Research

Quantifying the contribution of mass flow to nitrogen acquisition

by an individual plant root
Ross E. McMurtrie1 and Torgny N€asholm2
1
School of Biological, Earth and Environmental Sciences, The University of New South Wales, Sydney, NSW 2052, Australia; 2Department of Forest Ecology and Management, Swedish
University of Agricultural Sciences, Ume
a SE-901 83, Sweden

Summary
Author for correspondence:
The classic model of nitrogen (N) flux into roots is as a Michaelis–Menten (MM) function of
Ross E. McMurtrie soil-N concentration at root surfaces. Furthermore, soil-N transport processes that determine
Tel: +61 425306272
soil-N concentration at root surfaces are seen as a bottleneck for plant nutrition. Yet, neither
Email: r.mcmurtrie@unsw.edu.au
the MM relationship nor soil-N transport mechanisms are represented in current terrestrial
Received: 18 July 2017 biosphere models.
Accepted: 24 October 2017

Processes governing N supply to roots – diffusion, mass flow, N immobilization by soil
microbes – are incorporated in a model of root-N uptake. We highlight a seldom considered
New Phytologist (2018) 218: 119–130 interaction between these processes: nutrient traverses the rhizosphere more quickly in the
doi: 10.1111/nph.14927 presence of mass flow, reducing the probability of its immobilization before reaching the root
surface.

Root-N uptake is sensitive to the rate of mass flow for widely spaced roots with high N
Key words: diffusion, mass flow, nitrogen
(N) immobilization, nitrogen uptake model, uptake capacity, but not for closely spaced roots or roots with low uptake capacity. The results
rhizosphere processes, root–microbe point to a benefit of root switching from high- to low-affinity N transport systems in the pres-
competition, root-nitrogen uptake, soil- ence of mass flow.
nitrogen transport.
Simulations indicate a strong impact of soil water uptake on N delivery to widely spaced
roots through transpirationally driven mass flow. Furthermore, a given rate of N uptake per
unit soil volume may be achieved by lower root biomass in the presence of mass flow.

progress on their integration into whole-plant models (Warren

Introduction
Although the molecular underpinnings of plant-nitrogen (N)
uptake and metabolism and soil turnover of N have been studied
extensively, the actual processes by which plants acquire N from the
soil are still poorly understood. This is in spite of the notion that
soil-N transport processes, diffusion and mass flow, may constitute
the bottleneck for plant nutrition (Nye, 1977). The separation of
plant-N acquisition by diffusion and by mass flow is inherently
problematic, both conceptually and experimentally, and attempts
to quantify the contribution of each process have arrived at more or
less contrasting conclusions. Nevertheless, the potential ramifica-
tions of plant-N acquisition via diffusion or via mass flow are far
reaching and include effects as diverse as plant inter- and intra-
species competition, plant allocation optimization, plant water-use
efficiency and growth responses to CO2 and N fertilization.
Ideally, models of root-N uptake should simulate processes
operating on fine spatial scales that control N flux into roots from
surrounding soil – processes such as solute movement to roots
through diffusion and mass flow, competition for N between
plant roots and soil microbes, and kinetics of root-N uptake.
Although seminal models of these rhizosphere processes were
published and tested decades ago (Nye & Marriott, 1969; Barber
& Cushman, 1981; Tinker & Nye, 2000), there has been limited
et al., 2015). This shortcoming is illustrated by current terrestrial
biosphere models (TBMs) (Zaehle et al., 2014), few of which
simulate N uptake by spatially distributed root systems, only one
of which simulates mass flow (Gerber et al., 2010) and none of
which simulates all the above rhizosphere processes. Conse-
quently, root-N uptake is crudely represented in current TBMs
and, in particular, linkages between plant-N uptake and water
uptake are overlooked.
The question ‘Is root-N uptake sensitive to the rate of root
water uptake?’ is the focus of this article. As stated above, past
attempts to answer this question through modelling have arrived
at conflicting conclusions. Whereas some models suggest a poten-
tial synergistic interaction between water and N uptake (Barber,
1995; Leadley et al., 1997), others arrive at the conclusion that
there should be no benefit of mass flow caused by root water
uptake on N acquisition (Yanai, 1994; Darrah et al., 2006;
BassiriRad et al., 2008). Experimental support for a role of tran-
spirationally induced N gains by plants comes from a diverse
range of studies. Cramer et al. (2008) reported increased transpi-
ration by Enhartia calycina plants that could not access N through
direct interception/diffusion, and interpreted this as plants using
transpiration as a means to acquire N. Matimati et al. (2014)
showed that transpiration increased (and water-use efficiency

