Plant Soil
https://doi.org/10.1007/s11104-020-04738-3

REGULAR ARTICLE

Root water uptake under heterogeneous soil moisture
conditions: an experimental study for unravelingcompensatory root water uptake and hydraulicredistribution
Anooja Thomas & Brijesh Kumar Yadav& Jiří Šimůnek

Received: 23 June 2020 / Accepted: 7 October 2020
# Springer Nature Switzerland AG 2020

Abstract
Aims Plant roots often encounter heterogeneity in soil
water content and respond by compensating water uptake from wet zones to cope with the transpiration
demand. Simultaneously, plants may also exhibit rootmediated hydraulic redistribution from wet to dry zones.
Experiments were conducted to simultaneously monitor
compensated root water uptake and hydraulic redistribution in the vadose zone.
Methods Vertical and horizontal split-root lysimeters
were used to hydraulically isolate maize roots underaltering soil water conditions. Compensated root water
uptake and root-mediated hydraulic redistribution weremonitored by continuous measurement of water content
in the lysimeter compartments.
Results Soil water heterogeneity and limited soil water
availability were found to accelerate the root water uptake from moist region to compensate the reduced water

availability in dry zone. However, no measurable root
mediated hydraulic redistribution was observed in shortterm basis, despite high water potential gradient in theroot zone of both lysimeters. The night-time transpiration and xylem refilling processes seem to override
the hydraulic redistribution on a diurnal basis in our
experiment.
Conclusions Our study shows that compensated root
water uptakeplays a major role in meeting the transpiration demand. In contrast, the role of root mediatedhydraulic redistribution is found to benegligible inmaize plant.
Keywords Compensatory root water uptake . Hydraulicredistribution . Split-root lysimeter . Night-timetranspiration . Xylem refilling

Introduction
Responsible Editor: Rafael S. OliveiraElectronic supplementary material The online version of thisarticle (https://doi.org/10.1007/s11104-020-04738-3) contains
supplementary material, which is available to authorized users.
A. Thomas : B. K. Yadav (*)
Department of Hydrology, Indian Institute of Technology
Roorkee, Roorkee 247667, Indiae-mail: brijkfhy@iitr.ac.in
e-mail: brijeshy@gmail.com
A. Thomas : J. Šimůnek
Department of Environmental Sciences, University of California
Riverside, Riverside, CA 92521, USA

Water uptake by plant roots is often regulated by endogenous factors such as root-shoot biomass and growthstage, as well as by external factors including soil watercontent, nutrient availability, and prevailing weather conditions (Albasha et al. 2015). The soil water content in theroot zone is often heterogeneously distributed due tomultiple factors such as soil type, irrigation/rainfall variability, non-uniform root distribution, and dynamic root
water uptake patterns (Doussan et al. 2006; Yadav andMathur 2008; Dara et al. 2015). Therefore, plants often
deploy compensated root water uptake (hereafter referred
to as CRWU) (Green and Clothier 1995; Yadav et al.

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2009), root mediated hydraulic redistribution (HR)(Richards and Caldwell 1987; Caldwell et al. 1998;
Oliveira et al. 2005), and adaptive root growth(Clausnitzer and Hopmans 1994) to cope with the soil
moisture heterogeneity.
CRWU is a process in which water requirements ofthe plant under limiting soil moisture conditions are
fulfilled by enhanced uptake from wetter root zone(Šimůnek and Hopmans 2009; Couvreur et al. 2012;
Javaux et al. 2013). For example, when the water content in the upper zone with a high root density decreases,
water absorption from the deeper moist layers increases
for compensation (Teuling et al. 2006). Thereby,
CRWU allows plants to transpire at or close to thepotential demand though a part of the root system issubjected to limited soil moisture availability (Soylu
et al. 2017). CRWU is a prominent root water uptake
mechanism in many plants with roots in the capillaryzone (Kang et al. 2002; Karimov et al. 2014; Soylu et al.
2017) or zones with heterogeneous soil structure(Kuhlmann et al. 2012). In addition, CRWU can beobserved when some part of root biomass gets permanently damaged (Poni et al. 1992; Vysotskaya et al.
2004; Black et al. 2011). Alternate partial root-zone
drying (Kang et al. 2003; Mingo et al. 2004), regulated
deficit irrigation (Kang and Zhang 2004; Leib et al.
2006; Chai et al. 2016), localized irrigation (Green andClothier 1995), and alternate furrow irrigation (Kanget al. 2002) are some of the irrigation practices that aresupposed to use CRWU to reduce evaporation loss.
Therefore, an accurate estimation of CRWU is essential
for understanding plant water uptake patterns and for
simulating soil water flow in the vadose zone undervarying soil moisture conditions.
HR is a passive transfer of soil moisture via the rootsystem from a region of high water potential to low
water potential (Oliveira et al. 2005). Thereby, underheterogenous soil moisture condition, the roots reallocate water from wetter soil layers to drier soil layers. The
transferred water is further used for transpiration(Burgess and Bleby 2006) and to some extent, moderate
the intensity of CRWU (Guswa 2012). The magnitudeof HR depends on multiple factors, including water
potential gradient between the soil layers, root conductivity, spatial distribution of the root system, and transpiration demand (Meinzer et al. 2004; Doussan et al.
2006). HR is typically observed in deep-rooted desert
plants, shrubs, and trees, for which hydraulically
redistributed water contributes towards the transpiration

