Reciprocal Ammonium Transport Into and Out of Plant Roots: Modifications by Plant Nitrogen Status and Elevated Root Ammonium Concentration

Morgan, M. A.; Jackson, W. A.

doi:10.1093/jxb/40.2.207

Cited by 30 publications

(25 citation statements)

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“…For instance, NH 4 1 suppresses high-affinity K 1 transport (Scherer et al, 1984;Vale et al, 1987Vale et al, , 1988Morgan and Jackson, 1984;Hirsch et al, 1998;Spalding et al, 1999;Santa-Maria et al, 2000;Ashley et al, 2006), while low-affinity K 1 transport is relatively NH 4 1 insensitive and contributes to the relief from NH 4 1 toxicity at high K 1 (Santa-Maria et al, 2000;Britto and Kronzucker, 2002;Kronzucker et al, 2003b). Similarly, variable sensitivities of K 1 transporters to soil Na 1 are critical factors in salinity tolerance (Epstein et al, 1963;Kochian et al, 1985;Tester and Davenport, 2003;Volkov et al, 2004;Kader and Lindberg, 2005).…”

Section: /Hmentioning

confidence: 99%

Rapid, Futile K+ Cycling and Pool-Size Dynamics Define Low-Affinity Potassium Transport in Barley

2006

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Using the short-lived radiotracer 42K+, we present a comprehensive subcellular flux analysis of low-affinity K+ transport in plants. We overturn the paradigm of cytosolic K+ pool-size homeostasis and demonstrate that low-affinity K+ transport is characterized by futile cycling of K+ at the plasma membrane. Using two methods of compartmental analysis in intact seedlings of barley (Hordeum vulgare L. cv Klondike), we present data for steady-state unidirectional influx, efflux, net flux, cytosolic pool size, and exchange kinetics, and show that, with increasing external [K+] ([K+]ext), both influx and efflux increase dramatically, and that the ratio of efflux to influx exceeds 70% at [K+]ext ≥ 20 mm. Increasing [K+]ext, furthermore, leads to a shortening of the half-time for cytosolic K+ exchange, to values 2 to 3 times lower than are characteristic of high-affinity transport. Cytosolic K+ concentrations are shown to vary between 40 and 200 mm, depending on [K+]ext, on nitrogen treatment (NO3− or NH4+), and on the dominant mode of transport (high- or low-affinity transport), illustrating the dynamic nature of the cytosolic K+ pool, rather than its homeostatic maintenance. Based on measurements of trans-plasma membrane electrical potential, estimates of cytosolic K+ pool size, and the magnitude of unidirectional K+ fluxes, we describe efflux as the most energetically demanding of the cellular K+ fluxes that constitute low-affinity transport.

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Section: /Hmentioning

confidence: 99%

Rapid, Futile K+ Cycling and Pool-Size Dynamics Define Low-Affinity Potassium Transport in Barley

2006

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“…Nitrogen starvation or nitrogen-limiting conditions lead to a marked increase in the root capacity to take up NO 3 Ϫ or NH 4 ϩ (Lee and Rudge 1986), a response that is mostly due to the stimulation of the HATSmediated influx of the two ions (Morgan and Jackson, 1988;Hole et al, 1990;Lee, 1993;Wang et al, 1993), and is associated in Arabidopsis with a strong increase in the expression of the NO 3 Ϫ and NH 4 ϩ transporter genes AtNrt2.1 and AtAmt1.1 (Gazzarrini et al, 1999;Lejay et al, 1999). This regulation is thought to be due to repression of NO 3 Ϫ and NH 4 ϩ transporters by reduced nitrogen metabolites accumulating in the tissues under satiety conditions (Jackson et al, 1986;Clarkson and Lü ttge, 1991;Lee et al, 1992;Muller and Touraine, 1992).…”