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decreased) in Phaseolus vulgaris when mesh prevented roots from
accessing N through interception/diffusion. Recently, a new tech-
nique for the study of soil-N fluxes supported the notion that
mass flow leads to increased soil-N fluxes (Oyewole et al., 2014).
The effect of mass flow is investigated here using a new model
of competition for available soil-N between plant roots and soil
microbes. Microbial N uptake occurs continuously as nutrient is
transported to root surfaces at which plant-N uptake occurs. The
model addresses a seldom considered interaction – in the pres-
ence of mass flow, nutrient is transported more quickly to root
surfaces, reducing the probability of its immobilization by soil
microbes before reaching the root surface. We utilize an estab-
lished model of N transport by mass flow and diffusion (Barber
& Cushman, 1981). Root-N influx is a Michaelis–Menten
(MM) function of solute concentration at the root surface (cso).
Solution of the N transport equation yields a second equation for
root-N influx as a function of cso. These two relationships will be
portrayed as the root’s N demand and N supply equations,
respectively. The formulation of root-N uptake in terms of equa-
tions for root-N demand and soil-N supply to the root surface
provides a powerful graphical tool for unpacking soil and root
processes that jointly determine root-N uptake.
A further relationship that emerges is an equation for the parti-
tioning of soil-N uptake between roots and soil microbes. The
root-N uptake fraction, defined as the proportion of available soil-
N taken up by roots from unit soil volume, is shown to range
between zero in the extreme of very widely spaced roots and unity
in the extreme of very closely spaced roots. The explanation for this
variation is that, as root spacing decreases, the distance traversed by
nutrient to reach the root surface shortens, and the probability of
N immobilization by soil microbes before reaching the root surface
decreases. The root-N uptake fraction is thus an increasing func-
tion of rooting density. For related reasons, the N uptake fraction
is also an increasing function of the root’s water uptake – the effect
of water uptake is to reduce the time for nutrient to traverse the dis-
tance to the root surface, and hence to decrease the probability of
microbial N immobilization. Several published rhizosphere models
have considered both mass flow and microbial immobilization of
soil-N (Somma et al., 1998; Gerber et al., 2010; Grant et al.,
2010), but none has focused specifically on how mass flow associ-
ated with plant transpiration may benefit plants in their competi-
tive contest with soil microbes for bio-available N. Equations for
the N uptake fraction, root-N supply and N demand are presented
in the next section, and utilized to ascertain whether and when
mass flow makes a significant contribution to root-N uptake.
Description
Model of N uptake by an individual root
This section presents equations for root-N uptake derived from
the Barber–Cushman (BC) model of solute transport in the
rhizosphere, represented as a cylindrical volume of soil sur-
rounding an individual root (Barber & Cushman, 1981). Our
model simulates the balance between the supply of plant-
available N and losses associated with its uptake by plant roots
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and soil microbes and other mechanisms. As a first approxima-
tion, we assume that soil microbes are uniformly distributed
through the rhizosphere and that soil-N is supplied at a con-
stant rate (S, g N m3 d1), cf. Leadley et al. (1997). Nutrient
uptake by soil microbes is commonly represented as an MM
function of solute concentration at soil microsites (Kuzyakov
& Xu, 2013; Zhu et al., 2017). We make the simplifying
assumption that solute concentrations are lower than the MM
coefficient for microbial uptake (Lipson & N€asholm, 2001;
Kuzyakov & Xu, 2013), so that microbial N uptake at any
point in the rhizosphere is approximately proportional to the
local solute concentration. Assuming that other losses, for
example through chemical transformations, occur at constant
rates (Corbeels et al., 2005; Grant et al., 2010), total N loss
can be represented by a single rate parameter m (d1). Experi-
ments monitoring the immobilization of N added to boreal
forest soil indicate that the time constant for soil-N immobi-
lization is of the order of several days (Blasko et al., 2013;
Inselsbacher et al., 2014). Representation of soil-N dynamics as
a balance between input at a constant rate and immobilization
governed by a single rate parameter is a gross simplification of
the complex soil–microbial interactions that operate in plant
rhizospheres (Schimel & Bennett, 2004; Frank & Groffman,
2009). An advantage of making these simplifying assumptions
is that they enable us to derive analytical expressions for root-
N uptake – analytical solutions of special cases are valuable as
precursors to (numerical) solution of the full model (Mahajan,
2014).
Our objective is to derive equations for N uptake per unit soil
volume u (g N m3 d1), which equals the flux of nutrient into
roots j (g N m2 d1) multiplied by the root surface area per unit
soil volume:
u ¼ 2pro lr j; Eqn 1
where ro (m) is the root radius and lr (m2) is the root length
density. Parameter definitions are given in Table 1. The influx j is
an active process, with proton coupling providing the energy
required to drive the process (e.g. Wang et al., 2012). Root
uptake patterns resemble enzyme kinetics (Epstein & Hagen,
1952) and can thus be described using the tools developed by
Michaelis & Menten (1913), in which the efficiency of the active
component (the root cell transporter) is, by convention, the soil
solution concentration that corresponds to half the maximal rate
of transport (substrate conversion), and the capacity for transport
is the conversion rate at infinite concentration. Thus, j is com-
monly represented as an MM function of solute concentration at
the root surface cso (g N m3) (Kuzyakov & Xu, 2013):
jrmax
j¼ ; Eqn 2
1 þ jrmax =kcso
where jrmax (g N m2 d1) is the maximum root-N influx and k
(m d1), the initial slope of the jcso relationship, is the so-called
root absorbing power for nutrient. Equation 2, which expresses j
as a function of cso, represents an equation for root-N demand.
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A second equation for j as a function of cso, representing the sup-


1d dcs ro v o dcs
ply of solute to the root, can be derived from the BC model as fol- Sþ rDb þ ¼ mcs for ro \r\rx ;
r dr dr r dr
lows. The BC model simulates the radial movement of solute
through mass flow and diffusion down a concentration gradient Eqn 4
generated by uptake at the root surface over radial distances r
extending from the root surface ro to a distance rx (m), the half- where vo (m d1) is the velocity of water at the root surface, D
distance to the nearest neighbouring root (assuming radial symme- (m2 d1) is the effective diffusion coefficient of nutrient in the
try). For a regular array of parallel roots, rx is related to the root soil and b is the buffer power of the soil (b = dc/dcs, where c is the
length density lr: concentration of total diffusible nutrient). The product Db in
Eqn 4 represents the diffusion coefficient of solute. The solution
1 of Eqn 4 is subject to boundary conditions at r = ro and rx. The
lr ¼ : Eqn 3 former boundary condition requires that the root-N influx j,
pðrx  ro 2 Þ
2
given by Eqn 2, is equal to the flux of solute arriving at the root
The radial distribution of solute concentration at steady state surface through mass flow jMF and diffusion jDF:
cs(r) satisfies the following differential equation, derived in Sup-
porting Information Notes S1: j ¼ jMF þ jDF ; Eqn 5a