demand (Hultine et al. 2003; Oliveira et al. 2005;
Neumann and Cardon 2012). The ecological impactsof HR such as preventing the loss of hydraulic conductivity of roots (Bauerle et al. 2008), increasing nutrientsacquisition and their mobilization (Warren et al. 2008,
Armas et al. 2012; Sardans and Peñuelas 2014), havealso been described previously. However, studies on
HR in agriculture crops under field conditions are limited and have contradictory observations on its relevance from a hydrological perspective (ZegadaLizarazu and Iijima 2004; Cai et al. 2018; Meunieret al. 2018).
HR is more likely to happen when the transpiration
demand is low, especially during night hours (Richards
and Caldwell, 1987) and after rainfall (Hultine et al.
2004). However, the active night-time transpiration
has been observed in many crops due to partial closureof the stomata (Tolk et al. 2006; Caird et al., 2007a, b).
Moreover, studies have shown that plants can also lose
the hydraulic conductivity of xylem tissues in roots,
shoots and stem during day time due to embolism/
cavitation as a result of soil water stress (McCully
1999; Domec et al. 2006; Lovisolo et al. 2008;
Johnson et al. 2009). Depending on multiple factors
such as species, genotype, stage of development, extent
and severity of water stress (Thapa et al. 2011; Knipfer
et al. 2017), plants can recover from cavitation by xylem
refiling (McCully et al. 1998; Yu et al. 2018) during
night hours (Domec et al. 2006) or after irrigation(Brodersen et al. 2010). Therefore, night-time transpiration and xylem refilling can modulate the magnitude of
HR (Howard et al. 2009; Prieto et al. 2010a, b; Yu et al.
2018).
Though the mechanisms of root water uptake,including CRWU and HR, were studied under varying soil moisture conditions (Drew 1975;
Koebernick et al. 2015; Dara et al. 2015), the cause
and impact on each other require further investigations. As both mechanisms can be triggered underheterogeneous soil moisture conditions, we studied
the co-occurrence and magnitude of these mechanisms in maize plant. This can be achieved by generating a water potential gradient between root zones
followed by measuring the change in soil watercontent as a proxy for water uptake/release by plantroots. However, an accurate estimation of root water
uptake is often limited by the soil water flux due tothe water potential gradient between the root zone
(Musters and Bouten 2000). Therefore, wePlant Soil

performed a series of split-root lysimeter experiments, wherein the plant roots are compartmentalized into hydrologically isolated regions aligned
vertically or horizontally. Further, the role of nighttime transpiration and xylem refilling were also investigated in association with HR. Therefore,
the current study aimed at improving the understanding of root water uptake by maize under heterogeneous soil moisture conditions while simultaneously considering CRWU and HR.

Materials and methods
Experimental rationale and setup
The design of the vertical and horizontal split-root lysimeters and the location of sensors is shown in Fig. 1. The
design and experimental strategies of the column lysimeter are described in the supporting information (S1). The
vertical split-root lysimeter is constructed by assembling
two chambers made of acrylic glass with an internalmeasurement of 12 × 22 × 43 cm (L × W × H). The horizontal split-root lysimeter is made of a cylindrical PVC
column with an internal diameter of 12.7 cm and a heightof 55 cm, divided into two compartments using beeswax

