to support changes in electron flow between PSII and PSI, the observation by Zhu et al. (2000) that NH + bara et al. 1998). Moreover, ammonium feeding, in at least the reduction of molecular oxygen in the Mehler reaction indi- one case, has been shown to lead to a suppression of root cates that such an impairment might have nevertheless auxin content (Kudoyarova et al. 1997).
occurred. This possibility is further supported by other stud- In a series of studies with tomato, A. V. Barker and co- ies in which an increased export of redox equivalents under workers investigated the role of ethylene in the development 3 -feeding indicated a more efficient photosynthetic elec- of the NH4 toxicity syndrome (Feng and Barker 1992 a – d, tron flow (Backhausen et al. 1994, Krömer 1995, Noctor and Barker and Corey 1991, Barker 1999 a, b). Ethylene production Foyer 1998). Zhu et al. (2000) observed increased lipid per- is a more or less universal response to physiological stresses oxidation, an important consequence of enhanced Mehler in plants, to the extent that it is often used as a plant stress in- dicator (Barker 1999 a, b), but in these studies a more specific also appears to be favored by magnesium and potassium role in ammonium toxicity was implicated. Ethylene evolution deficiencies (Cakmak and Marschner 1992, Polle et al. 1992, from leaf tissue was shown to increase linearly with tissue Cakmak 1994), conditions which are associated with NH + ammonium content once a threshold value of 0.2 mg NH4 -N nutrition (see section III-2 above). It must be pointed out that g–1 (fresh wt.) was reached (Barker 1999 a), regardless of the alleviation of overreduced photosystems via the Mehler external pH. Importantly, it was further shown that ammonium reaction is insufficient to lend full protection against photo- accumulation preceded ethylene evolution (Barker 1999 b).
inactivation (Wiese et al. 1998) and, therefore, alternative Ammonium accumulation was high enough under urea feed- means of photoprotection, especially in the absence of the ing to trigger ethylene evolution, while nitrate nutrition zeaxanthin component, must be operating to maintain energy increased ammonium accumulation only slightly, and did not quenching, at least in the short term. In the absence of such trigger ethylene evolution (Feng and Barker 1992 c). The mechanisms, photorespiration is a possible means of alleviat- application of amino-oxyacetic acid (although problematic as ing light stress (Heber et al. 1996), and indeed enhanced it is also an aminotransferase inhibitor – Oaks 1994) and silver photorespiratory rates have been observed with NH + thiosulfate, inhibitors of ethylene synthesis and action, amelio- tion (Zhu et al. 2000). In the long term, a connection between rated symptoms of ammonium toxicity (Barker and Corey – induced growth suppression at high light, and 1991, Feng and Barker 1992 b, d). Clearly, the role of ethylene enhanced damage to the photosynthetic centers themselves, toxicity deserves further attention.
IV. Alleviation of NH + toxicity
4. Hormonal balance
Ammonium-induced changes in growth and development are undoubtedly linked to alterations in hormonal balance, but viated in certain cases by buffering external pH such that the there is much contradictory evidence in the literature regard- acidification of the rhizosphere associated with ammonium ing this, and it is important to point out here that, other than in uptake is counteracted. Maintaining neutral to slightly alkaline the case of ethylene (see below), no explanations of NH + pH can also prevent the precipitous fall in cellular malate typi- toxicity have been forthcoming from such studies. In the case cally associated with provision of ammonium (Goodchild and of a recent review (Gerendas et al. 1997), a string of argu- Givan 1990). In addition, optimization of light regimes so as to ments, mostly speculative, were presented to link increased avoid high light effects (section III.3) is more critical with auxin transport to the roots with increased cytokinin produc- ammonium-grown plants than with plants grown with nitrate or tion in roots. It was suggested that more prolific root branch- organic N. It is also very important to maintain high levels, in ing results from the increased strength of the root tissue as a nutrient solutions, of cations known to be depressed in plant tissue when NH4 is used as a sole N source (section III.2). In auxin delivery to the root (Ziegler 1975, Torrey 1976, Sattel- particular, the supply levels of K+ have been shown to alle- macher and Thoms 1995). The increased number of root tips, viate toxicity both in solution culture experiments and in the which has been often observed, could then lead to increased field (Barker et al. 1967, Lips et al. 1990, Zhang et al. 1990, production of cytokinins in ammonium-grown plants, and in Feng and Barker 1992 a, Barker 1995). At present, it is not turn, could shift root : shoot ratios in favor of increased shoot known whether the normally homeostatically-controlled cyto- growth (Gerendas et al. 1997). However, there is little evi- solic concentrations of potassium, or only the vacuolar pools dence to support the notion of increased cytokinin production (Walker et al. 1996, and references therein), are affected by provision conditions. In fact, the highest levels of high NH4 supply. Our preliminary results (unpublished) sug- gest that in NH4 -sensitive species such cytosolic displace- alone (Singh et al. 1992, Smiciklas and Below 1992, Wang ment does indeed occur. In the case of calcium, it is interest- and Below 1996, Chen et al. 1998, Walch-Liu et al. 2000), with ing to speculate whether the much-depressed vacuolar (and possibly other intracellular) pools of this universal signaling cytokinin synthesis (Samuelson and Larsson 1993, Sakaki- dampening of the amplitude of Ca2+-spike responses to vari- proportion of the xylem N flux is unmetabolized NO – ous stimuli, as a result of diminished gradients.
the remainder consists mostly of products of ammonium as- One of the most fascinating aspects of NH + similation (Kronzucker et al. 1999 a). Enhanced root assimila- that, while toxicity is observed in many species when NH + tion in the presence of nitrate is supported by several studies provided alone, it can be alleviated by co-provision of nitrate (Goyal et al. 1982 b, Ota and Yamamoto 1989), and can be (Goyal et al. 1982 a, b, Below and Gentry 1987, Deignan and mechanistically explained by the induction by nitrate of the Lewis 1988, Hecht and Mohr 1990, Feng and Barker 1992 a, c, GS-GOGAT pathway specifically localized in the proplastids Adriaanse and Human 1993, Cruz et al. 1993, Gill and Reise- of roots (Redinbaugh and Campbell 1993), opening up a nauer 1993, Schortemeyer et al. 1997). Furthermore, co-provi- pathway not available to ammonium assimilation in the ab- sion induces a synergistic growth response that can surpass sence of nitrate. In addition to these dramatic effects, the maximal growth rates on either N-source alone by as much as presence of nitrate may help to alleviate NH + 40 to 70 % in solution culture (Weissman 1964, Cox and Rei- its ability to be reduced in the shoot, moderating the differen- senauer 1973, Heberer and Below 1989), though by some- tial carbon drain between roots and shoots, and improving what less in soil (Hagin et al. 1990, Gill and Reisenauer 1993).
electron flow between photosytems I and II (section III.3).
Interestingly, the synergistic response is observed even in Obviously, the synergistic response to co-provision of NH + species such as conifers, where nitrate uptake is very small 3 , in addition to providing a promising avenue for (van den Driessche 1971, van den Driessche and Dangerfield agronomic improvements, has also yielded insights into the 1978, Kronzucker et al. 1997). However, in a few cases, such mechanisms of ammonium toxicity, and is an area in need of as some Ericaceous plants, a synergistic response is absent, and some plants even experience growth inhibition on nitrate(Dijk and Eck 1995). Several proposals have been put forth V. Conclusions
which attempt to explain the phenomenon of nitrate-ammo-nium synergism. Pivotal to many of these is the possible role The suppression of growth and yield in NH + of nitrate as a signal that stimulates (or optimizes) a multitude cies can be severe, and for this reason NH + of biochemical responses (Stitt and Krapp 1999, Tischner major importance in agricultural and ecological settings. Cer- 2000). One possibility is that cytokinin synthesis is maximized tain plant species, and even families, are particularly sensi- and NH4 are provided together (Smiciklas and Below 1992, Chen et al. 1998; also see section III.4). Another ever, the symptoms of, mechanisms underlying, and means is that the rhizospheric alkalanization effect of nitrate uptake of alleviating, ammonium toxicity, are diverse. Explanations of by plants may help to limit the acidification associated with nutrition (Imsande 1986, Marschner 1995, also see sec- pered by numerous misconceptions regarding this subject, tion III.2). However, this effect can at best be partial or require and many often-cited possibilities have more recently been : NH4 ratios in the nutrient solution, because shown to be at best insufficient, partial explanations, or even uptake is significantly inhibited, often by as much as incorrect. These latter include the uncoupling of photophos- 50 %, by ammonium (Kronzucker et al. 1999 a, b, and refer- in planta; the effects of external pH de- lated by nitrate (Rideout et al. 1994, Saravitz et al. 1994, Kron- pH-stat mechanisms in cells accounting for differences in the zucker et al. 1999 a). Given that nitrogen efflux is also sub- internal H+ balance associated with differences in NH + stantially lowered with co-provision, the net result of the metabolism; the accumulation per se of free NH4 in plant’s use of the two separate N sources together is that total plant tissues (including, specifically, the cytosol); and the N uptake can be significantly (up to 75 %) higher than with the higher root carbon allocation to amino acid synthesis under same N concentration presented in the form of either N nutrition. More plausible explanations include the in- source alone (Kronzucker et al. 1999 a).