Table 1 Symbol definitions and units used in the model

Symbol Definition and source (relevant equation or figure or table) Units

b Buffer power of soil, (4) –

cs(r), Cs(R) Steady-state solute concentration as function of radial distance r, dimensionless solute concentration as g N m3, –
function of dimensionless radial distance R, (4), (Supporting Information Notes S1.5)
cs(r, t), Cs(R,T) Time-dependent radial distribution of solute concentration, dimensionless time-dependent radial g N m3, –
distribution of solute concentration, (8), (Notes S2.2)
cso, Cso Solute concentration at root surface, dimensionless solute concentration at root surface, (2), g N m3, –
(Notes S1.8)
csomax, Csomax Maximum solute concentration at the root surface, dimensionless maximum solute concentration at g N m3, –
the root surface, (Notes S1.29), (Notes S1.29)
D Effective diffusion coefficient of nutrient in soil, (4) m2 d1
E Daily water extraction by roots from unit soil volume, (13) m3 water m3 soil
volume d1
gN, GN Rhizosphere conductance for solute, dimensionless rhizosphere conductance for solute, (7), m d1, –
(Notes S1.26)
j, Jr Root-nitrogen (N) influx, dimensionless root-N influx, (2), (10) g N m2 d1, –
jDF, JDF Root-N influx associated with diffusion, dimensionless root-N influx associated with diffusion, (5a), g N m2 d1, –
(Fig. 2a)
jMF, JMF Root-N influx associated with mass flow (= j  jDF), dimensionless root-N influx associated with mass g N m2 d1, –
flow (= Jr  JDF), (5a), (Fig. 2a)
jrmax, Jrmax Maximum root-N influx, dimensionless maximum root-N influx, (2), (Table 2) g N m2 d1, –
jsmax, Jsmax Maximum soil-N flux at root surface, dimensionless maximum soil-N flux at root surface, (7), (12) g N m2 d1, –
k Root absorbing power for nutrient, (2) m d1
Km Michaelis–Menten coefficient, (Table S1) g N m3
lr Root length density, (3) m root m3 soil volume
m Rate of solute loss through immobilization by soil microbes and other losses, (4) d1
r, R Radial distance from centre of root, dimensionless radial distance, (4), (Notes S1.6) m, –
rm N immobilization distance, (Table 2) m
ro, Ro Fine root radius, dimensionless fine root radius, (1), (Table 2) m, –
rx, Rx Half inter-root distance, dimensionless half inter-root distance, (3), (Notes S1.7) m, –
Rr Uptake : diffusion ratio, (Table 2) –
Rv Mass flow : diffusion ratio, (Table 2) –
S Rate of supply of diffusible solute per unit soil volume, (4) g N m3 d1
t, T Time, dimensionless time, (8), (Notes S2.1) d, –
u Rate of N uptake by individual root per unit soil volume, (1) g N m3 d1
vo, v(r) Radial velocity of water at the root surface, and at radial distance r, (4), (13) m d1, m d1
Vr Root volume density (root volume per unit soil volume), (Table 2) –
/, /max N uptake fraction, upper limit to N uptake fraction based on maximum root-N influx and maximum –, –
soil-N supply to roots, (9), (12)
sd, su, sv Timescale for nutrient to disperse a distance ro by diffusion, timescale for uptake of nutrient within one d, d, d
radial distance ro of the root surface, timescale for accumulation of nutrient adjacent to the root sur-
face through mass flow (Notes S3)

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where radial distributions evolve over time when the water uptake veloc-
ity at the root surface switches at time t = 0 from zero to a con-
jMF ¼ v o cso ; Eqn 5b stant, non-zero, rate vo.
Our next modelling objective is to derive a general equation for
and steady-state N uptake per unit soil volume (u, Eqn 1). Before
 doing so, we consider the solution in the absence of soil-N
dcs  immobilization. By setting m = 0 and r = rx and substituting
jDF ¼ Db  : Eqn 5c
dr ro equations for the outer boundary condition (Eqn 6), u (Eqn 1)
and lr (Eqn 3) into the N balance equation (Eqn S1.3), we find
The second boundary condition is that solute transport is zero that, in the absence of microbial immobilization, the solution is
at r = rx: u = S (i.e. root-N uptake equals N input, cf. Leadley et al., 1997).
 This result means that, in the absence of soil microbial immobi-
ro dcs  lizers, N uptake will be independent of all parameters other than
v o cs ðrx Þ þ Db  ¼ 0; Eqn 6
rx dr rx S. In particular, root-N uptake will be independent of water
uptake, which is proportional to vo, unless N immobilization is
which amounts to assuming that solute located at r = rx is equally incorporated in the model.
likely to move either towards the root or away from it. In the presence of microbial N immobilization, that is when m
Our objective is to derive an equation for j as a function is non-zero, we expect to find u < S. The solution for u, which is
of cso from Eqns 4–6, without imposing the boundary condi- obtained by substituting the above solution for j into Eqn 1, can
tion at the root radius (Eqn 2). Equation 5 constitutes an be written as a function of five dimensionless (scale-independent)
equation for j as a function of cso, except for the term dcs/dr parameter combinations, Rr (uptake : diffusion ratio), Rv (mass-
(ro). However, dcs/dr(ro) can be expressed as a linear function flow : diffusion ratio), Vr (root volume density), Ro (dimension-
of cso with negative slope (Notes S1). The slope is negative less root radius) and Jrmax (dimensionless N uptake capacity),
because, if the solution of the transport equation (Eqn 4) is which are defined in Table 2:
constrained by the zero transfer boundary condition at r = rx
(Eqn 6), but not by the boundary condition at r = ro (Eqn 2), u ¼ S  /ðRr ; Rv ; Vr ; Ro ; Jrmax Þ: Eqn 9
a steepening of the concentration gradient at the root surface
necessitates a reduction in cso. Equation 5a can then be writ- The function / = u/S represents the N uptake fraction, that is
ten as an equation for the supply of solute to the root surface the proportion of bio-available soil-N taken up annually by the
in the form: root. The solution for / is presented in Notes S1. The parameter
combinations are explained in Table 2 and Notes S3. In
j ¼ jsmax  g N cso ; Eqn 7 Notes S3, we argue for the inclusion of the dimensionless param-
eter combinations in root trait databases (Iversen et al., 2017). It
where jsmax (g N m2 d1) is the maximum soil-N flux at the root should be noted that Eqn 9 does not imply that N uptake is pro-
surface and the slope gN (m d1) can be regarded as the rhizo- portional to the supply rate S because one of the dimensionless
sphere conductance for solute. Equations for jsmax and gN are parameter combinations Jrmax depends on S. The N uptake frac-
given in Notes S1. They depend on the N input rate S, transport tion can also be expressed as
parameters D, b and vo, root spacing rx and immobilization rate
m. The N demand and N supply equations (Eqns 2 and 7, 2pro lr j
/¼ ¼ 2Vr Jr ; Eqn 10
respectively) are then equated and solved for cso and j at steady S
state.
Before achieving steady state, the radial nutrient distribution is where Jr is the dimensionless root-N influx:
time dependent. Time-dependent solute concentration cs(r, t)
j
satisfies the reaction diffusion equation Jr ¼ : Eqn 11
ro S


oc ocs ro v o ocs 1 o ocs
¼b ¼ S  mcs þ þ rDb Values of maximum root-N influx (jrmax, Eqn 2) and maxi-
ot ot r or r or or Eqn 8
for ro \r\rx ; 0\t \1; mum soil-N supply (jsmax, Eqn 7) set upper limits to the N
uptake fraction:
where t represents time (Nye & Marriott, 1969; Barber & Cush-
man, 1981). This partial differential equation can be derived 2pro lr
/max ¼ minðjrmax ; jsmax Þ ¼ 2Vr minðJrmax ; Jsmax Þ;
from the conservation of mass (e.g. Barber & Cushman, 1981). S
In order to solve Eqn 8, initial values cs(r, 0) are required for Eqn 12
ro ≤ r ≤ rx. Boundary conditions at r = ro and r = rx (Eqns 5, 6) are
satisfied at all times. Equation 8 is solved using the Crank–Nicol- where Jsmax (= jsmax/roS) is the dimensionless maximum soil-N
son method (Farlow, 1993) – see Notes S2 – to investigate how supply at the root surface.