Section: The Atnrt2 Mutant Lacks the Hats Component Under Feedback Comentioning

confidence: 99%

Major Alterations of the Regulation of Root NO3 − Uptake Are Associated with the Mutation of Nrt2.1 and Nrt2.2 Genes in Arabidopsis

et al. 2001

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The role of AtNrt2.1 and AtNrt2.2 genes, encoding putative NO 3 Ϫ transporters in Arabidopsis, in the regulation of high-affinity NO 3 Ϫ uptake has been investigated in the atnrt2 mutant, where these two genes are deleted. Our initial analysis of the atnrt2 mutant (S. Filleur, M. Ϫ uptake is affected in this mutant due to the alteration of the high-affinity transport system (HATS), but not of the low-affinity transport system. In the present work, we show that the residual HATS activity in atnrt2 plants is not inducible by NO 3 Ϫ , indicating that the mutant is more specifically impaired in the inducible component of the HATS. Thus, high-affinity NO 3 Ϫ uptake in this genotype is likely to be due to the constitutive HATS. Root 15 NO 3 Ϫ influx in the atnrt2 mutant is no more derepressed by nitrogen starvation or decrease in the external NO 3 Ϫ availability. Moreover, the mutant also lacks the usual compensatory up-regulation of NO 3 Ϫ uptake in NO 3 Ϫ -fed roots, in response to nitrogen deprivation of another portion of the root system. Finally, exogenous supply of NH 4 ϩ in the nutrient solution fails to inhibit 15 NO 3 Ϫ influx in the mutant, whereas it strongly decreases that in the wild type. This is not explained by a reduced activity of NH 4 ϩ uptake systems in the mutant. These results collectively indicate that AtNrt2.1 and/or AtNrt2.2 genes play a key role in the regulation of the high-affinity NO 3 Ϫ uptake, and in the adaptative responses of the plant to both spatial and temporal changes in nitrogen availability in the environment. The uptake of NO 3Ϫ by roots cells is a key process for higher plants because it is the first step of the assimilatory pathway providing most of organic nitrogen required for synthesis of biomolecules, including proteins and nucleic acids (Beevers and Hageman, 1980). More than 30 years of physiological investigations have led to the conclusion that at least three uptake systems are responsible for the influx of NO 3 Ϫ into the roots (for review, see Clarkson, 1986;Glass and Siddiqi, 1995;Crawford and Glass, 1998;Daniel-Vedele et al., 1998;Forde, 2000). Two highaffinity transport systems (HATS) are able to take up NO 3 Ϫ at low concentrations in the external medium, and display saturable kinetics as a function of the external NO 3 Ϫ concentration ([NO 3 Ϫ ] o ), with saturation in the range of 0.2 to 0.5 mm [NO 3 Ϫ ] o . One of these systems appears to be present even in plants never supplied with NO 3 Ϫ , and thus is considered as constitutive (cHATS). The other HATS is specifically stimulated by NO 3 Ϫ , and is consequently assumed to be inducible (iHATS). The maximum activity (V max ) recorded for the iHATS is generally much larger than that of the cHATS, suggesting that the former system plays a key role in the root uptake of NO 3 Ϫ from external media where [NO 3 Ϫ ] o does not exceed 1 mm. The iHATS and cHATS appear to be genetically distinct because a mutant defective in the cHATS, but not in the iHATS, has been isolated in Arabidopsis (Wang and Crawford, 1996)....

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“…14 NH 4 ؉ Generation in Roots Morgan and Jackson (1988a, 1988b, 1989 (Lambers et al, 1982;Cooper and Clarkson, 1989). In spite of this possibility, no measurable net transport of endogenous 14 N from roots to shoots occurred during the 3-d exposure to 15 NH 4 ϩ .…”