Fig. 1 Schematic representation of the split-root lysimeter experiment
setups. (a) The vertical split-root lysimeter with soil moisture sensor
locations. The root distribution is represented in the right panel in termsof 1 cm thickness. The consistency of the wax was
reduced by adding vegetable oil to avoid crack during
root growth and diurnal temperature variations. A provision for drainage was also made at the bottom of alllysimeter compartments, along with the option for irrigating them separately. The soil substratum made of silt,clay, and organic matter in the proportion of 16:4:1(bulk density 1.36 g/cm3) was used as the growing
medium in the experimental setup. Germinatedseedlings of maize were planted in the lysimeters.
In the vertical split-root lysimeter, the root cap withapical meristem (1 cm from the tip) of the seedlings was
excised and transplanted to the seedling chamberthat placed directly in the middle of the lysimeter (Fig.
1a). This was to enhance the primary lateral root growth(Brouder and Cassman, 1994; Fernández et al. 2011),
which leads to equal distribution of roots between thecompartments while interconnected only via the plantbiomass. One week after transplantation, the lysimeters
were thinned to two seedlings per setup. All lysimeters
were kept outdoors during the growing stage and irrigated daily and weekly with the NPK (16–16–16) solution till their reproductive stage. To minimize the impact
of radiation-induced heating of the root zone on root
growth, lysimeters were wrapped with jute and kept
moist during the growth period (Poni et al. 1992).

of its dry weight (in grams). (b) The horizontal split-root lysimeter. (c)The control lysimeter with dimensions

Plant Soil

For continuous measurement of soil water content,
four soil moisture sensors (WaterScout SM 100, sensing
area is 6 cm × 2 cm) were installed in each zone of thelysimeter as shown in Fig. 1. In the vertical split-root
lysimeter, two sensors were installed per compartment,
one at a distance of 15 cm below the root-shoot junction(L1/R1) and the other 5 cm above the bottom drainage(L2/R2). In horizontal split-root lysimeter, the sensors
were installed at the locations of 10 cm (S1), 20 cm (S2),
33 cm (S3), and 43 cm (S4) from the top. The readingfrom each sensor was considered as the average soil
water content of the corresponding zone. The entire
experimental setup was mounted over a weighing machine (Wensar counter scale 30 kg, accuracy 0.1 g) forthe mass balance analysis. Control lysimeters were built
in parallel to corresponding split-root lysimeters formeasuring potential transpiration (Fig. S1A and Fig.
S2A, respectively).
Vertical split-root lysimeter
The vertical lysimeter was left unirrigated to bring thesoil water content in both compartments to wilting pointby allowing the plants to transpire over multiple days
(phase I) (Fig. 2a I). Phase II was initiated by irrigating
the right compartment to field capacity, while the left
compartment remained under water stress (Fig. 2a II).
When the soil water content in the right compartment
reached the wilting point, phase III was initiated byswitching irrigation to the left compartment (Fig. 2aIII). Phase IV began by irrigating both compartments
to field capacity when the left compartment reached thewilting point (Fig. 2a IV). At the end of phase IV, theshoot biomass of the plant was excised from its root, thestem-root interface was sealed with parafilm to prevent
sap flow, and the right compartment was then irrigatedto field capacity (Fig. 2a V, S1B). At the end of phase V,
each compartment was segmented into two sections of
20 cm each (Fig. S1C, D), the roots were separated fromthe soil by washing, and the dry weight of the roots fromeach section was measured (Fig. 1a).

Fig. 2 Schematic representation of irrigation during different phases ofvertical and horizontal split-root lysimeter experiments. The initial soil
water content of blue coloured compartments was near to field capacity,while the sand filling represents the compartments with soil watercontent near the wilting point. (a) Irrigation scenarios in the vertical
split-root lysimeter: (I) Both left and right compartments are under water
stressed conditions; (II) The right compartment is irrigated while the left
compartment is under waster stress; (III) The left compartment is irrigated and the right compartment is under water stress; (IV) Both compartments are irrigated; (V) Zero transpiration conditions with the irrigated right compartment after shoot removal. (b) Irrigation scenarios in thehorizonal split-root experiment: (I) Both left and right compartments
irrigated to field capacity; (II) The lower compartment irrigated while
the upper compartment is under waster stress; (III) The water table as abottom boundary condition

phase I, by irrigating only the lower compartment (Fig.
2b II). When the soil water content in the lower compartment declined to 3% due to continuous transpiration, the water table treatment (phase III) was performed
for three days (Fig. 2b III). For this, the whole lysimeter
setup was kept partially immersed in a water reservoir
under a constant level of water and the surface evaporation was prevented. In the end, the lysimeter wassegmented into four sections of 10 cm each, such thatthe sensor location was in the middle of each section.
The roots were then collected, washed (Fig. S1B), andthe dry root biomass was determined (Fig. 1b).