volvement of ethlylene synthesis and action as a key plant re- An interesting aspect of this analysis is that, at least in rice, stress; the role of NH4 membrane flux pro- cesses, particularly the energy-demanding active efflux of cy- 4 ; photosynthetic effects, particularly with respect cells (Kronzucker et al. 1999 a), attenuating the requirement to photoprotection; and displacement of essential cation con- for charge balancing of either N source, at least in the cyto- centrations from homeostatic set points in subcellular com- sol. Possibly the most important synergistic response of co- partments. These possibilities deserve more research atten- and NH4 lies in the enhanced transport of tion. In addition, much could be learned about ammonium nitrogen to the shoot. This is an issue of high agronomic im- toxicity mechanisms by examining its alleviation through vari- portance, since nitrogen stored in shoot tissue can be remo- ous means, particularly through the co-presence of nitrate.
bilized during the critical period of grain-filling and fruit devel-opment, when N-delivery via roots can become impaired due Acknowledgements. This work was supported by the Natural Scien-
to the onset of senescence (Mae et al. 1985). A significant ces and Engineering Research Council of Canada (NSERC).
Blackwell RD, Murray AJS, Lea PJ (1987) Inhibition of photosynthesis in barley with decreased levels of chloroplastic glutamine synthet- Abbes C, Parent LE, Karam A, Isfan D (1995) Onion response to am- Blackwell RD, Murray AJS, Lea PJ, Joy KW (1988) Photorespiratory moniated peat and ammonium sulfate in relation to ammonium tox- amino donors, sucrose synthesis and the induction of CO in barley deficient in glutamine synthetase and/or glutamate syn- Adriaanse FG, Human JJ (1993) Effect of time of application and ni- trate: ammonium ratio on maize grain yield, grain nitrogen concen- Blacquière T, De Visser R (1984) Capacity of cytochrome and altern- tration and soil mineral nitrogen concentration in a semi-arid re- ative path in coupled and uncoupled root respiration of Pisum and Plantago. Physiol Plant 62: 427– 432 Allen S, Raven JA (1987) Intracellular pH regulation in Ricinus commu- Blacquière T, Hofstra R, Stulen I (1987) Ammonium and nitrate nutrition nis grown with ammonium or nitrate as N source: The role of long- in Plantago lanceolata and Plantago major L. ssp. major. I. Aspects distance transport. J Exp Bot 38: 580 – 596 of growth, chemical composition and root respiration. Plant Soil Allen S, Smith JAC (1986) Ammonium nutrition in Ricinus communis: Its effect on plant growth and the chemical composition of the Blacquière T, Hofstra R, Stulen I (1988) Ammonium and nitrate nutri- whole plant, xylem and phloem saps. J Exp Bot 184: 1599 –1610 tion in Plantago lanceolata L. and Plantago major L. ssp. major. III.
Andreev IM (2001) Functions of the vacuole in higher plant cells. Russ Nitrogen metabolism. Plant Soil 104: 129 –141 Blew RD, Parkinson D (1993) Nitrification and denitrification in a white Arnozis PA, Nelemans JA, Findenegg GR (1988) Phospoenolpyruvate spruce forest in southwest Alberta, Canada. Can J For Res 23: carboxylate activity in plants grown with either NO – organic nitrogen source. J Plant Physiol 132: 23 – 27 Bligny R, Gout E, Kaiser W, Heber U, Walker D, Douce R (1997) pH Atkinson CJ (1985) Nitrogen acquisition in four coexisting species regulation in acid-stressed leaves of pea plants grown in the pres- from an upland acidic grassland. Physiol Plant 63: 375 – 387 ence of nitrate or ammonium salts: Studies involving 31P-NMR Backhausen JE, Kitzmann C, Scheibe R (1994) Competition between spectroscopy and chlorophyll fluorescence. Biochim Biophys Acta electron acceptors in photosynthesis – regulation of the malate valve during CO2 fixation and nitrite reduction. Photosynth Res 42: Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Barker AV (1995) Laboratory experiment to assess plant responses to Bobbink R (1998) Impacts of tropospheric ozone and airborne nitro- environmental stresses. J Nat Res Life Sci Educ 24: 145 –149 genous pollutants on natural and semi-natural ecosystems: A com- Barker AV (1999 a) Ammonium accumulation and ethylene evolution by tomato infected with root-knot nematode and grown under dif- Bobbink R, Hornung M, Roelofs JGM (1998) The effects of air-borne ferent regimes of plant nutrition. Comm Soil Sci Plant Anal 30: 175 – nitrogen pollutants on species diversity in natural and semi-natural European vegetation. J Ecol 86: 717–738 Barker AV (1999 b) Foliar ammonium accumulation as an index of Boukcim H, Pages L, Plassard C, Mousain D (2001) Root system arc- stress in plants. Comm Soil Sci Plant Anal 30: 167–174 hitecture and receptivity to mycorrhizal infection infection in seed- Barker AV, Corey KA (1991) Interrelations of ammonium toxicity and lings of Cedrus atlantica as affected by nitrogen source and con- ethylene action in tomato. Hort Sci 26: 177–180 Barker AV, Maynard DN, Lachman WH (1967) Induction of tomato Boxman AW, Krabbendam H, Bellemakers MJS, Roelofs JGM (1991) stem and leaf lesions and potassium deficiency by excessive am- Effects of ammonium and aluminum on the development and nutri- monium nutrition. Soil Sci 103: 319 – 327 tion of Pinus nigra in hydroculture. Environ Pollut 73: 119 –136 Barker AV, Maynard DN, Mioduchowska B, Buch A (1970) Ammonium Breteler H (1973) A comparison between ammonium and nitrate nutri- and salt inhibition of some physiological processes associated with tion of young sugar beet plants grown in nutrient solutions at con- seed germination. Physiol Plant 23: 898 – 907 stant acidity. 2. Effect of light and carbohydrate supply. Neth J Ag- Barneix AJ, Breteler H, van de Geijn SC (1984) Gas and ion exchan- ges in wheat roots after nitrogen supply. Physiol Plant 61: 357– 362 Britto DT, Glass ADM, Kronzucker HJ, Siddiqi MY (2001 a) Cytosolic Bauer GA, Berntson GM (1999) Ammonium and nitrate acquisition by concentrations and transmembrane fluxes of NH + plants in response to elevated CO2 concentration: The roles of root luation of recent proposals. Plant Physiol 125: 523 – 526 physiology and architecture. Tree Physiol 21: 137–144 Britto DT, Siddiqi MY, Glass ADM Kronzucker HJ (2001 b) Futile trans- Below FE, Gentry LE (1987) Effect of mixed N nutrition on nutrient ac- cycling: A cellular hypothesis to explain ammo- cumulation, partitioning, and productivity of corn. J Fert Issues 4: nium toxicity in plants. Proc Natl Acad Sci USA 98: 4255 – 4258 Butterworth RF (1998) Pathogenesis of acute hepatic encephalopathy.
