Compartmental analysis of sulphate transport in Lemna minor L., taking plant growth and sulphate metabolization into consideration

Thoiron, A.; Thoiron, Bernard; Demarty, Mauríce; Thellier, Michel

doi:10.1016/0005-2736(81)90054-7

Cited by 27 publications

(20 citation statements)

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“…But at the same time as it increases the complexity ofthe kinetics, a metabolic compartment provides extra access to the system since it can be sampled independently. Thus, future studies of the metabolism and transport of sulfur will combine measurements of the changes of 3S in organic compounds (as made by Giovanelli et aL, 13) with measurements of influx and efflux kinetics as in the present paper and in that ofThoiron et aL (27). From these measurements, chemical as well as physical flows of S will be calculable.…”

Section: Discussionmentioning

confidence: 76%

“…Preliminary attempts with carrot root tissue to see whether the lag in the build up of 3S in organic S corresponded to that predicted from the value of kc, obtained from washout measurements failed because of the variability of the tissue. It seems appropriate to recall once again the necessity for doing such experiments at or very near a steady state (4,29,31), as has been emphasized in recent work on So0 and sulfur transport and metabolism (13,27). If the system is not at a steady state, then there is no a priori basis for interpreting exchange kinetics.…”

Section: Discussionmentioning

confidence: 99%

“…treated in inactive solution (as above), then placed in a solution of the same chemical composition but containing 35so42-to label cellular s042-and organic S pools, and finally transferred to successive aliquots of unlabeled solution of the same composition. All 3S flowing to the external solution would be as s042- (27). An example of the time course of loss of 3S to the external solution is shown in Figure 1.…”

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Characteristics of Sulfate Transport Across Plasmalemma and Tonoplast of Carrot Root Cells

Cram¹

1983

Plant Physiol.

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Compartmental analysis of "SO4-2 exchange kinetics is used to obtain S042-fluxes and compartment contents in carrot (Daucus carota L.) storage root cells, where 2 to 5% of the S042-taken up is reduced to organic form. The necessary curve fit is verified by (a) consistency between 'content versus time' and 'rate versus time' plots of washout data; (b) agreement between loading and washout kinetics; and (c) correct identification of the fastest exchange phase as being from extracellular spaces.Sulfate is actively transported up an electrochemical potential gradient at both plasmalemma and tonoplast. The plasmalemma influx is from 2 to 10 times higher than the tonoplast Influx, is much greater than the S042 reduction rate, and would not lmit the rate of either. This is consistent with the finding that the plasmie a influx is not regulated by internal S042-or cysteine (Cram 1982 Plant Sci Lett, in press Sulfate is the second most abundant of the elements which are taken up as ions and metabolized (nitrogen being the most abundant) (8). Understanding the mechanism and control of its uptake in relation to long distance transport, storage and mobility (20, 28), nutrient balance (11,24), and metabolism (1, 13, 14, 24) in plants demands that fluxes of S042-and of organic S compounds across individual cell membranes and between metabolites should be measured. In particular, in the vacuolated higher plant cell, the kinetics and regulation of s042-flows across the plasmalemma and subsequently either to the vacuole or to reductive assimilation products can only be studied using such measurements. This paper provides an experimental justification of the use of compartmental analysis of 'S exchange for estimating fluxes in carrot storage root cells. The method is then used to obtain thermodynamic and kinetic characteristics of S042-transport in these cells, and the implications for the rate limitation and control of So02-accumulation and metabolism are discussed.The first destination of s042-after uptake across the plasmalemma is reductive assimilation. In nonvacuolated bacteria, as in vacuolated fungi and higher plants, it has been shown that reductive assimilation is self-regulated by negative feedback from products of s042-metabolism. Cysteine, for instance, feeds back to the first enzyme of s042-metabolism, ATP sulfurylase (which catalyzes the production of 'activated SO2-,' which in tUn is reduced in a sequence of reactions to S2-and then converted to cysteine, etc.) (1, 21). In bacteria, the study of mutants has shown, further, that this negative feedback also extends to the uptake of S042-across the plasmalemma, so that the uptake and reduction of S042-are to some extent matched (1,7,21). Similar control of s042-influx across the plasmalemma in higher plant cells has also been claimed (15,23,24), although without supporting measurements of the plasmalemma influx.A priori, such a tight regulation of s042 influx across the plasmalemma in vacuolated cells seems unlikely. If s042-uptake were matched to S042 reduct...

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Section: Discussionmentioning

confidence: 76%

Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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Characteristics of Sulfate Transport Across Plasmalemma and Tonoplast of Carrot Root Cells

Cram¹

1983

Plant Physiol.