Horizontal split-root lysimeter
Estimation of actual and potential transpiration
Phase I of the horizontal split-root experiment was initiated by irrigating both compartments to field capacity(Fig. 2b I). The lysimeter was then left unirrigated for
one week, while the soil water content was recorded
continuously. Phase II started from the wilting point ofPotential transpiration from all lysimeters was estimated from its corresponding control lysimeter. For that, acontrol lysimeter was maintained along with each splitroot lysimeter setup under the same environmental

Plant Soil

conditions. Before each experiment, a correlation function (K) for transpiration was obtained for each splitroot lysimeter with its corresponding control(Table S1). For that, the soil water content in the main
lysimeter and its control were maintained in the optimal
range, and the transpiration flux was measured at multiple time intervals. From this data, a correlation coefficient (K) (Ray and Sinclair 1997; Vamerali et al.
2003) was obtained by assuming a linear relationshipbetween the transpiration rate from the main experiment and its control. Here we assumed that the change
in plant biomass during the yield formation stage of themaize plant is in the same proportion (Koca and Erekul2016). Therefore, the potential transpiration from themain lysimeter (Tp) can be estimated from the transpiration rate of the control (Tpc) using the correlation
coefficient, K (Tp = Tpc * K).
Throughout the experiment, the soil water content in the control lysimeter was maintained in the
optimal range by replenishing water lost by transpiration. Surface evaporation from the main splitroot lysimeters and their corresponding controls
was prevented by a layer of sand and aluminium
foil (Faria et al. 2010; Moradi et al. 2011). As the
exposure of the soil surface to the atmosphere wasrestricted, it was assumed that the evaporation loss
during the experiment was negligible. This suggeststhat the weight loss from any lysimeter between
two time points was exclusively due to the transpiration flux. To measure the actual and potential
transpiration rates, the weight of the lysimeter
setups and their corresponding controls were recorded every day at 7 am, 10 am, 1 pm, 4 pm,
and 7 pm throughout the experiment. Actual transpiration during any time interval was then obtained by mass balance. Corresponding potential transpiration was estimated by multiplying the transpiration flux from the control lysimeter with its correlation coefficient (K).

Results
CRWU under varying soil moisture conditions in maize
Vertical split-root lysimeter
During the early days of phase II and III (days 2, 3,
6, 7), the transpiration demand of the plant was

fulfilled from the irrigated compartment, while thesoil water content in the other compartment wasnear the wilting point (Fig. 3a, c, d). Also, a sharp
decline in the soil water content in the irrigatedcompartments was observed during these days, ascompared to phase IV. These observations confirm
the occurrence of CRWU by enhanced water uptake
from the irrigated compartments that compensatedthe water uptake reduction from the dry compartments (Šimůnek and Hopmans 2009; Yadav et al.
2009). Also, after irrigating the dry compartment
during the phase change, the transpiration rate was
fully recovered, indicating that the roots in dry compartments remained viable despite temporary water
stress.
The relative soil water depletion from zones R1
and R2 of the wet compartment on day 2 (phase II)
was 81.5% and 18.5%, respectively, while the depletion from zones L1 and L2 of the dry compartment remained negligible (Fig. 3b). Similarly, on
day 6 of the experiment (phase III), the relative soil
water depletion was nearly 76.7% and 23.3% fromzones L1 and L2, respectively, while it remained
insignificant from zones R1 and R2. During days
10 and 11 (phase IV), the relative soil moisture
depletion from zones L1, L2, R1, and R2 was
37.8%, 11.45%, 39.7%, and 11%, respectively.
Comparable root distribution and soil moisture depletion on days 10 and 11 with optimal soil watercontent suggest a linear correlation between water
uptake and root density (Fig. 3b). As the soil watercontent was gradually depleted from the high root
density regions (below 15%, phase II, III, and IV), a
shift in the location of water extraction to low root
density zones and an increased absorption rate fromthese zones were observed. For example, on day 4(phase II), the relative water depletion from location
R1 decreased to 25.7% and from R2 increased to74.3%, while it remained unchanged in the drycompartment. Similarly, on day 10, the relative water depletion from L1 and R1 was 41.6%, and 39.4%,
whereas it was 11.5%, and 7.5% from L2 and R2
respectively. On day 14, the relative water depletionfrom locations L1 and R1 decreased to 13.8% and12.3%, respectively (Fig. 3b). In comparison, it increased from L2 and R2 to 37.7% and 36.2%, respectively, indicating that compensatory water uptake
from zones L2 and R2, and thus the potential transpiration rate was maintained (Fig. 3d). It was further