Bendixen R, Gerendás J, Schinner K, Sattelmacher B, Hansen UP (2001) Difference in zeaxanthin formation in nitrate- and ammo- Cakmak I (1994) Activity of ascorbate-dependent H2O2-scavenging nium-grown Phaseolus vulgaris. Physiol Plant 111: 255 – 261 enzymes and leaf chlorosis are enhanced in magnesium- and po- Berridge MJ (1997) The AM and FM of calcium signalling. Nature 386: tassium-deficient leaves, but not in phosphorus-deficient leaves. J Bijlsma RJ, Lambers H, Kooijman SALM (2000) A dynamic whole- Cakmak I, Marschner H (1992) Magnesium deficiency and high light plant model of integrated metabolism of nitrogen and carbon. 1.
intensity enhance activities of superoxide dismutase, ascorbate Comparative ecological implications of ammonium-nitrate interac- peroxidase, and glutathione reductase in bean leaves. Plant Phys- Cao W, Tibbits TW (1998) Response of potatoes to nitrogen concen- Dijk E, Grootjans AB (1998) Performance of four Dactylorhiza species trations differ with nitrogen forms. J Plant Nutr 21: 615 – 623 over a complex trophic gradient. Acta Bot Neerl 47: 351– 368 Cerezo M, Tillard P, Gojon A, Primo-Millo E, Garcia-Agustin P (2001) Dijkshoorn W (1962) Metabolic regulation of the alkaline effect of ni- Characterization and regulation of ammonium transport systems in trate utilization in plants. Nature 194: 165 –167 Citrus plants. Planta 214: 97–105 Dou H, Alva AK, Bondada BR (1999) Growth and chloroplast ultra- Chaillou S, Morot-Gaudry JF, Salsac L, Lesaint C, Jolivet E (1986) structure of two citrus rootstock seedlings in response to ammo- nium and nitrate nutrition. J Plant Nutr 22: 1731–1744 Elmlinger MW, Mohr H (1992) Glutamine synthetase in Scots pine Chaillou S, Vessey JK, Morot-Gaudry JF, Raper CD Jr, Henry LT, Bou- seedlings and its control by blue light and light absorbed by phyto- tin JP (1991) Expression of characterisitics of ammonium nutrition as affected by pH of the root medium. J Exp Bot 42: 189 –196 Eviner VT, Chapin FS III (1997) Plant-microbial interactions. Nature Chen JG, Cheng SH, Cao WX, Zhou X (1998) Involvement of endoge- nous plant hormones in the effect of mixed nitrogen source on Falkengren-Grerup U (1995) Interspecies differences in the prefer- growth and tillering of wheat. J Plant Nutr 21: 87– 97 ence of ammonium and nitrate in vascular plants. Oecologia 102: Claasen MET, Wilcox GE (1974) Effect of nitrogen form on growth and composition of tomato and pea tissue. J Amer Soc Hort Sci 99: Falkengren-Grerup U, Lakkenborg-Kristensen H (1994) Importance of ammonium and nitrate to the performance of herb-layer species Clark RB (1982) Nutrient solution growth of sorghum and corn in min- from deciduous forests in southern sweden. Environ Exp Bot 34: eral nutrition studies. J Plant Nutr 5: 1039 –1057 Claussen W, Lenz F (1999) Effect of ammonium or nitrate nutrition on Fangmeier A, Hadwiger-Fangmeier A, van der Eerden L, Jäger H-J net photosynthesis, growth, and activity of the enzymes nitrate re- (1994) Effects of atmospheric ammonia on vegetation – a review.
ductase and glutamine synthetase in blueberry, raspberry and Farquhar GD, Firth PM, Wetselaar R, Weir B (1980) On the gaseous Clough ECM, Pearson J, Stewart GRS (1989) Nitrate utilization and ni- exchange of ammonia between leaves and the environment. De- trogen status in English woodland communities. Ann Sci For 46 termination of the ammonia compensation point. Plant Physiol 66: Cooke IJ (1962) Toxic effects of urea on plants. Nature 194: 1262 – Feng J, Barker AV (1992 a). Ethylene evolution and ammonium ac- cumulation by nutrient-stressed tomato plants. J Plant Nutr 15: 137– Cox WJ, Reisenauer HM (1973) Growth and ion uptake by wheat sup- plied with nitrogen as nitrate, or ammonium, or both. Plant Soil 38: Feng J, Barker AV (1992 b) Ethylene evolution and ammonium ac- cumulation by nutrient-stressed tomatoes grown with inhibitors of Cramer MD, Lewis OAM (1993) The influence of nitrate and ammo- ethylene synthesis or action. J Plant Nutr 15: 155 –167 nium nutrition on the growth of wheat (Triticum aestivum) and Feng J, Barker AV (1992 c) Ethylene evolution and ammonium ac- maize (Zea mays) plants. Ann Bot 72: 359 – 365 cumulation by tomato plants with various nitrogen forms and regi- Crofts AR (1967) Amine uncoupling of energy transfer in chloroplasts.
mes of acidity. I. J Plant Nutr 15: 2457– 2469 Feng J, Barker AV (1992 d) Ethylene evolution and ammonium ac- Cruz C, Lips SH, Martinsloucao MA (1993) Growth and nutrition of ca- cumulation by tomato plants under water and salinity stresses. II. J rob plants as affected by nitrogen sources. J Plant Nutr 16: 1–15 Davenport RJ, Tester M (2000) A weakly voltage-dependent, nonse- lective cation channel mediates toxic sodium influx in wheat. Plant Feng J, Volk RJ, Jackson WA (1994) Inward and outward transport of ammonium in roots of maize and sorghum: Contrasting effects of methionine sulphoximine. Plant Physiol 5: 429 – 439 de Graaf MCC, Bobbink R, Verbeek PJM, Roelofs JGM (1998) Differ- ential effects of ammonium and nitrate on three heathland species.
Feng J, Volk RJ, Jackson WA (1998) Source and magnitude of ammo- nium generation in maize roots. Plant Physiol 118: 835 – 841 de Visser PHB, Keltjens WB (1993) Growth and nutrient uptake of Findenegg GR (1987) A comparative study of ammonium toxicity at Douglas-fir seedlings at different rates of ammonium supply, with different constant pH of the nutrient solution. Plant Soil 103: 239 – or without additional nitrate and other nutrients. Neth J Agri Sci 41: Forde B (2000) Nitrate transporters in plants: Structure, function and de Visser R, Lambers H (1983) Growth and the efficiency of root respi- regulation. Biochim Biophys Acta 1465: 219 – 235 ration of Pisum sativum as dependent on the source of nitrogen.
Ganmore-Neumann R, Kafkafi U (1983) The effect of root temperature – NH4 ratio on strawberry plants. 1. Growth, flowering, Deignan MT, Lewis OAM (1988) The inhibition of ammonium uptake and root development. Agron J 75: 941– 947 by nitrate in wheat. New Phytol 110: 1– 3 Gardner DK, Lane M, Spitzer A, Batt P (1994) Enhanced rates of Dietz KJ, Heber U, Mimura T (1998) Modulation of the vacuolar H+- cleavages and development for sheep zygotes cultured to the ATPase by adenylates as basis for the transient CO blastocyst stage in vitro in absence of serum and somatic cells: acidification of the leaf vacuole upon illumination. Biochim Biophys Amino acids, vitamins and culturing embryos in groups stimulate Dijk E, Eck N (1995) Ammonium toxicity and nitrate response of axeni- Garnett TP, Smethurst PJ (1999) Ammonium and nitrate uptake by Eu- cally grown Dactylorhiza incarnata seedlings. New Phytol 131: calyptus nitens: Effects of pH and temperature. Plant Soil 214: 133 – Garnett TP, Shabala SN, Smethurst PJ, Newman IA (2001) Simultane- Haghighat N, McCandless DW, Geraminegad P (2000 a) Responses ous measurement of ammonium, nitrate and proton fluxes along in primary astrocytes and C6-glioma cells to ammonium chloride the length of eucalypt roots. Plant Soil 236: 55 – 62 and dibutyryl cyclic-AMP. Neurochem Res 25: 277– 284 Gerendas J, Ratcliffe RG (2000) Intracellular pH regulation in maize Haghighat N, McCandless DW, Geraminegad P (2000 b) The effect of root tips exposed to ammonium at high external pH. J Exp Bot 51: ammonium chloride on metabolism of primary neurons and neu- roblastoma cells in vitro. Metabol Brain Dis 15: 151–162 Gerendas J, Sattelmacher B (1995) Influence of ammonium supply on Hagin J, Olson SR, Shaviv A (1990) Review of interaction of ammo- growth, mineral nutrient and polyamine contents of young maize nium-nitrate and potassium nutrition of crops. J Plant Nutr 13: 1211– plants. Z Pflanzenernaehr Bodenkd 158: 299 – 305 Gerendas J, Zhu Z, Bendixen R, Ratcliffe RG, Sattelmacher B (1997) Harada T, Takaki H, Yamada Y (1968) Effect of nitrogen sources on the Physiological and biochemical processes related to ammonium chemical components in young plants. Soil Sci Plant Nutr 14: 47– toxicity in higher plants. Z Pflanzenernaehr Bodenkd 160: 239 – 251 Gigon A, Rorison IH (1972) The response of some ecologically distinct Hauxwell J, Cebrian J, Furlong C, Valiela I (2001) Macroalgal cano- plant species to nitrate- and to ammonium-nitrogen. J Ecol 60: 93 – pies contribute to eelgrass (Zostera marina) decline in temperate estuarine ecosystems. Ecology 82: 1007–1022 Gijsman AJ (1990 a) Nitrogen nutrition of Douglas-fir (Pseudotsuga Hawkins HJ, George E (2001) Reduced N-15-nitrogen transport menziesii), on strongly acid sandy soil. I. Growth, nutrient uptake through arbuscular mycorrhizal hyphae to Triticum aestivum L.
