J. Plant Physiol. 159. 567 – 584 (2002)  Urban & Fischer Verlag 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: [email protected] 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).
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