Nitrate Control of Root Hydraulic Properties in Plants: Translating Local Information to Whole Plant Response

Abstract

The sessile lifestyle of plants constrains their ability to acquire mobile nutrients such as nitrate. Whereas proliferation of roots might help in the longer term, nitrate-rich patches can shift rapidly with mass flow of water in the soil. A mechanism that allows roots to follow and capture this source of mobile nitrogen would be highly desirable. Here, we report that variation in nitrate concentration around roots induces an immediate alteration of root hydraulic properties such that water is preferentially absorbed from the nitrate-rich patch. Further, we show that this coupling between nitrate availability and water acquisition results from changes in cell membrane hydraulic properties and is directly related to intracellular nitrate concentrations. Split-root experiments in which nitrate was applied to a portion of the root system showed that the response is both localized and reversible, resulting in rapid changes in water uptake to the portions of the roots exposed to the nitrate-rich patch. At the same time, water uptake by roots not supplied with nitrate was reduced. We believe that the increase in root hydraulic conductance in one part causes a decline of water uptake in the other part due to a collapse in the water potential gradient driving uptake. The translation of local information, in this case nitrate concentration, into a hydraulic signal that can be transmitted rapidly throughout the plant and thus coordinate responses at the whole plant level, represents an unexpected, higher level physiological interaction that precedes the level of gene expression.

LeFRK2 is required for phloem and xylem differentiation and the transport of both sugar and water

“…The hydraulic conductance of tomato root systems was determined by measuring the Xow induced in response to an applied pressure gradient (Gorska et al 2008). Detopped root systems were Wtted with a plastic tube Wlled with DI water and connected to a beaker located on a balance ( §0.01 mg).…”

Nitrate induction of root hydraulic conductivity in maize is not correlated with aquaporin expression

“…Application of NR activity products as a nitrogen source did not enhance water uptake in nitrogen starved plants, suggesting that it is nitrate itself and particularly its in-plant concentration that is involved in the signaling pathway responsible for rapid changes in maize root hydraulic properties. A similar conclusion was drawn from cellular studies of cucumber roots in which tungstate treatment was shown to block nitrate uptake and NR activity but direct injection of nitrate to root cortical cells caused an increase in membrane hydraulic conductivity (Gorska et al 2008).…”

“…Although variation in transpiration rate and stomatal conductance in response to nitrate availability has been observed in a number of crop species (maize, tomato, cotton, barley), this response was mediated by adjustments in root hydraulic properties rather then via direct regulation of stomatal conductivity (Chapin et al 1988;Radin 1990;Radin and Matthews 1989). The sensitivity of root hydraulic resistance to nitrate concentrations Carvajal et al 1996;Ezeta and Jackson 1975;Gloser et al 2007;Horau et al 1996), provides the basis for an alternative scenario in which water Xow is enhanced only to roots exposed to high nitrate levels (Gorska et al 2008). An important outcome of such a local response is that it will magnify the positive eVect of the altered root resistance on total nitrate uptake by prioritizing water uptake from roots exposed to nutrient rich patches.…”

Distribution Profiles and Interrelations of Stomatal Conductance, Transpiration Rate and Water Dynamics in Young Maize Laminas under Nitrogen Deprivation

“…Regulation of transpiration by nitrate may be accomplished by the concerted regulation of root hydraulic conductivity through control of aquaporins, and of stomatal conductance through NO, hormone action and pH [14]. It has been demonstrated [15] that there is interaction between nitrate concentration in the nutrient solution and root hydraulic properties. This interaction adjusts water uptake and the link between resoursce availability and the hydraulic adjustments provides appropriate dynamic responses at the whole plant level.…”