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Table 2 Explanation of composite parameters defined in the solution for the nitrogen (N) uptake fraction (Eqn 9) (further explanation is given in Supporting
Information Notes S3)

Symbol Name and units Definition Explanatory notes

ro k
Rr Uptake : diffusion ratio Root absorption rate divided by diffusive rate. If Rr » 1, root absorbing power for N is strong,
Db
(dimensionless) and nutrient close to the root surface is likely to be taken up by the root. Strong pulling power
of the root depletes nutrient concentrations adjacent to the root surface, leading to a steep
concentration gradient that draws nutrients towards the root surface by diffusion. If Rr « 1,
root absorbing power for N is weak, and nutrient close to the root at any time is more likely
to diffuse away before uptake can occur
ro vo
Rv Mass flow : diffusion Advective transport rate divided by diffusive rate. Its value characterizes the contribution of
Db
ratio (dimensionless)  2  mass flow to the flux of nutrient arriving at the root surface
Vr Root volume density pro2 lr ¼ 1= rrox 2  1 Root volume per unit soil volume (root length density multiplied by root cross-sectional area)
(dimensionless) qffiffiffiffiffi
Db
rm N immobilization m Root-mean-square distance of nutrient dispersal by diffusion on the timescale for N
distance (cm) qffiffiffiffiffi immobilization by soil microbes
Ro Dimensionless root radius ro = Db
m Root radius relative to the N immobilization distance
qffiffiffiffi
ffi
Rx Dimensionless half inter- rx = Db
m Half inter-root distance relative to the N immobilization distance
root distance
jrmax
Jrmax Dimensionless root-N ro S Maximum N uptake rate relative to the rate of N input within radial distance ro of the root
uptake capacity

Daily water uptake per unit soil volume (E, m3 wa-
ter m3 soil d1) is the product of the root surface area (2prolr)
and the water uptake velocity (vo):
2Db
E ¼ 2pro lr v o ¼ Vr Rv ¼ 2prlr vðrÞ;
ro 2
where v(r) is the velocity of water at radial distance r.
Model parameterization
In line with our aim for a general equation for N uptake as a
function of dimensionless parameter combinations (Rr , Rv ,
Vr, Ro, Jrmax), we parameterize the model for a generic plant
species, rather than for a particular species. Values of
uptake : diffusion ratio (Rr , Table 2) can range widely from
considerably less than unity to considerably larger than unity
(Table S1). In the simulations below, we consider values
Rr = 0.2, 1 and 5, representing low, intermediate and high
uptake : diffusion ratio. We show simulations with Rv = 0 and
0.4. The term (rovo = E/2plr, Eqn 13) in the numerator of Rv
(Table 2) can be estimated from whole-plant transpiration and
the root length active in the absorption of soil water. When
the assumption is made that vo is the same for all roots, val-
ues obtained for Rv tend to be considerably less than unity
(Leadley et al., 1997; Darrah et al., 2006; BassiriRad et al.,
2008). However, the assumption of uniform vo is not sup-
ported by evidence that the root water uptake capacity, root
hydraulic conductivity and aquaporin activity vary consider-
ably on the scale of individual fine roots and across fine root
orders (Gorska et al., 2008; Rewald et al., 2012; Gambetta
et al., 2013; Li et al., 2016; Wang et al., 2016). Values of Rv
may therefore be considerably higher for a subset of fine roots
with enhanced capacity for resource acquisition, called absorp-
tive fine roots (McCormack et al., 2015). The parameter com-
bination Ro is fixed at Ro = 0.02. Jrmax is given values of 500,
1000 and 2000. The root volume density Vr assumes values
of 0.0001 and 0.0016 for widely and closely spaced roots,
respectively.
We show simulations of the partial differential equa-
tion (Eqn 8) with the following values of dimensionless parame-
Eqn 13
ter combinations: Rr = 0.2, 1 and 5, Rv = 0 and 0.4, Ro = 0.02,
Vr = 0.0001 and Jrmax = 2000. It is instructive to determine values
of the model’s nine parameters (ro, rx, k, jrmax, vo, D, b, m, S) that
give these values of the dimensionless parameter combinations.
As an example, consider the uptake of a mobile ion, such as
nitrate, by fine roots with radius ro = 0.02 cm, N immobilization
rate m = 0.05 d1, b = 1, D = 0.05 cm2 d1 (values that give
Ro = 0.02), S = 0.014 g N m3 d1 (value that gives a steady-state
solute concentration in the absence of roots S/m =
20 lM = 0.28 g N m3), root absorbing power k = 2.5 cm d1
(value that gives Rr = 1), maximum root-N influx
jrmax = 0.0056 g N m2 d1 (value that gives Jrmax = 2000) and
root water velocity at the root surface vo = 0 and 1 cm d1 (value
that gives Rv = 0.4). The dispersal distancepofffiffiffiffiffiffiffiffiffiffiffiffi
nutrient on the
ffi
timescale for microbial immobilization ( Db=m = 1 cm) is
intermediate between the half inter-root distances for widely and
closely spaced roots (rx = 2 and 0.5 cm, Vr = 0.0001 and 0.0016,
respectively).
Results
Figure 1 illustrates how the radial distribution of the solute con-
centration cs(r, t) responds over time to a step increase in the rate
of root water uptake. Simulations consider widely spaced roots
for three contrasting values of the uptake : diffusion ratio Rr .
Simulations were initialized with steady-state radial distributions
in the absence of mass flow, which depict a zone of N depletion
adjacent to the root surface at all three values of Rr (solid orange
curves). Broken curves show solutions of Eqn 8 at times t = 1 and
20 d after a step increase in Rv from zero to 0.4 at t = 0. Follow-
ing the increase in Rv , nutrient concentrations well away from