and ionic balance. Plant Soil 126: 53 – 61 supplied with ammonium vs. nitrate nutrition. Ann Bot 87: 303 – 311 Gijsman AJ (1990 b) Rhizosphere pH along different root zones of Haynes RJ, Goh KM (1978) Ammonium and nitrate nutrition of plants.
Douglas-fir (Pseudotsuga menziesii), as affected by source of ni- Heber U (1984) Flexibility of chloroplast metabolism. In: Sybesma C Gill MA, Reisenauer HM (1993) Nature and characterization of ammo- (ed) Advances in Photosynthesis Research. Martinus Nijhoff/Dr. W.
nium effects on wheat and tomato. Agron J 85: 874 – 879 Givan CV (1979) Metabolic detoxification of ammonia in tissues of Heber U, Wagner U, Kaiser W, Neimanis S, Bailey K, Walker D (1994) higher plants. Phytochemistry 18: 375 – 382 Fast cytoplasmic pH regulation in acid-stressed leaves. Plant Cell Glass ADM, Shaff JE, Kochian LV (1992) Studies of the uptake of ni- trate in barley. 4. Electrophysiology. Plant Physiol 99: 456 – 463 Heber U, Bligny R, Streb P, Douce R (1996) Photorespiration is essen- Glass ADM, Crawford N (1998) Molecular and physiological aspects tial for the protection of the photosynthetic apparatus of C3 plants of nitrate uptake in plants. Trends Plant Sci 3: 389 – 395 against photoinactivation under sunlight. Bot Acta 109: 307– 315 Gloser V, Gloser J (2000) Nitrogen and base cation uptake in seed- Heberer JA, Below FE (1989) Mixed nitrogen nutrition and productivity lings of Acer pseudoplatanus and Calamagrostis villosa exposed of wheat grown in hydroponics. Ann Bot 63: 643 – 649 to an acidified environment. Plant Soil 226: 71–77 Hecht U, Mohr H (1990) Factors controlling nitrate and ammonium ac- Goodchild JA, Givan CV (1990) Influence of ammonium and extracel- cumulation in mustard (Sinapis alba) seedlings. Physiol Plant 78: lular pH on the amino and organic acid contents of suspension cul- ture cells of Acer pseudoplatanus. Physiol Plant 78: 29 – 37 Henriksen GH, Raman DR, Walker LP, Spanswick RM (1992) Measure- Gorison A, Jansen AE, Oltshoorn AFM (1993) The response of some ment of net fluxes of ammonium and nitrate at the surface of barley ecologically distinct plant species to nitrate- and to ammonium- roots using ion-selective microelectrodes. II. Patterns of uptake along the root axis and evaluation of the microelectrode flux esti- Gosz JR, White CS (1986) Seasonal and annual variation in nitrogen mation technique. Plant Physiol 99: 734 –747 mineralization and nitrification along an elevational gradient in New Herrmann A, Felle HH (1995) Tip growth in root hair cells of Sinapis alba L.: Significance of internal and external Ca2+ and pH. New Goulding KWT, Bailey NJ, Bradbury NJ, Hargreaves P, Howe M, Murphy DV, Poulton PR, Willison TW (1998) Nitrogen deposition Holldampf B, Barker AV (1993) Effects of ammonium on elemental nu- and its contribution to nitrogen cycling and associated soil proces- trition of red spruce and indicator plants grown in acid soil. Comm Goyal SS, Lorenz OA, Huffaker RC (1982 a) Inhibitory effects of ammo- Howitt SM, Udvardi MK (2000) Structure, function and regulation of niacal nitrogen on growth of radish plants. I. Characterization of ammonium transporters in plants. Biochim Biophys Acta 1465: on growth and its alleviation by NO3 . J Amer Hunter AS, Rosenau WA (1966) The effects of urea, biuret ammonia Goyal SS, Huffaker RC, Lorenz OA (1982 b) Inhibitory effects of am- on germination and early growth of corn. Soil Sci Soc Amer Proc moniacal nitrogen on growth of radish plants. II. Investigation on the possible causes of ammonium toxicity to radish plants and its Husted S, Hebbern C, Mattsson M, Schjoerring JK (2000) A critical reversal by nitrate. J Amer Soc Hort Sci 107: 130 –135 experimental evaluation of methods for determination of NH + Greidanu T, Schrader LE, Dana MN, Peterson LA (1972) Essentiality of plant tissue, xylem sap, and apoplastic fluid. Physiol Plant 109: ammonium for cranberry nutrition. J Amer Soc Hort Sci 97: 272 – Ikeda M, Yamada Y (1981) Dark CO2 fixation in leaves of tomato plants Hagen SJ, Wu H, Morrison SW (2000) NH4Cl inhibition of acid se- grown with ammonium and nitrate as nitrogen sources. Plant Soil cretion: Possible involvement of an apical K+ channel in bullfrog oxyntic cells. Amer J Phsyiol – Gastroint Liv Physiol 279: G400 – Imsande J (1986) Nitrate ammonium ratio required for pH homeosta- sis in hydroponically grown soybean. J Exp Bot 37: 341– 347 Ingestad T (1973) Mineral nutrient requirements of Vaccinium vitis- Krause GH, Vernotte C, Briantais JM (1982) Photoinduced quenching idaea and V. myrtillus. Physiol Plant 29: 239 – 246 of chlorophyll fluorescence in intact chloroplasts and algae. Bio- Izawa S, Good NE (1972) Inhibition of photosynthetic electron trans- port and photophosphorylation. Meth Enzymol 24: 355 – 377 Krogmann DW, Jagendorf AT, Avron M (1959) Uncouplers of spinach Jackson WA, Chaillou S, Morot-Gaudry J-F, Volk RJ (1993) Endoge- chloroplast photosynthetic phosphorylation. Plant Physiol 34: 272 – nous ammonium generation in maize roots and its relationship to other ammonium fluxes. J Exp Bot 44: 731–739 Krömer S (1995) Respiration during photosynthesis. Annu Rev Plant Jackson RB, Caldwell MM (1993) The scale of nutrient heterogeneity around individual plants and its quantification with geostatistics.
Kronzucker HJ, Siddiqi MY, Glass ADM (1995 a) Compartmentation and flux characteristics of ammonium in spruce. Planta 196: 691– Jeong BR, Lee CW (1992) Growth suppression and raised tissue chlo- ride contents in ammonium-fed marigold, petunia and salvia. J Kronzucker HJ, Siddiqi MY, Glass ADM (1995 b) Analysis of 13NH4 ef- Joy KW (1988) Ammonia, glutamine, and asparagine: A carbon-nitro- flux in spruce roots: A test case for phase identification in compart- gen interface. Can J Bot 66: 2103 – 2109 mental analysis. Plant Physiol 109: 481– 490 Kafkafi U, Ganmore-Neumann R (1997) Ammonium in plant material: Kronzucker HJ, Siddiqi MY, Glass ADM (1996) Kinetics of NH + Real or artifact? J Plant Nutr 20: 107–118 Kaiser G, Martinoia E, Schroppelmeier G, Heber U (1989) Active Kronzucker HJ, Siddiqi MY, Glass ADM (1997) Conifer root discrimina- transport of sulfate into the vacuole of plant-cells provides halotol- tion against soil nitrate and the ecology of forest succession. Na- erance and can detoxify SO2. J Plant Physiol 133: 756–763 Kandlbinder A, da Cruz C, Kaiser W (1997) Response of primary N Kronzucker HJ, Schjoerring JK, Erner Y, Kirk GJD, Siddiqi MY, Glass metabolism to the N source. Z Pflanzenernaehr Bodenkd 160: ADM (1998) Dynamic interactions between root NH + influx and long-distance N translocation in rice: Insights into feedback pro- Karasawa T, Hayakawa T, Mae T, Ojima K, Yamaya T (1994) Charac- cesses. Plant Cell Physiol 39: 1287–1293 teristics of ammonium uptake by rice cells in suspension culture.
