H⁺extrusion and organic‐acid synthesis in N₂‐fixing symbioses involving vascular plants

Abstract

SUMMARY An analysis of published data suggests that the N2‐fixing symbiotic vascular plants extrude more H+ per unit N fixed than would be expected from data on the same genotypes growing on NH4+ if the plants had the same chemical composition when grown on the two N sources. The H+/N ratio with urea as the N source is similar to that with N2. The higher H+/N ratio and higher organic acid/N ratio with N2 or urea as N source implies higher whole‐plant energy and water costs per unit of biomass and, ultimately, inclusive fitness, produced. The rhizosphere acidification resulting from H+ extrusion may serve to change rhizosphere pH to some ‘optimal’ value, and to increase the availability of such limiting resources as P, Mo and Fe which are especially needed in diazotrophy. Data in the literature are consistent with these possibilities in the few cases examined. Within the plant, data on xylem and phloem sap composition in conjunction with shoot composition, of diazotrophically‐growing legumes suggest that shoot acid‐base homoiostasis can be maintained via the import of appropriate solutes in the xylem and the export of appropriate solutes in the phloem. Acid‐base regulation of the nodules in the absence of any H+ exchange with their environment can also probably be explained in terms of the solutes supplied in the phloem and exported in the xylem. This conclusion is based on data in the literature on the composition of stem phloem sap and of xylem sap exuding from detached nodules of diazotrophic vascular plants. These considerations do not exclude the possibility of net H+ efflux from nodules fixing N2 in contact with an aqueous medium. The limited data available are consistent with extrusion of some of the H+ generated in nodules as an alternative to their neutralization by metabolism of organic anions entering in the phloem. Such H+ extrusion by nodules could aid in their acquisition of Fe from the medium, albeit not always at a phase in the life or the nodule when there is a net requirement for Fe.

Factors affecting soil acidification under legumes. III. Acid production by N2‐fixing legumes as influenced by nitrate supply

“…However, when NO $ − is the source of N, anion uptake predominates and the roots excrete OH − (Tang, 1997). The acid generated by N # -fixing legumes has been suggested to range from 0.2 to 1.6 mol H + mol −" N fixed whereas the uptake and assimilation of one mole of NH % + is associated with the excretion of 1.1-1.6 mol of H + (Raven et al, 1990). By contrast, the uptake and assimilation of NO $ − involve OH − efflux or H + influx.…”

Terrestrial rhizophytes and H+ currents circulating over at least a millimetre: an obligate relationship?

“…low M^ organic anion salt occurs are, on the basis of present knowledge, the bryophytes and tracheophytes (Raven, 1984a(Raven, , 1987a(Raven, , 6, 1988a(Raven, , 1989; increased organic anion salt accumulation with rhizosphere acidification in response to nutrient deficiencies are known to occur for iron deficient non-graminaceous terrestrial flowering plants, and for phosphorus-deficient terrestrial fiowering plants (Raven, 1987a;Raven et al, 1990a). Among the rhizophytic algae, constitutive organic anion ac--cumulation is known to be minimal in the Characeae (Charophyceae): Raven (1984aRaven ( , 1987aRaven ( , 6, 1988aRaven ( , 1989.…”

“…While not themselves generating currents, the presence of these symbionts has several implications for the circulating H^ currents generated by the host (see Miller et al, 1986;Raven, 19886;Raven et al, 1990a).…”

“…1). The acidified sub-apical zones into which H"^ efflux occurs can increase the availability of phosphate for plants growing in low phosphate, relatively alkaline soils, while iron availability is increased for vascular land plants (other than grasses) by H"*^ excretion accompanied by surface reductase activity and excretion of organic acids and reductants (Raven et al, 1990a). Evidence that the alkaline apical rhizosphere acts as suggested by Raven el al (1990 a) in increasing molybdenum availability is currently only available from the correlation of increased molybdenum availability with decreased bulk soil pH; further investigations are under way.…”

“…The alkaline apex may also function as a means of protecting the dividing cells from toxic levels of aluminium in relatively acid bulk soil (Haussling et al, 1985). It is important to note that the H^ circulations related to electric current flow are superimposed on (i) any net H^ flux between the cell or organ and its environment related to acid-base regulation as a function of nitrogen source for growth and the way that the plant disposes spatially of nitrate assimilation, and (ii) net H^ efflux resulting from additional organic acid synthesis followed by H*-cation exchange attendant on phosphorus or iron deficiency (Raven, 1987a;Raven et al, 1990a). H"^ recirculation thus represents an energyefficient alternative to the net H* efflux associated with organic acid synthesis as a means of acidifying a part of the rhizosphere (regardless of the nitrogen source: Raven, 1987a), with the additional potential benefit of an alkalinized root zone with respect to molybdenum acquisition and reduction in aluminium toxicity.…”