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the root surface decrease because mass flow propels nutrient more
quickly towards the root. Nearer to the root surface, nutrient
concentrations increase, leading to enhanced root-N uptake. At
low Rr (Fig. 1a), the zone of nutrient depletion adjacent to the
root surface is replaced by a zone of N accumulation. At higher
Rr (Fig. 1b,c), however, the depletion zone is maintained
throughout the simulation. Radial distributions gradually
approach the new steady states at Rv = 0.4 (solid blue curves). A
difference between distributions simulated with contrasting Rr
relates to the concentration gradient at the root surface, which, in
the absence of mass flow, is most shallow at low Rr and most
steep at high Rr . In the presence of mass flow, the concentration
gradient is negative at low Rr (Fig. 1a), indicating reversal of the
diffusive flux, and positive at intermediate and high Rr . At inter-
mediate Rr , it is less steep at non-zero Rv than at zero Rv
(Fig. 1b), whereas, at high Rr , it is steeper at non-zero Rv than at
zero Rv (Fig. 1c). The implication is that, at high Rr , the pres-
ence of mass flow causes an increase in the diffusive component
of N flux at the root surface as well as the mass flow component.
The stimulation of diffusive flux by mass flow has been observed
in experiments (Oyewole et al., 2014).
(a)
(b)
(c)
Fig. 1 Solutions of the non-steady-state model (Eqn 8) for three values of
the uptake : diffusion ratio (a) Rr = 0.2, (b) Rr = 1 and (c) Rr = 5.
Simulations show how the radial distribution of solute concentration cs(r, t)
responds over time to a step change in the water uptake rate. Simulations
were initialized with steady-state radial distributions achieved without
mass flow (orange solid lines). Mass flow was switched on at time t = 0
with the mass flow : diffusion ratio held constant thereafter at Rv = 0.4.
Simulated radial distributions are shown at times t = 1 d (black dashes) and
20 d (red dashes). The blue solid line shows the steady-state radial
distribution at Rv = 0.4. Values of key parameters: Jrmax = 2000,
pffiffiffiffiffiffiffiffiffiffiffiffiffi
ro = 0.02 cm, rx = 2 cm, D = 0.05 cm2 d1, b/m = 20 d, Db=m = 1 cm,
Vr = 0.0001, Ro = 0.02, Rx = 2.
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We seek an explanation for the stimulation of diffusive flux by
mass flow seen in Fig. 1(c). Figure 2(a,b) shows steady-state mass
flow and diffusive fluxes (jMF and jDF, respectively) at the root
surface as functions of solute concentration at the root surface cso
for widely and closely spaced roots – jMF is proportional to cso
(Eqn 5b), whereas jDF is a linear function of cso with negative
slope (Eqn 7). Figure 2(a,b) indicates that, at low values of cso,
jDF is higher when Rv = 0.4 than when Rv = 0, implying that the
diffusive flux at the root surface may be stimulated by mass flow,
provided that the value of cso is small – the effect is pronounced
for widely spaced roots (Fig. 2a), but not for closely spaced roots
(Fig. 2b).
The soil-N supply curve (Eqn 7), which is the sum of the dif-
fusive and mass flow components (Eqn 5a), is shown in Fig. 2c
for widely spaced roots (Vr = 0.0001) when Rv = 0 and 0.4. The
N supply curve is a linear function of cso with negative slope that
is raised vertically with increasing Rv . When Rv = 0 and 0.4, the
Y-intercept is Jsmax = 607 and 1095, respectively. As Rv increases,
nutrient traverses the distance to the root surface more quickly,
and the probability of its immobilization by soil microbes before
reaching the root surface decreases. Decreased N immobilization
means, in turn, that nutrient supply to the root surface is
enhanced. Root-N demand curves (Eqn 2) are shown in Fig. 2(c)
for Jrmax = 500 and 2000. The curves approach Jrmax asymptoti-
cally. Steady-state solutions for cso and dimensionless root-N
influx Jr correspond to X- and Y-values at the intersections of the
N supply and N demand curves. Jrmax and Jsmax set upper limits
to the solution for Jr (Eqn 12). That is, the solution for Jr is less
than the minimum of Jrmax and Jsmax. When Jrmax ≫ Jsmax,
because Jr is limited by the maximum N supply Jsmax, increased
mass flow leads to large increases in the solution for Jr. For
instance, if Jrmax = 2000, the solution is Jr = 461 and 927 when
Rv = 0 and 0.4 (orange and blue circled points, Fig. 2c), respec-
tively. However, when Jrmax is low, because the N demand curve
is relatively flat, the solution for Jr is limited by Jrmax rather than
Jsmax. Increased Rv leads to N accumulation at the root surface
and large increases in cso, but relatively small increases in Jr. For
instance, at low Jrmax, the solution for Jr = 343 and 464 when
Rv = 0 and 0.4 (orange and blue dots), respectively. Figure 3
shows that Jr is an increasing function of Rv that is asymptotic to
Jrmax. The Y-intercept of each curve, which is the dimensionless
flux associated with diffusion JDF, is relatively insensitive to Jrmax,
but the ratio (Jr  JDF)/Rv , which is the slope of the line from
the Y-intercept to any point on the curve, and which is propor-
tional to the N uptake associated with mass flow per unit water
uptake (from Eqns 10, 13), is sensitive to Jrmax.
We now consider closely spaced roots (Fig. 2d). N supply
curves are lower and less sensitive to Rv than for widely spaced
roots. Y-values at intersections in Fig. 2d indicate that increased
Rv leads to modest increases in N uptake flux at both values of
Jrmax.
The model’s sensitivity to the uptake : diffusion ratio Rr is
considered in Fig. 2(e) for widely spaced roots. Soil-N demand
curves are shown for low and high Rr . As Rr increases, the N-
demand curve steepens but, because Jrmax is fixed, its asymptote
does not change. The curves in Fig. 2(c,e) are helpful in
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explaining why mass flow causes a reversal of the diffusive flux at
low Rr , a decrease in the diffusive flux at intermediate Rr and an
increase in the diffusive flux at high Rr , as seen in Fig. 1. At high
Rr , solutions for the dimensionless root-N influx Jr and dimen-
sionless fluxes associated with mass flow JMF (= jMF/roS) and dif-
fusion JDF (= jDF/roS) correspond to the points circled in
Fig. 2(a,e). At high Rr , in the presence of mass flow (blue circled
points in Fig. 2a,e), we calculate cso/(S/m) = 0.18, Jr = 1052,
JMF = 178 and JDF = 874. In the absence of mass flow (orange cir-
cled points), cso/(S/m) = 0.064, Jr = 568, JMF = 0 and JDF = 568.
In this case, water uptake increases the total influx Jr by 484,
37% of which arises through increased mass flow at the root sur-
face and 63% of which arises through increased diffusive flux. By
repeating these calculations for the other N demand curves with
Jrmax = 2000 in Fig. 2(c,e), at low, intermediate and high Rr , we
obtain JDF = 254, 461 and 568, respectively, in the absence of
mass flow, and JDF = 1240, 236 and 874, respectively, in the
presence of mass flow. Thus, the diffusive flux is stimulated by
mass flow at high Rr , but not at lower Rr . These modelled
changes in JDF with mass flow are consistent with changes in the
simulated concentration gradient at the root surface shown in
Fig. 1. The value of Rr is critical, because it influences the value
of cso where the N supply and N demand curves intersect. As Rr
increases, the N demand curve, shown in Fig. 2(e), steepens, low-
ering the solution for cso until it enters the region of Fig. 2(a),
where the diffusive flux jDF is stimulated by mass flow, and where
the mass flow flux jMF, which is proportional to cso, is small rela-
tive to jDF.
The N supply and demand curves shown in Fig. 2 depict the
effect of mass flow on root-N uptake as a consequence of reduced
N immobilization by soil microbes. This effect will be unimpor-
tant on timescales considerably shorter than the timescale for
microbial N immobilization, such as in short-term experiments
on how mass flow affects root-N uptake (Oyewole et al., 2014).