Kronzucker HJ, Siddiqi MY, Glass ADM, Kirk GJD (1999 a) Nitrate- Kendall AC, Wallsgrove RM, Hall NP, Turner JC, Lea PJ (1986) Carbon ammonium synergism in rice: A subcellular analysis. Plant Physiol and nitrogen metabolism in barley (Hordeum vulgare L.) mutants lacking ferredoxin-dependent glutamate synthase. Planta 168: Kronzucker HJ, Glass ADM, Siddiqi MY (1999 b) Inhibition of nitrate uptake by ammonium in barley. Analysis of component fluxes.
Kirkby EA (1968) Influence of ammonium and nitrate nutrition on the cation-anion balance and nitrogen and carbohydrate metabolism Kronzucker HJ, Britto DT, Davenport R, Tester M (2001) Ammonium of white mustard plants grown in dilute nutrient solutions. Soil Sci toxicity and the real cost of transport. Trends Plant Sci 6: 335 – 337 Kubin P, Melzer A (1996) Does ammonium affect accumulation of Kirkby EA, Mengel K (1967) Ionic balance in different tissues of tomato starch in rhizomes of Phragmites australis (Cav) Tin ex Steud? Fol plant in relation to nitrate, urea or ammonium nitrogen. Plant Phys- Kudoyarova GR, Farkhutdinov RG, Veselov SY (1997) Comparison of the effects of nitrate and ammonium forms of nitrogen on auxin membranes. Biochim Biophys Acta 639: 41– 52 content in roots and the growth of plants under different temper- Klingensmith KM, van Cleve K (1993) Patterns of nitrogen mineraliza- ature conditions. Plant Growth Reg 23: 207– 208 tion and nitrification in floodplain successional soils along the Ta- nana River, interior Alaska. Can J For Res 23: 964 – 969 Lambert DH, Weidensaul TC (1991) Element uptake by mycorrhizal Köchy M, Wilson SD (2001) Nitrogen deposition and forest expansion soybean from sewage-sludge-treated soil. Soil Sci Soc Amer J 55: in the northern Great Plains. J Ecol 89: 807– 817 Kosegarten H, Grolig F, Wieneke J, Wilson G, Hoffmann B (1997) Dif- Lang B, Kaiser WM (1994) Solute content and energy status of roots ferential ammonia-elicited changes of cytosolic pH in root hair cells of barley plants cultivated at different pH on nitrate- or ammonium- of rice and maize as monitored by 2′,7′-bis-(2-carboxyethyl)-5 (and – 6)-carboxyfluorescein-fluorescence ratio. Plant Physiol 113: 451– Lee JA, Stewart GR (1978) Ecological aspects of nitrogen assimilation.
Kosenko E, Felipo V, Minana MD, Grau E, Grisolía S (1991) Ammonium Lee RB, Ratcliffe RG (1991) Observations on the subcellular distribu- ingestion prevents depletion of hepatic energy metabolites in- tion of the ammonium ion in maize root tissue using in vivo 14N- duced by acute ammonium intoxication. Arch Bioch Biophys 290: nuclear magnetic resonance spectroscopy. Planta 183: 359 – 367 Kosenko EA, Kaminskii YG, Korneev VN, Lukyanova LD (1995) Pro- Leport L, Kandlbinder A, Bauer B, Kaiser WM (1996) Diurnal modula- tective action of M- and N-cholinoceptor blockers in acute ammo- tion of phosphoenolpyruvate carboxylation in pea leaves and roots nium intoxication. Bull Exp Biol Med 120: 1111–1114 as related to tissue malate concentrations and to the nitrogen Krajina VJ, Madoc-Jones S, Mellor G (1973) Ammonium and nitrate in the nitrogen economy of some conifers growing in Douglas-fir Lewis OAM, Leidi EO, Lips SH (1989) Effect of nitrogen source on communities of the Pacific North-West of America. Soil Biol Bio- growth response to salinity stress in maize and wheat. New Phytol Lewis OAM, Soares MIM, Lips SH (1986) A photosynthetic and N in- Martinoia E, Heck V, Wiemken A (1981) Vacuoles as storage compart- vestigation of the differential growth response of barley to nitrate, ments for nitrate in barley leaves. Nature 289: 292 – 294 ammonium, and nitrate + ammonium nutrition. In: Lambers H, Nee- Matsumoto H, Tamura K (1981) Respiratory stress in cucumber roots teson JJ, Stulen I (eds) Fundamental, Ecological and Agricultural treated with ammonium or nitrate nitrogen. Plant Soil 60: 195 – 204 Aspects of Nitrogen Metabolism in Higher Plants. Developments in Matsumoto H, Wakiuchi N, Takahashi E (1971) Changes of starch syn- Plant and Soil Sciences. Martinus Nijhoff Publishers, Dordrecht, thestase activity of cucumber leaves during ammonium toxicity.
Liao Z, Woodard HJ, Hossner LR (1994) The relationship of soil and McClure PR, Kochian LV, Spanswick RM, Shaff J (1990) Evidence for leaf nutrients to rice leaf oranging. J Plant Nutr 17: 1781–1802 cotransport of nitrate and proton in maize roots. I. Effects of nitrate Lindt T, Feller U (1987) Effect of nitrate and ammonium on long dis- on the membrane potential. Plant Physiol 76: 913 – 917 tance transport in cucumber plants. Bot Helv 97: 45 – 52 McQueen A, Bailey JE (1991) Growth inhibition of hybridoma cells by Lips SH, Leidi EO, Silberbush M, Soores MIM, Lewis EM (1990) Phy- ammonium ion: Correlation with effects on intracellular pH. Bioproc siological aspects of ammonium and nitrate fertilization. J Plant Megie CA, Pearson RW, Hiltbold AE (1967) Toxicity of decomposing Lodhi MAK (1978) Inhibition of nitrifying bacteria, nitrification, and min- corn residues to cotton germination and seedling growth. Agron J eralization of spoil soils as related to their successsional stages.
Mae T, Hoshino T, Ohira K (1985) Proteinase activities and loss of ni- brane of Arabidopsis thaliana root hairs: Kinetic control by pH and trogen in the senescing leaves of field-grown rice (Oryza sativa L.).
membrane voltage. J Membr Biol 145: 49 – 66 Mehrer I, Mohr H (1989) Ammonium toxicity: Description of the synd- Magalhaes JR, Huber DM (1989) Ammonium assimilation in different rome in Sinapis alba and the search for its causation. Physiol Plant plant species as affected by nitrogen form and pH control in solu- Mevius W, Engel H (1931) Die Wirkung der Ammoniumsalze in ihrer Magalhaes JS, Wilcox GE (1983 a) Tomato growth and mineral com- Abhängigkeit von der Wasserstoffionenkonzentration II. Planta 9: position as influenced by nitrogen form and light intensity. J Plant Min X, Siddiqi MY, Guy RD (1999) A comparative study of fluxes and Magalhaes JS, Wilcox GE (1983 b) Tomato growth and nutrient uptake compartmentation of nitrate and ammonium in early-successional patterns as influenced by nitrogen form and light intensity. J Plant tree species. Plant Cell Environ 22: 821– 830 Min XJ, Siddiqi MY, Guy RD, Glass ADM, Kronzucker HJ (2000) A Magalhaes JS, Wilcox GE (1984 a) Ammonium toxicity development in comparative kinetic analysis of nitrate and ammonium influx in two tomato plants relative to nitrogen form and light intensity. J Plant early-successional tree species of temperate and boreal forest ecosystems. Plant Cell Environ 23: 321– 328 Magalhaes JS, Wilcox GE (1984 b) Growth, free amino acids, and min- Minelli A, Lyons S, Nolte C, Verkhratsky A, Kettenmann H (2000) Am- eral composition of tomato plants in relation to nitrogen form and monium triggers calcium elevation in cultured mouse microbe glial growing media. J Amer Soc Hort Sci 109: 406 – 411 cells by initiating Ca2+ release from thapsigargin-sensitive intracel- Magalhaes JR, Machado AT, Huber DM (1995) Similarities in response lular stores. Eur J Physiol 439: 370 – 377 of maize genotypes to water logging and ammonium toxicity. J Mirabet M, Navarro A, Lopez A, Canela EI, Mallol J, Lluis C, Franco R (1997) Ammonium toxicity in different cell lines. Biotechnol Bioeng Majerowicz N, Kerbauy GB, Nievola CC, Suzuki RM (2000) Growth and nitrogen metabolism of Catasetum fimbriatum (Orchidaceae) Mironova GD, Grigoriev SM, Skarga YY, Negoda AE, Kolomytkin OV grown with different nitrogen sources. Environ Exp Bot 44: 195 – (1996) ATP-dependent potassium channel from rat liver mitochond- ria – inhibitory analysis, channel clusterization. Biologicheskie Marcaida G, Felipo V, Hermenegildo C, Miñana MD, Grisolía S (1992) Acute ammonia toxicity is mediated by the NMDA type of gluta- Mistrik I, Ullrich CI (1996) Mechanism of anion uptake in plant roots: Margolis D (1960) The range of free amino acids and amides in to- tries. Plant Physiol Biochem 34: 629 – 636 mato plants and the effects of nitrate or ammonium as nutrients.