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Fig. 3 The vertical split-root lysimeter with a fully grown maize plantunder varying soil moisture conditions. (a) Soil water content recordedby soil moisture sensors from four different locations under different
irrigation scenarios. Solid lines indicate the soil water content variation
during day time and dotted lines indicate the soil water content duringconfirmed from the control setup that the potential
transpiration rate was maintained despite the prevailing soil water stress in some regions during phase II,
III, and IV (Fig. 3c, days 2–3, 6–8, and 13–14).
When the soil water content in both compartments of the vertical split-root lysimeter was nearfield capacity (days 10 and 11), water uptake fromzones L2 and R2 was nearly 11.5% and 9% of thetotal diurnal water uptake rate, respectively (Fig.
3b). During phase II and III, when CRWU occurredunder heterogeneous water distribution, the water
uptake from zones L2 and R2 was as high as 70%(day 4) and 75% (day 8), respectively, of the corresponding total diurnal water uptake quantity. Thissuggests that when compensation occurs, a fractionof roots in the wet soil exhibits a high water absorption rate per unit of its dry weight as compared to
the roots present in the dry zone. Thus, under localized water stress condition, the roots that are “active” in supplying water to plants can be defined as
the portion of roots that are exposed to soil withfavorable water content.

night. (b) Relative soil moisture depletion (root water uptake) fromsensor zones L1, L2, R1, and R2 in the vertical split-root lysimeterand the corresponding relative root distribution. (c) Actual transpiration(Ta) and potential transpiration (Tp) measured in litres at a regular timeinterval. (d) Daily relative transpiration

Horizontal split-root lysimeterOn days 1 and 2 of phase I in horizontal split-root lysimeter
experiment, relative soil moisture depletion from zones S1,
S2, S3, and S4 was 46%, 25%, 19%, and 10%, respectively, and the corresponding root distribution was 47%,
29%, 16%, and 8% (Fig. 4b). This indicates that the water
extraction rate from the soil is linearly correlated with theroot density distribution under optimal soil moisture condition, as reported previously by Yu et al. (2007) andYadav et al. (2009). After that, when the soil water content
of a region was reduced below 15%, the root water extraction rate from that zone decreased substantially (Fig. 4a, b).
Also, the zone of maximum root water uptake shifted
downwards into deeper soil layers with a lower root density. Water absorption from these deeper soil layers increased to cope with the transpiration demand. The highest
rate of water uptake from zone S4 with the lowest root
density was observed during the final days ofphase I and II when the average soil water content
in the lysimeter fell below 10%. This indicates that
reduced root water uptake from the dry zone wasPlant Soil

Fig. 4 The horizontal split-root lysimeter with a fully grown maize plantunder different soil moisture conditions. (a) Soil water content variations
recorded using soil moisture sensors under different irrigation scenarios. Day time soil water content is represented by solid lines and dottedlines represent the night time soil water content. (b) Relative soil

moisture depletion (root water uptake) from sensor zones S1, S2, S3,
and S4 in the horizontal split-root lysimeter and the corresponding root
distribution in the zones. (c) Actual transpiration (Ta) and potential
transpiration (Tp) measured at a regular time interval. (d) Daily relativetranspiration

fully or partially compensated by enhanced water
uptake from the wetter zone (Fig. 4b).
The comparable actual and potential transpiration
rates estimated from the control lysimeter further confirmed the existence of CRWU (Fig. 4c, days 4–6, 8–9,
and 12–14). On day 8 (phase II), when only the lower
compartment was irrigated while the upper compartment was near the wilting point, a reduction in root
water uptake from the upper compartment was fullycompensated by increased water uptake from the lower
compartment. Likewise, during the water table boundary treatment (phase III), when the roots in the lower
compartment received ample water, a reduction in root
water uptake from the upper compartment was almost
fully compensated by an increased uptake from thelower compartment supplied with water by a capillaryrise, and thereby the transpiration demand was fulfilled(Fig. 4d). Moreover, during the water table treatment,
around 24% of fine roots in the lower compartmentthat had access to the capillary water mostly contributed
towards the transpiration demand. In comparison, water
uptake from the remaining 76% of fine roots was negligible. Thus, a fraction of the root biomass present in