(a) (b)

Fig. 2 Nitrogen (N) supply and demand

curves derived from the steady-state model
(Eqn 4) for widely and closely spaced roots (c) (d)
with and without mass flow. (a, b) N arriving
at the root surface as diffusive and mass flow
fluxes vs solute concentration at the root
surface cso. Curves are shown for (a) widely
spaced roots (root volume density
Vr = 0.0001, rx = 100 ro) and (b) closely
spaced roots (Vr = 0.0016, rx = 25 ro). The
diffusive flux (jDF, Eqn 5c) is shown without
mass flow (Rv = 0, orange solid lines) and
with mass flow (Rv = 0.4, blue solid lines).
The mass flow flux (jMF, Eqn 5b) is shown for
Rv = 0.4 (blue dashed lines). (c, d, e) N
demand curves (Eqn 2, solid black lines),
expressing root-N influx j as a Michaelis–
Menten function of cso, are shown for N (e)
uptake capacity Jrmax = 2000 and 500 and
uptake : diffusion ratios Rr = 0.2, 1 and 5, as
specified in the figures. N supply curves
(Eqn 7, dashed coloured lines), which are the
sum of the diffusive and mass flow fluxes in
(a, b), are shown without mass flow (Rv = 0,
orange) and with mass flow (Rv = 0.4, blue)
(c, e) for widely spaced roots (Vr = 0.0001),
and (d) for closely spaced roots
(Vr = 0.0016). Orange and blue symbols in
(a, c, e) indicate steady-state solutions
without and with mass flow, respectively.
Value of dimensionless root radius is
Ro = 0.02.