Monselise EBI, Kost D (1993) Different ammonium-ion uptake, metab- olism and detoxification efficiencies in two Lemnaceae: A nitrogen- Marschner H (1995) Mineral Nutrition of Higher Plants. Academic 15 nuclear magnetic resonance study. Planta 189: 167–173 Murthy CRK, Bender AS, Dombro RS, Bai G, Norenberg MD (2000) Marschner H, Häussling M, George E (1991) Ammonium and nitrate Elevation of glutathione levels by ammonium ions in primary cul- uptake rates and rhizosphere pH in non-mycorrhizal roots of Nor- tures of rat astrocytes. Neurochem Int 37: 255 – 268 way roots (Picea abies L. Karst.). Trees 5: 14 – 21 Nesdoly RG, van Rees KCJ (1998) Redistribution of extractable nutri- Martin B (ed) (1987) Plant Vacuoles: Their Importance in Solute Com- ents following disc trenching on Luvisols and Brunisols in Saskatc- partmentation in Cells and their Applications in Plant Biotechno- Nielsen KH, Schjoerring JK (1998) Regulation of apoplastic NH + Martinelle K, Haggstrom L (1993) Mechanism of ammonia and ammo- centration in leaves of oilseed rape. Plant Physiol 118: 1361–1368 nium ion toxicity in animal cells: Transport across cell membranes.
Nihlgard B (1985) The ammonium hypothesis – an additional explana- tion to the forest dieback in Europe. Ambio 14: 2 – 8 Ninnemann O, Jauniaux JC, Frommer JB (1994) Identification of a Rennenberg H (1998) Field and laboratory experiments on net uptake transporter from plants. EMBO J 13: 3464 – 3471 of nitrate and ammonium by the roots of spruce (Picea abies) and Noctor G, Foyer CH (1998) A re-evaluation of the ATP : NADPH budget beech (Fagus sylvatica) trees. New Phytol 138: 275 – 285 during C-3 photosynthesis: A contribution from nitrate assimilation Rennenberg H, Kreutzer K, Papen H, Weber P (1998) Consequences and its associated respiratory activity? J Exp Bot 49: 1895 –1908 of high loads of nitrogen for spruce (Picea abies) and beech (Fa- Oaks A (1994) Primary nitrogen assimilation in higher plants and its gus sylvatica) forests. New Phytol 139: 71– 86 Rice EL, Pancholy SK (1972) Inhibition of nitrification by climax eco- Oja V, Savchenko G, Jakob B, Heber U (1999) pH and buffer capac- ities of apoplastic and cytoplasmic cell compartments in leaves.
Rideout JW, Chaillou S, Raper CD Jr, Morot-Gaudry J-F (1994) Ammo- nium and nitrate uptake by soybean during recovery from nitrogen Olff H, Huisman J, van Tooren BF (1993) Species dynamics and nutri- ent accumulation during early primary succession in coastal sand Rigano C, Di Martino Rigano V, Vona V, Carfagna S, Carillo P, Esposito S (1996) Ammonium assimilation by young plants of Hordeum vul- Oltshoorn AFM, Keltjens WG, van Baren B, Hopman MCG (1991) Influ- gare in light and darkness – effects on respiratory oxygen con- ence of ammonium on fine root development and rhizosphere pH sumption by roots. New Phytol 132: 375 – 382 of Douglas-fir seedlings in sand. Plant Soil 133: 75 – 82 Ritchie RJ, Gibson J (1987) Permeability of ammonia, methylamine and ethylamine in the cyanobacterium Synechococcus R-2 (Ana- Ota K, Yamamoto Y (1989) Promotion of assimilation of ammonium cystis nidulans) PCC7942. J Membr Biol 95: 131–142 ions by simultaneous application of nitrate and ammonium ions in radish plants. Plant Cell Physiol 30: 365 – 371 Roberts JKM, Pang MKL (1992) Estimation of ammonium ion distribu- tion between cytoplasm and vacuole using nuclear magnetic reso- Pearson J, Stewart GR (1993) The deposition of atmospheric ammo- nance spectroscopy. Plant Physiol 100: 1571–1574 nia and its effects on plants. New Phytol 125: 283 – 305 Rosnitschek-Schimmel I (1985) The influence of nitrogen nutrition on Peckol P, Rivers JS (1995) Physiological responses of the opportunis- the accumulation of free amino acids in root tissue of Urtica dioica tic macroalgae Cladophora vagabunda (L.) van den Hoek and and their apical transport of xylem sap. Plant Cell Physiol 26: 215 – Gracilaria tikvahiae (MacLachlan) to environmental disturbances associated with eutrophication. J Exp Mar Biol Ecol 23: 122 –127 Runge M (1983) Physiology and ecology of nitrogen nutrition. In: Peterson LA, Stang EJ, Dana MN (1988) Blueberry response to am- Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Physiological monium nitrogen and nitrate nitrogen. J Amer Soc Hort Sci 113: Plant Ecology, III, 12C. Springer Verlag, New York pp 163 – 200 Ryan PR, Walker NA (1994) The regulation of ammonia uptake in Petit PX, O’Connor D, Grunwald D, Brown SC (1990) Analysis of the Chara australis. J Exp Bot 45: 1057–1067 membrane potential of rat- and mouse-liver mitochondria by flow Sakakibara H, Suzuki M, Takei K, Deji, Taniguchi M, Sugiyama T cytometry and possible applications. Eur J Biochem 194: 389 – 397 (1998) A response-regulator homologue possibly involved in nitro- Pill WG, Lambeth VN (1977) Effects of ammonium and nitrate nutrition gen signal transduction mediated by cytokinin in maize. Plant J 14: with and without pH adjustment on tomato growth, ion composition, and water relations. J Amer Soc Hort Sci 102: 78 – 81 Salisbury FB, Ross CW (1992) Plant Physiology. Wadsworth, Belmont, Plieth C, Sattelmacher B, Knight MR (2000) Ammonium uptake and cellular alkalanisatin in roots of Arabidopsis thaliana: The involve- Salsac L, Chaillou S, Morot-Gaudry JF, Lesaint C, Jolivoe E (1987) Ni- ment of cytoplasmic calcium. Physiol Plant 110: 518 – 523 trate and ammonium nutrition in plants. Plant Physiol Biochem 25: Polle A, Chakrabarti K, Chakrabarti S, Seifert S, Schramel P, Rennen- berg H (1992) Antioxidants and manganese deficiency in needles Samuelson ME, Larsson CM (1993) Nitrate regulation of zeatin ribo- of Norway spruce (Picea abies L.) trees. Plant Physiol 99: 1084 – side levels in barley roots – effects of inhibitors of N assimilation and comparison with ammonium. Plant Sci 93: 77– 84 Puritch GS, Barker AV (1967) Structure and function of tomato leaf Saravitz CH, Chaillou S, Musset J, Raper CD Jr, Morot-Gaudry J-F chloroplasts during ammonium toxicity. Plant Physiol 42: 1229 – (1994) Influence of nitrate on uptake of ammonium by nitrogen- depleted soybean: Is the effect located in roots or shoots? J Exp Raab TK, Terry N (1994) Nitrogen source regulation of growth and photosynthesis in Beta vulgaris L. Plant Physiol 105: 1159 –1166 Sasakawa H, Yamamoto Y (1978) Comparison of the uptake of nitrate Raven JA, Farquhar GD (1981) Methylammonium transport in Phaseo- and ammonium by rice seedlings. Influences of light, temperature, lus vulgaris leaf slices. Plant Physiol 67: 859 – 863 oxygen concentration, exogenous sucrose, and metabolic inhib- Raven JA, Smith FA (1976) Nitrogen assimilation and transport in vas- cular land plants in relation to intracellular