Section: Source Ofmentioning

confidence: 99%

“…Moreover, after a 5-h pretreatment in 15 NH 4 ϩ solution, the subsequent efflux of 15 NH 4 ϩ to the ambient 14 NH 4 ϩ solution was greater than the initial NH 4 ϩ content of the root (Morgan and Jackson, 1989). Thus, appreciable generation of NH 4 ϩ from endogenous organic N sources accompanies concurrent uptake and assimilation of NH 4 ϩ by roots.…”

mentioning

confidence: 92%

Source and Magnitude of Ammonium Generation in Maize Roots

Volk

Jackson

1998

Plant Physiology

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Short-term studies with 13 NH 4 ϩ have provided estimates of NH 4 ϩ influx, efflux, and cytoplasmic concentration in spruce (Kronzuker et al., 1995a(Kronzuker et al., , 1995b. As the NH 4 ϩ concentration in the external solution increased from 10 to 1500 m, cytosolic NH 4 ϩ levels increased from 2 to 33 mm and efflux increased from 10% to 35% of influx. Similar rates were reported for rice: as external NH 4 ϩ levels increased from 2 to 1000 m, cytosolic NH 4 ϩ levels increased from 3 to 38 mm and efflux rose from 11% to 29% of influx (Wang et al., 1993 ϩ generation in maize roots was estimated to be 50% faster than concurrent NH 4 ϩ uptake (Jackson, et al., 1993). The potential for substantial generation, recycling, and efflux of endogenous NH 4 ϩ in roots is thus indicated.A crucial question raised by these observations is whether protein turnover is the source of endogenous NH 4 ϩ generation, or if recycling of intermediates of the NH 4 ϩ assimilation pathway, such as Gln, is the source. To address this question, maize (Zea mays) seedlings that had been grown on 14 NH 4 ϩ were exposed to highly labeled 15 NH 4 ϩ for 3 d. It was hypothesized that if protein turnover is the source of NH 4 ϩ and if part of this NH 4 ϩ is subject to efflux and translocation to the shoot, a decline in endogenous 14 N protein in the root should occur as new protein is synthesized from the entering 15 NH 4 ϩ . The fact that 15 NH 4 ϩ was applied during six diurnal periods also permitted us to (a) directly measure of the diurnal pattern of NH 4 ϩ fluxes into and out of roots, (b) compare 15 NH 4 ϩ uptake and assimilation by roots during successive light and dark periods, and (c) determine the relationship of the latter processes to carbohydrate levels in shoots and roots. MATERIALS AND METHODS Plant CultureMaize (Zea mays L. cv Pioneer 3320) caryopses were germinated at 30°C in contact with 0.1 mm CaSO 4 . After 30 h, uniform seedlings were selected and their seminal roots excised. Cultures of eight seedlings each were transplanted into 160 L of basal nutrient solution, pH 6.0, containing 0.125 mm (NH 4 ) 2 SO 4 , 1.25 mm K 2 SO 4 , 0.25 mm Ca(H 2 PO 4 ) 2 , 1 mm CaSO 4 , 46 m B, 9 m Mn, 0.8 m Zn, 0.3 m Cu, 0.1 m Mo, and 54 m Fe as ferric diethylenetriamine pentaacetate. The solution was aerated with compressed air that had been washed with H 2 SO 4 and water to remove ambient NH 4 ϩ . A combination of sodium vapor and metal halide lamps provided 1140 E m Ϫ2 s Ϫ1 illumination at canopy height during a 14-h photoperiod (7 am to 9 pm). The average air temperature during the experiment was 23.4°C Ϯ 1.6°C. Both pH and [NH 4 ϩ ] of the nutrient

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Reciprocal Ammonium Transport Into and Out of Plant Roots: Modifications by Plant Nitrogen Status and Elevated Root Ammonium Concentration

Cited by 30 publications

References 0 publications

Rapid, Futile K+ Cycling and Pool-Size Dynamics Define Low-Affinity Potassium Transport in Barley

Rapid, Futile K+ Cycling and Pool-Size Dynamics Define Low-Affinity Potassium Transport in Barley

Major Alterations of the Regulation of Root NO3 − Uptake Are Associated with the Mutation of Nrt2.1 and Nrt2.2 Genes in Arabidopsis

Source and Magnitude of Ammonium Generation in Maize Roots

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