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Therefore, in Fig. 4, we show N supply and demand curves
obtained when source–sink terms are omitted from the transport
equation. One additional assumption is made: at radial distance
r = rx, the concentration cs(rx) is equal to the bulk soil concentra-
tion cb. The N supply equation for this model is derived in
Notes S4. The N supply and demand curves in Fig. 4(b,c) are
qualitatively similar to their counterparts for the original model
(Fig. 2c,e), and the jMFcso and jDFcso relationships in Fig. 4(a)
are similar to those in Fig. 2(a). In particular, the sensitivity of
root-N influx to the mass flow : diffusion ratio (Rv ) is similar for
the models with and without source–sink terms. Mechanisms for
the Rv response are different, however: for the model without
source–sink terms, N input through mass flow across the outer
boundary, which equals 2provocb (g N cm1 root length d1), is
an increasing function of vo. Because m = 0, there is no mecha-
nism for N loss within the rhizosphere, so that root-N uptake,
which, at steady state equals the N input across the outer bound-
ary, is also an increasing function of vo and Rv .
Figure 5 shows solutions for the N uptake fraction / (Eqn 9)
at high and low Jrmax. / is shown as a function of the root volume
density Vr for contrasting values of daily water uptake E. The
highest root volume density (Vr = 0.004) corresponds to closely
spaced roots with rx = 16ro. / is an increasing function of Vr that
approaches unity asymptotically. For widely spaced roots with
low Vr, / is considerably less than unity, indicating that the avail-
able soil-N is mostly immobilized by soil microbes before reach-
ing the root surface. In the absence of mass flow (E = 0), /
increases gradually with increasing Vr, and the /Vr relationship
is relatively insensitive to Jrmax (cf. Fig. 3). In the presence of mass
Fig. 3 Dependence of root-nitrogen (N) influx j on mass flow : diffusion
ratio Rv . Relationships are shown for high (orange), intermediate (blue)
and low (red) N uptake capacity (Jrmax = 2000, 1000 and 500,
respectively). Values of key parameters: root volume density Vr = 0.0001,
uptake : diffusion ratio Rr = 1, dimensionless root radius Ro = 0.02. The Y-
intercept of each curve represents dimensionless diffusive flux of soil-N at
the root surface JDF.
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flow, / increases more steeply with increasing Vr. The /Vr rela-
tionship is shown in Fig. 5 for E = 0.01 and 0.05 d1. According
to Eqn 13, E is proportional to Rv Vr. Hence, for a given value of
E, Rv is inversely proportional to Vr. It follows that / is most
sensitive to E at low Vr, that is for widely spaced roots, and
becomes less sensitive to E with increasing Vr (cf. McMurtrie
et al., 2012). Water uptake has a reduced effect on / as Jrmax is
reduced from 2000 to 500 (Fig. 5a,b). At low Jrmax, / is relatively
insensitive to E at all values of Vr. This result is consistent with
Fig. 2c,d, showing that, at low Jrmax, root-N influx is insensitive
to Rv for both widely and closely spaced roots. It follows from
Fig. 5 that, with increasing water uptake E, a specified rate of N
uptake per unit soil volume, given by u = /S, will be achieved by
a lower root volume density. For instance, at high Jrmax (Fig. 5b),
the value of Vr that gives / = 0.5 is lower by a factor of 6 when
(a)
(b)
(c)
Fig. 4 Nitrogen (N) supply and demand curves for the model without
source–sink terms. (a) N arriving at the root surface as diffusive and mass
flow fluxes vs solute concentration at the root surface cso. The diffusive
flux (jDF, Supporting Information Eqn S4.15) is shown without mass flow
(Rv = 0, orange solid line) and with mass flow (Rv = 0.4, blue solid line).
The mass flow flux (jMF, Eqn S4.14) is shown for Rv = 0.4 (blue dashed
line). (b, c) N demand curves (Eqn 2, solid black lines), expressing root-N
influx j as a Michaelis–Menten function of cso, are shown for N uptake
capacity Jrmax’ = jrmax/(Dbcb/ro) = 0.8 and 0.2 and uptake : diffusion ratio
Rr = 0.2, 1 and 5, as specified in the figures. N supply curves (Eqn S4.16),
which are the sum of the diffusive and mass flow fluxes, are shown
without mass flow (Rv = 0, orange dashes) and with mass flow (Rv = 0.4,
blue dashes). Values of other parameters: Rx’ = 25 (e.g. ro = 0.02 cm,
rx = 0.5 cm).
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E = 0.05 d1 compared with E = 0 (Vr = 0.00013 vs 0.0008,
respectively).
Discussion
The main conclusion emerging from Figs 1–5 is that the response
of root-N uptake to water uptake depends on rooting density.
Two factors contribute to the large response of N uptake seen in
Fig. 5(a) at low rooting density. First, a large response is likely if,
in the absence of mass flow, a high proportion of nutrient is
immobilized by soil microbes before reaching the root surface.
When this condition is met, for example at low root absorbing
power or high immobilization rate m, or low rooting density, a
small reduction in microbial N acquisition in the presence of
mass flow, because nutrient travels more quickly to the root sur-
face, can give rise to a large relative increase in root-N acquisi-
tion. Second, the response is amplified with decreasing root
volume density Vr, because a given daily water uptake per unit
soil volume E is distributed over a reduced root surface area, and
the velocity of water towards the root surface, given by v(r) in
Eqn 13, is inversely proportional to Vr. Thus, water uptake by
roots at low rooting densities may considerably enhance root-N
acquisition at the expense of N acquisition by soil microbes.
(a)
(b)
Fig. 5 Nitrogen (N) uptake fraction / as a function of root volume density
Vr for contrasting values of N uptake capacity and daily water uptake.
Curves are shown for three values of daily water uptake per unit soil
volume, E = 0 (orange), 0.01 (blue) and 0.05 (red), and for two values of N
uptake capacity, (a) Jrmax = 2000 and (b) Jrmax = 500. For each value of E,
Eqn 13 was used to determine how Rv varies with increasing Vr, with
Db = 0.05 cm2 d1 and ro = 0.02 cm. The asymptotic value, / = 1, is
approached in the limit of high Vr, when all available N is taken up by roots
and none is immobilized by soil microbes before reaching the root surface.
At low Vr, the value of Jrmax sets an upper limit to the N uptake fraction
/max = 2JrmaxVr (Eqn 12), which is shown as black dashed lines. Values of
other parameters: Ro = 0.02, Rr = 1.
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Implicitly, in the presence of mass flow, plants can compete effi-
ciently with microbes for N with a smaller proportion of their
biomass allocated to roots than in the absence of mass flow. A
precondition to these results is that mass flow will only have a
substantial effect on root-N uptake if root-N uptake capacity
jrmax is not limiting. This limitation explains why the N uptake
fraction is less sensitive to daily water uptake at low jrmax (Fig. 5b)
than at high jrmax (Fig. 5a), and suggests that root expression of
low-affinity transport systems for N would be linked to mass
flow.
Evidence from modelling that high jrmax is conducive to N
acquisition via mass flow is notable given the capacity of roots to
increase jrmax by switching from high- to low-affinity transport
systems (Wang et al., 2012; Nacry et al., 2013; Sun et al., 2014).
These publications show that root-N uptake kinetics are regu-
lated both on the basis of local concentrations around individual
roots and systemically via cues related to the internal N status of
the plants. High-affinity uptake systems operate at low concentra-
tions, typically as low as a few lM, whereas low-affinity uptake
systems are active at higher concentrations, often as high as 1–
10 mM (Crawford & Glass, 1998; N€asholm et al., 2009; Nacry
et al., 2013). N accumulates around roots when the mass flow
delivery of N to roots exceeds the root uptake capacity (Figs 1a,
2c,e). Under such conditions, sensing of local N concentrations
may lead to a switch in root uptake kinetics from high- to low-
affinity uptake systems, enabling plants to acquire N at a higher
rate, and hence taking advantage of mass flow. Such dynamics in
the composition of plasma membranes occur in response to vari-
ous environmental cues (Luschnig & Vert, 2014). Notably, alter-
ations of the composition of membrane transporters of the root
epidermis are not specific for variations in N availability, but are
a ubiquitous mechanism by which plants regulate nutrient uptake
(e.g. Lambers et al., 1998). Furthermore, experimental evidence
suggests that mass flow in itself may be stimulated by soil-N
availability. Root hydraulic resistance is, in the short term, regu-
lated by the expression and activity of aquaporins, and there is