pH regulation. New Phy- Sattelmacher B, Thoms K (1995) Morphology and physiology of the seminal root-system of young maize (Zea mays L.) plants as influ- Rawat SR, Silim SN, Kronzucker HJ, Siddiqi MY, Glass ADM (1999) enced by a locally restricted nitrate supply. Z Pflanzenernaehr Bo- thaliana: Evidence for regulation by root glutamine levels. Plant J Schachtman DP, Schroeder JI, Lucas WJ, Anderson JA, Gaber RF (1992) Expression of an inward-rectifying potassium channel by the Redinbaugh MG, Campbell WH (1993) Glutamine synthetase and fer- Arabidopsis KAT1 cDNA. Science 258: 1654 –1658 redoxin-dependent glutamate synthase expression in the maize Schenk M, Wehrmann J (1979) The influence of ammonium in nutrient (Zea mays) root primary response to nitrate. Evidence for an or- solution on growth and metabolism of cucumber plants. Plant Soil gan-specific response. Plant Physiol 101: 1249 –1255 Schjoerring JK, Husted S, Mack G, Nielsen KH, Finnemann J, Matts- Tobin AK, Yamaya T (2001) Cellular compartmentation of ammonium son M (2000) Physiological regulation of plant-atmosphere ammo- assimilation in rice and barley. J Exp Bot 52: 591– 604 Torrey (1976) Root hormones and plant growth. Annu Rev Plant Phys- Schjoerring JK, Husted S, Mäck G, Mattsson M (2002) The regulation of ammonium translocation in plants. J Exp Bot (in press) Tremblay GC, Bradley TM (1992) L-carnitine protects fish against Schlee J, Komor E (1986) Ammonium uptake by Chlorella. Planta 168: acute ammonia toxicity. Comp Bioch Physiol C 101: 349 – 351 Troelstra SR, Van Dijk C, Blacquière T (1985) Effects of N source on Schortemeyer M, Stamp P, Feil B (1997) Ammonium tolerance and proton excretion, ion balance and growth of Alnus glutinosa L.
carbohydrate status in maize cultivars. Ann Bot 79: 25 – 30 (Gaertner): Comparison of N2 fixation with single and mixed sour- Schubert S, Yan F (1997) Nitrate and ammonium nutrition of plants: Ef- fects on acid/base balance and adaptation of root cell plasma- Troelstra SR, Wagenaar R, Smant W (1995) Nitrogen utilization by lemma H+ ATPase. Z Pflanzenernaehr Bodenkd 160: 275 – 281 plant species from acid heathland soils. 1. Comparison between Sener A, Malaisse WJ (1980) The stimulus secretion coupling of ami- nitrate and ammonium nutrition at constant low pH. J Exp Bot 46: no-acid induced insulin release 2. Sensitivity to K+, NH + leucine stimulated islets. Diabete Metab 6: 97–101 Truax B, Lambert F, Gagnon D, Chevrier N (1994) Nitrate reductase Siddiqi MY, Glass ADM (1993) Mechanisms of nitrate uptake by and glutamine synthetase activities in relation to growth and nitro- higher plants. Curr Top Plant Physiol 1: 219 – 228 gen assimilation in red oak and red ash seedlings: Effects of Siebke K, Yin ZH, Raghavendra AS, Heber U (1992) Vacuolar pH os- N-forms, N concentration and light intensity. Trees 9: 12 –18 cillations in mesophyll cells accompany oscillations of photosyn- Ullrich WR, Larsson M, Larsson C-M, Lesch S, Novacky A (1984) Am- thesis in leaves – interdependence of cellular compartments, and monium uptake in Lemna gibba G 1, related membrane potential regulation of electron flow in photosynthesis. Planta 186: 526 – 531 changes, and inhibition of anion uptake. Physiol Plant 61: 369 – 376 Singh ST, Letham DS, Zhang XD, Palni LMS (1992) Cytokinin bio- Vale FR, Volk RJ, Jackson WA (1988) Simultaneous influx of ammo- chemistry in relation to leaf senescence. 6. Effect of nitrogenous nium and potassium into maize roots: Kinetics and interactions.
nutrients on cytokinin levels and senescence of tobacco leaves.
Valiela I, Geist M, McClelland J, Tomasky G (2000) Nitrogen loading Smiciklas KD, Below FE (1992) Role of cytokinin in enhanced produc- from watersheds to estuaries: Verification of the Waquoit Bay Nitro- gen Loading Model. Biogeochem 49: 277– 293 van Beusichem ML, Kirkby EA, Baas R (1988) Influence of nitrate and Smirnoff N, Todd P, Stewart GR (1984) The occurrence of nitrate re- ammonium nutrition on the uptake, assimilation, and distribution of ductase in the leaves of woody plants. Ann Bot 54: 363 – 374 nutrients in Ricinus communis. Plant Physiol 86: 914 – 921 Smith FA (1982) Transport of methylammonium and ammonium ions van Breemen N, Burrough PA, Velthorst EJ, van Dobben HF, Dewit T, by Elodea densa. J Exp Bot 33: 221– 232 Ridder TB, Reijnders HFR (1982) Soil acidification from atmos- Smith FA, Raven JA (1979) Intracellular pH and its regulation. Annu pheric ammonium sulfate in forest canopy throughfall. Nature 299: Smith WH, Bormann FH, Likens GE (1968) Response of chemoau- van Breemen N, van Dijk HFG (1988) Ecosystem effects of atmos- totrophic nitrifiers to forest cutting. Soil Sci 106: 471– 473 pheric deposition of nitrogen in the Netherlands. Environ Poll 54: Sokolik AI, Yurin VM (1986) Potassium channels in the plasmalemma of Nitella cells at rest. J Membr Biol 89: 9 – 22 van Cleve K, Yarie J, Erickson R (1993) Nitrogen mineralization and ni- Speer M, Brune A, Kaiser WM (1994) Replacement of nitrate by am- trification in successional ecosystems on the Tanana River flood- monium as the nitrogen source increases the salt sensitivity of pea plain, interior Alaska. Can J For Res 23: 970 – 978 plants. 1. Ion concentrations in roots and leaves. Plant Cell Environ van Dam D, Van Dobben HF, Terbraak CFJ, De Witt T (1986) Air pollu- tion as a possible cause for the decline of some phanerogamic Speer M, Kaiser WM (1994) Replacement of nitrate by ammonium as species in the Netherlands. Vegetatio 65: 47– 52 the nitrogen source increases the salt sensitivity of pea plants. 2.
van den Driessche R (1971) Response of conifer seedlings to nitrate Intercellular and intracellular solute compartmentation in leaflets.
and ammonium sources of nitrogen. Plant Soil 34: 421– 439 van den Driessche R, Dangerfield J (1978) Response of Douglas-fir Stark JM, Hart SC (1997) High rates of nitrification and nitrate turnover seedlings to nitrate and ammonium nitrogen sources under various in undisturbed coniferous forests. Nature 385: 61– 64 environmental conditions. Plant Soil 42: 685 –702 Stitt M, Krapp A (1999) The interaction between elevated carbon dio- van der Eerden L (1982) Toxicity of ammonia to plants. Agri Environ 7: xide and nitrogen nutrition: The physiological and molecular back- ground. Plant Cell Environ 22: 583 – 621 van der Eerden L (1998) Nitrogen on microbial and global scales.
Takács E, Técsi L (1992) Effects of NO – rates, nitrate reductase activity and chloroplast ultrastructure in van Dijk HFG, Roelofs JGM (1988) Effects of excessive ammonium three cultivars of red pepper (Capsicum annuum L.). J Plant Phys- deposition on the nutritional status and condition of pine needles.