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“…For use with intact plant material, a detailed treatise on parameter extraction was presented by Jeschke and Jambor (1981) and Jeschke (1982). More recently, compartmental analysis has also been applied to metabolized ions, including S0,2p (Thoiron et al, 1981;Cram, 1983; Bell et al, 1994), Pi (Lefebvre and Clarkson, 1984;Macklon and Sim, 1992), NO,-(Presland and McNaughton, 1984 1986; Macklon et al, 1990;Siddiqi et al, 1991;Devienne et al, 1994;Kronzucker et al, 1995a Kronzucker et al, , 1995b, and NH,+ (Presland and McNaughton, 1986;Cooper et al, 1989;Macklon et al, 1990;Wang et al, 1993a;Kronzucker et al, 1995~). Despite this widespread use of the technique, workers have typically neglected to conduct physiological tests to verify the subcellular identities of the phases revealed in efflux data.…”

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confidence: 99%

“…For use with intact plant material, a detailed treatise on parameter extraction was presented by Jeschke and Jambor (1981) and Jeschke (1982). More recently, compartmental analysis has also been applied to metabolized ions, including S0,2p (Thoiron et al, 1981;Cram, 1983;Bell et al, 1994), Pi (Lefebvre and Clarkson, 1984;Macklon and Sim, 1992), NO,- (Presland and McNaughton, 1984;Lee and Clarkson, The work reported in this paper was supported by a National Sciences and Engineering Research Council of Canada grant to A.D.M.G. and by a University of British Columbia Graduate Fellowship to H.J.K.…”

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confidence: 99%

Analysis of 13NH4+ Efflux in Spruce Roots (A Test Case for Phase Identification in Compartmental Analysis)

1995

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111. Based on these findings and the assumption of an in-series arrangement of root cell compartments, it was concluded that phase 111 corresponded to the cytoplasm, phase II corresponded to the Donnan free space, and phase I corresponded to a film of solution adhering to the root surface.Efflux analysis is widely used to determine unidirectional ion fluxes, kinetic exchange constants of subcellular compartments, and ionic concentrations within compartments. In plants, compartmental analyses have been undertaken for a variety of ions, including Na+, K+, Mg2+, Ca2+, NH,+, NO,-, Pi, SO,'-, C1-, and Br-(for refs., see Wang, 1994). The majority of efflux studies have been limited to nonmetabolized ions and were performed usually on excised tissues or suspension-culture systems, mainly because of the (presumed) absence of complicating factors such as metabolism and long-distance transport to the shoot (Pitman, 1963; Cram, 1968;Poole, 1971aPoole, , 1971b Macklon, 1975a, 197513; Sim, 1976, 1981;Pfriiner and Bentrup, 1978;Macklon et al., 1990). For use with intact plant material, a detailed treatise on parameter extraction was presented by Jeschke and Jambor (1981) and Jeschke (1982). More recently, compartmental analysis has also been applied to metabolized ions, including S0,2p (Thoiron et al., 1981;Cram, 1983; Bell et al., 1994), Pi (Lefebvre and Clarkson, 1984;Macklon and Sim, 1992), NO,-(Presland and McNaughton, 1984 1986; Macklon et al., 1990;Siddiqi et al., 1991;Devienne et al., 1994;Kronzucker et al., 1995a Kronzucker et al., , 1995b, and NH,+ (Presland and McNaughton, 1986;Cooper et al., 1989;Macklon et al., 1990;Wang et al., 1993a;Kronzucker et al., 1995~). Despite this widespread use of the technique, workers have typically neglected to conduct physiological tests to verify the subcellular identities of the phases revealed in efflux data. As a consequence of this omission, the assignment of particular kinetically defined phases to their corresponding subcellular compartments has not always been unequivocal (Macklon et al., 1990). Only in studies by Cram (1968), Lee and Clarkson (1986), and Siddiqi et al.(19911, as well as in a previous study of NO,-exchange in spruce (Kronzucker et al., 1995a), was the assignment of compartments substantiated. Usually phase assignment has been based on the assumption of an in-series arrangement of cell compartments, i.e. cell wall, cytoplasm, and vacuole (Pitman, 1963; Cram, 1968Cram, , 1975. Thus, the first (rapidly exchanging) phase has been assumed to represent the cell wall and the last (slowest exchanging) phase has been assumed to represent the vacuole. However, the derivation of flux components as well as of pool sizes from efflux data is valid only if subcellular compartments are assigned correctly to their corresponding efflux phases.We have used a combination of strategies to analyze the efflux reported in the present study to distinguish between membrane-bound and metabolically dependent (intracellular) compartments and those that are nonmembrane bound and app...

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Sulfur and plant ecology: a central role of sulfate transporters in responses to sulfur availability

Hawkesford

2007

Plant Ecophysiology

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Compartmental analysis of sulphate transport in Lemna minor L., taking plant growth and sulphate metabolization into consideration

Cited by 27 publications

References 10 publications

Characteristics of Sulfate Transport Across Plasmalemma and Tonoplast of Carrot Root Cells

Characteristics of Sulfate Transport Across Plasmalemma and Tonoplast of Carrot Root Cells

Analysis of 13NH4+ Efflux in Spruce Roots (A Test Case for Phase Identification in Compartmental Analysis)

Sulfur and plant ecology: a central role of sulfate transporters in responses to sulfur availability

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