evidence to suggest that soil-N availability affects both root aqua-
porin activity and hydraulic conductivity (Gorska et al., 2008;
Hacke et al., 2010; Ishikawa-Sakurai et al., 2014; Ren et al.,
2015). The inference is that, under conditions of adequate soil
water and soil-N availabilities, mass flow and root-N uptake
capacity may be regulated in concert to enhance N acquisition
from soil. A further enhancement of mass flow may be achieved
if the anatomical characteristics of roots are altered in response to
N. Such changes in the anatomy of fine roots have been
described, showing that the diameter of root conductive cells
responds positively to enhanced N availability (e.g. Krasowski &
Owens, 1999).
Interacting effects of root-N uptake capacity and mass flow on
root-N uptake are directly addressed in Fig. 3. In the absence of
mass flow (i.e. when Rv = 0), an increase in dimensionless N
uptake capacity Jrmax from 500 to 2000 leads to a modest increase
in N uptake flux. At low Jrmax, an increase in Rv also causes a
modest increase in N uptake flux (red line). The increase in N
uptake flux is much greater, however, when Rv and Jrmax both
increase. These modelled responses to increased Jrmax suggest that
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128 Research
the benefit of a switch from high- to low-affinity transport sys-
tems may be enhanced in the presence of mass flow. The impact
of mass flow on modelled N uptake flux would be greater still if
N accumulation near the root surface led to the saturation of
microbial N uptake. This effect could be investigated using our
model by calculating N supply curves with an MM function used
to represent microbial N uptake (cf. Kuzyakov & Xu, 2013;
Tang & Riley, 2013; Zhu et al., 2017).
Although there is general acceptance that nutrient flux into the
root is an MM function of solute concentration at the root sur-
face cso (e.g. Tinker & Nye, 2000), this relationship has not yet
been incorporated in TBMs, arguably because of inadequate
understanding of soil transport processes that determine cso. Our
model predicts cso by solving a pair of equations for root-N
demand (the MM equation) and soil-N supply to the root sur-
face, both depending on cso. The approach is akin to the iconic
model of leaf gas exchange combining equations for CO2 supply
and demand, both depending on the intercellular CO2 concen-
tration (Farquhar & Sharkey, 1982). Modelling of CO2 supply
and demand is intrinsic to TBMs that simulate stomatal control
of photosynthesis (De Kauwe et al., 2013). An analogous
approach could be adopted for the simulation of the root system
N uptake based on the incorporation of our equations for soil-N
supply and demand into TBMs that calculate the spatial distribu-
tions of fine root biomass, soil-N availability and root water
uptake. To that end, we have summarized the relationships
derived above with potential for inclusion in TBMs in Table 3.
One way of incorporating our model into TBMs would be via
our equation for the root-N uptake fraction (Eqn 10). An alterna-
tive approach would be to separately evaluate N uptake associated
with diffusion and mass flow. Daily N uptake in the absence of
mass flow could be evaluated as described above using Eqn 10
with Rv = 0, whereas N uptake associated with mass flow could
be estimated using the JrRv relationship depicted in Fig. 3
Table 3 Summary of relationships depicted in Figs 2–4 that may be suitable for inclusion in terrestrial biosphere models (TBMs)
Relationship (Fig. & Eqn numbers) Y-variable X-variable
Root-N demand (Figs 2, 4; Eqn 2) Root-N influx cso
(j)
Root-N supply (Fig. 2; Eqn 7) Root-N influx cso
(j)
Root-N supply (Fig. 4; Notes S4 Root-N influx cso
Eqn S4.16) (j)
Root-N influx vs Rv (Fig. 3; Root-N influx Mass
solution of Eqns 2 & 7) (j) flow : diffusion
ratio Rv
Root-N uptake fraction vs Vr rela- Root-N Root volume
tionship (Fig. 5; Eqns 9 & 10) uptake density (Vr)
fraction (/)
cso, solute concentration at root surface; Jrmax, dimensionless root-N uptake capacity; Vr, root volume density.
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from daily water uptake multiplied by the relationship’s initial
slope. We anticipate that mass flow will make a small contribu-
tion to N uptake for most of the root system, echoing past mod-
elling work on the topic (Yanai, 1994; Darrah et al., 2006;
BassiriRad et al., 2008), but will make a larger contribution to
the modelled N uptake for a subset of roots with low rooting
density, high conductivity to water flux and high N uptake capac-
ity. The local redistribution of root hydraulic conductivities via
enhanced aquaporin activity for roots encountering N and
decreased activity for other parts of the root system (Gorska et al.,
2008) would exacerbate the role of mass flow for individual
roots.
One area of modelling uncertainty is that the equations above
were derived at steady state. The question arises: How will water
uptake affect N uptake when the model is not at steady state?
Solutions of the time-dependent model at high Jrmax (Fig. 1)
show that mass flow speeds up movement of nutrient to the root
surface, enhancing cso and hence N uptake, and that this response
occurs long before establishment of the steady state. Therefore, it
is anticipated that the sensitivity of root-N uptake to mass flow,
depicted in Figs 2–5, will apply when soil-N distributions are not
at steady state. A similar conclusion is reached from simulations
initiated with spatially uniform soil-N distributions, which
would apply when roots first enter a previously unexploited soil
patch, and begin foraging for N (Figs S1, S2). Root-N influx is
higher in the presence of mass flow throughout these simulations,
except for a short initial transient period. Again, the effect of
mass flow is apparent long before establishment of steady-state
conditions.
Future work with the model needs to focus on up-scaling to
whole-root systems (e.g. McMurtrie et al., 2012; Valentine &
M€akel€a, 2012; McMurtrie & Dewar, 2013), and on the quantifi-
cation of the contribution of mass flow to total N uptake by root
systems whose water uptake is consistent with rates seen at
Explanatory notes
Root-N influx (j) as Michaelis–Menten function of soil solution concentration at
root surface cso (root demand for substrate to achieve given value of j)
Flux of solute transported to root surface through diffusion and mass flow for
model incorporating microbial N immobilization
Flux of solute transported to root surface through diffusion and mass flow for
model without source–sink terms (applicable on timescales considerably shorter
than timescale for N immobilization)
Relationship’s Y-intercept represents root-N influx in absence of mass flow. At
low Rv , the relationship is approximately linear. Its initial slope, which is sensitive
to Vr and Jrmax, is proportional to mass flow utilization efficiency (N uptake asso-
ciated with mass flow per unit water uptake). Thus, provided that Rv is small,
transpirationally induced N uptake may be estimated from the modelled spatial
distribution of water uptake over the root system multiplied by mass flow utiliza-
tion efficiency. This proposed approach is akin to Fisher et al.’s (2010) and Ger-
ber et al.’s (2010) methods for the evaluation of passive N uptake. A difference
is that we model root-N uptake solely as an active process
Relationship for partitioning of N uptake between microbial immobilizers and
plant roots. Relationship is sensitive to water uptake rate at low Vr and high Jrmax
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macroscopic scales. Future work should also consider N uptake
by mycorrhizal fungi. It would be straightforward to incorporate
a term for mycorrhizal N uptake in the N transport equation,
similar to the term for microbial N immobilization in Eqn 8.
The model with mycorrhiza could assume that a fixed or variable
proportion of mycorrhizal N uptake contributes to host plant-N
uptake, but would also need to take into account the effect of
mycorrhizal formation on root uptake kinetics and hydraulic
conductivity.
Acknowledgements
This study was supported by The Swedish Research Council for
Environment, Agricultural Sciences and Spatial Planning, The
Kempe Foundations, The Swedish University of Agricultural
Sciences (SLU; TC4F and Bio4E), The Swedish Governmental
Agency for Innovation Systems (Vinnova), and The Knut and
Alice Wallenberg Foundation. We thank Anthony Walker,
Roddy Dewar and anonymous referees for helpful advice and
comments.
Author contributions
T.N. proposed the research question. R.E.M. formulated the
model and performed the research. R.E.M. and T.N. wrote the
manuscript.
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See also the Commentary on this article by Walker, 218: 8–11.

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