Taylor AR, Bloom AJ (1998) Ammonium, nitrate, and proton fluxes van Dijk HFG, Creemers RCM, Rijniers JPLWM, Roelofs JGM (1989) along the maize root. Plant Cell Environ 21: 1255 –1263 Impact of artificial, ammonium-enriched rainwater on soils and Tischner R (2000) Nitrate uptake and reduction in higher and lower young coniferous trees in a greenhouse. 1. Effects on the soils. En- plants. Plant Cell Environ 23: 1005 –1024 van Dijk HFG, Delouw MHJ, Roelofs JGM, Verburgh JJ (1990) Impact Wang XT, Below FE (1996) Cytokinins in enhanced growth and tillering of artificial, ammonium- enriched rainwater on soils and young co- of wheat induced by mixed nitrogen source. Crop Sci 36: 121–126 niferous trees in a greenhouse. 2. Effects on the trees. Environ Poll Warren CR, Chen ZL, Adams MA (2000) Effect of N source on con- centration of Rubisco in Eucalyptus diversicolor, as measured by van Katwijk MM, Vergeer LHT, Schmidtz GHW, Roelofs JGM (1997) capillary electrophoresis. Physiol Plant 110: 52 – 58 Ammonium toxicity in eelgrass Zostera marina. Mar Ecol Progr Ser Weissman GS (1964) Effect of ammonium and nitrate nutrition on pro- tein level and exudate composition. Plant Physiol 39: 947– 952 Vanselow KH (1993) The effect of N-nutrients on the acceptor pool of Wells D, Miller AJ (2000) Intracellular measurement of ammonium in PS I and thylakoid energization as measured by chlorophyll fluo- Chara corallina using ion-selective microelectrodes. Plant Soil 221: rescence of Dunaliella salina. J Exp Bot 44: 1331–1340 Venegoni A, Moroni A, Gazzarini S, Marre MT (1997) Ammonium and Westwood JH, Foy CL (1999) Influence of nitrogen on germination and methylammonium transport in Egeria densa leaves in conditions of early development of broomrape (Orobanche spp.). Weed Sci 47: different H+ pump activity. Bot Acta 110: 369 – 377 Vernon LP, Zang WS (1960) Photoreduction by fresh and aged chloro- White PJ (1996) The permeation of ammonium through a voltage-inde- plasts: Requirements for ascorbate and 2,6-dichlorophenol indo- pendent K+ channel in the plasma membrane of rye roots. J phenol with aged chloroplasts. J Biol Chem 235: 2728 – 2733 Vines HM, Wedding RT (1960) Some effects of ammonia on plant me- Wieneke J, Roeb GW (1997) Effect of methionine sulphoximine on tabolism and a possible mechanism for ammonia toxicity. Plant 13N-ammonium fluxes in the roots of barley and squash seedlings.
Vitousek PM (1994) Beyond global warming: Ecology and global Wiese C, Shi LB, Heber U (1998) Oxygen reduction in the Mehler Vitousek PM, Gosz JR, Grier CC, Melillo JM, Reiners WA (1982) A reaction is insufficient to protect photosystems I and II of leaves comparative analysis of potential nitrification and nitrate mobility in against photoinactivation. Physiol Plant 102: 437– 446 forest ecosystems. Ecol Monogr 52: 155 –177 Wilson GH, Grolig F, Kosegarten H (1998) Differential pH restoration Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human after ammonia-elicited vacuolar alkalisation in rice and maize root domination of Earth’s ecosystems. Science 277: 494 – 499 hairs as measured by fluorescence ratio. Planta 206: 154 –161 Vollbrecht P, Kasemir HI (1992) Effects of exogenously supplied am- Wolt J (1994) Soil solution Chemistry: Applications to Environmental monium on root development of Scots Pine (Pinus sylvestris L.) Science and Agriculture. John Wiley and Sons, New York Woolhouse HW, Hardwick K (1966) The growth of tomato seedlings in Vollbrecht P, Klein E, Kasemir H (1989) Different effects of supplied relation to the form of the nitrogen supply. New Phytol 65: 518 – 526 ammonium on glutamine synthetase activity in mustard (Sinapis Yamashita K, Kasai M, Ezaki B, Shibasaka M, Yamamoto Y, Matsu- alba) and pine (Pinus sylvestris) seedlings. Physiol Plant 77: 129 – moto H, Sasakawa H (1995) Stimulation of H+ extrusion and plas- ma-membrane H+-ATPase activity of barley roots by ammonium Von Wirén N, Gazzarini S, Gojon A, Frommer WB (2000) The molec- treatment. Soil Sci Plant Nutr 41: 133 –140 ular physiology of ammonium uptake and retrieval. Curr Opin Plant Yan F, Schubert S, Mengel K (1992) Effect of low root medium pH on net proton release, root respiration, and root growth of corn (Zea Walch-Liu P, Neumann G, Bangerth F, Engels C (2000) Rapid effects mays L.) and broad bean (Vicia faba L.). Plant Physiol 99: 415 – 421 of nitrogen form on leaf morphogenesis in tobacco. J Exp Bot 343: Yin ZH, Huve K, Heber U (1996 a) Light-dependent proton transport into mesophyll vacuoles of leaves of C-3 plants as revealed by pH- Walker DJ, Leigh RA, Miller AJ (1996) Potassium homeostasis in vacu- indicating fluorescent dyes: A reappraisal. Planta 199: 9 –17 olate plant cells. Proc Natl Acad Sci USA 93: 10510 –10514 Yin Z-H, Kaiser WM, Heber U, Raven JA (1996 b) Acquisition and as- Walker NA, Beilby MJ, Smith FA (1979 a) Amine uniport at the plasma- similation of gaseous ammonium as revealed by intracellular pH lemma of charophyte cells I. Current-voltage curves, saturation ki- changes in leaves of higher plants. Planta 200: 380 – 387 netics, and effects of unstirred layers. J Membr Biol 49: 21– 55 Zhang YS, Sun X, Ying QZ (1990) The effect of organic manure and Walker NA, Smith FA, Beilby MJ (1979 b) Amine uniport at the plasma- potassium in preventing ammonium toxicity in barley. Acta Pedo- lemma of charophyte cells II. Ratio of matter to charge transported and permeability of free base. J Membr Biol 49: 283 – 296 Wang MY, Siddiqi MY, Ruth TJ, Glass ADM (1993 a) Ammonium up- Zhu Z, Gerendas J, Bendixen R, Schinner K, Tabrizi H, Sattelmacher take by rice roots. I. Fluxes and subcellular distribution of 13NH + B, Hansen U-P (2000) Different tolerance to light stress in NO - and NH4 -grown Phaseolus vulgaris L. Plant Biol 2: 558 – 570 Wang MY, Siddiqi MY, Ruth TJ, Glass ADM (1993 b) Ammonium up- Ziegler H (1975) Nature of substances in phloem. In: Pirson A, Zim- take by rice roots. II. Kinetics of 13NH + mermann MH (eds) Encyclopedia of Plant Physiology. Vol 1.
Wang MY, Glass ADM, Shaff JE, Kochian LV (1994) Ammonium uptake Zornoza P, Caselles J, Carpena O (1987) Response of pepper plants by rice roots. III. Electrophysiology. Plant Physiol 104: 899 – 906 ratio and light intensity. J Plant Nutr 10: 773 –782

Source: http://docent.hogent.be/~fdbe129/amtox.pdf

O:\cr signed orders\fabela 05-0099-2o.wpd

Case 2:05-cr-00099-MHM Document 280 Filed 09/29/09 Page 1 of 13Currently pending before the Court is the United States of America’s request for anOrder pursuant to United States v. Sell, 539 U.S. 166 (2003). After reviewing the Partiespleadings and conducting an evidentiary hearing, the Court issues the following Order. BACKGROUND This is a criminal case in which Defendant, Anthony Fabela


EUTHYMICS BIOSCIENCE, INC. NAMES BIOTECH EXECUTIVE TIMOTHY J. BARBERICH TO BOARD OF DIRECTORS -- Former Sepracor Founder and CEO Brings a History of Experience and Success in Drug Development and Commercialization -- Cambridge, MA – November 4, 2010 - Euthymics Bioscience, Inc., a clinical-stage company developing next-generation antidepressants, today announced that Tim

Copyright © 2010-2014 Online pdf catalog