the moist layer meets the plants’ transpiration demandthrough the CRWU.
Root mediated HR under heterogeneous soil moisture
conditions
Vertical split-root lysimeter
Previous studies (Ryel et al. 2002; Mendel et al. 2002;
Amenu and Kumar 2008; Couvreur et al. 2014) revealed
that the high water potential gradient in the root zone
along with the reduced transpiration demand can resultin the redistribution of soil moisture through root-shootbiomass. Phase II and III of the vertical split-root lysimeter experiment were performed with an objective tocreate a high water potential gradient between the twocompartments. In the split-root lysimeter experiments,
HR can be analyzed by observing an increase in the soil
water content in the dry compartment during low transpiration periods. A high water potential gradient between the hydraulically isolated compartments was generated during phase II (Fig. 2a II, Fig. 3a II). A reciprocal water potential gradient was also generated in phasePlant Soil

III between the compartments to make sure that bothcompartments possess active roots despite being temporarily subject to water-stress (Fig. 2a III, Fig. 3a III).
Since the maize plant was in yield-forming stage andretained comparable root biomass in both compartments(Fig. S1D), redistribution of water between the wet todry compartments was expected. Although the night
hours in early days of phase II and III supported favorable conditions for HR, no considerable increase in thesoil water content was observed in the dry compartments (Fig. 3a II zone L1 and L2, Fig. 3a III zone R1
and R2), indicating the absence of HR.
To assess any possible existence of passive HR
between the compartments in the absence of transpiration, the shoot biomass was removed, the rightcompartment was irrigated, and the soil moisture
distribution was monitored over a period of 24 h(phase V) (Fig. 2aA V, Fig. S1B). It was hypothesized that HR through the roots should occur under ahigh water potential gradient as long as roots areintact and hydrated even in the absence of shootbiomass (Leffler et al. 2005). The existence of astrong soil moisture gradient between the two compartments interconnected via the shared root systemand the absence of any measurable change in watercontent in the two compartments suggested the lackof measurable passive redistribution of soil moistureby roots (Fig. 3a V). A high water potential gradientcreated after the removal of the plant shoot biomass
did not result in a redistribution of soil water to thedry zone, even in the absence of transpiration.

Night-time transpiration and xylem refillingunder different soil moisture conditions
Vertical split-root lysimeter
Under optimal soil moisture conditions, the nighttime transpiration was up to 12% of the total transpiration. This suggests its significant contribution
towards the daily transpiration flux(Fig. 5a). In contrast, a reduction in the night-time transpiration ondays 4, 8, and 13–14, compared with the control
suggests that night-time transpiration can also beaffected by soil water stress. When the daily transpiration rate dropped below 70% of the potential
transpiration demand, the observed night-time transpiration was negligible (on days 5, 9, 15, and 16).
Moreover, during days 4, 8, 14, and 15, a high water
uptake rate by plant roots was observed during night(e.g., Fig. 3a: zones R2 and L2, days 14–15, dottedlines, Fig. S3B), while night-time transpiration was
nearly zero (Fig. 3c). Although the plant showedtemporary wilting during these days, the recovery
during night hours suggested the existence of xylem
refilling.

Horizontal split-root lysimeter
During the early days of phase II and III of the horizontal split-root lysimeter experiment, a strong water potential gradient and hydraulic isolation existed between theupper and lower compartments (Fig. 4a). In the groundwater table treatment, during the transition from phase II
to III, soil water content in the sensor regions S3 and S4
were increased to the optimal soil moisture range, while
the upper compartment remained unaffected. The night
hours of phase III (days 12, 13, and 14) were found to befavorable for HR. However, a visible increase in the soil
water content was not observed in the dry compartment(Fig. 4a III). Phase III was further extended for three
more days and two nights, but no measurable HR was
observed by the sensors.

Fig. 5 Actual t(Ta) and potential (Tp) transpiration fluxes measured
during day and night from the (a) vertical split-root lysimeter and (b)horizontal split-root lysimeter

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Horizontal split-root lysimeter
Similarly, in the horizontal split-root lysimeter, when
the soil water content was not limiting on days 1, 2, 3,
and 8, the night-time transpiration rate was comparable
to the control experiment (Fig. 4c, Fig. 5b). During thesedays, night-time transpiration accounted for 8–12% of
the total daily transpiration loss. On days 6 and 7, when
the day-time transpiration reduced, the night-time transpiration flux was insignificant compared to the control.
Since the control and horizontal split-root lysimeter
experiments were carried out under the same environmental conditions, the soil moisture availability was the
single most important factor that controlled night-timetranspiration. Under water stress, the transpiration flux
overrides the water absorption rate during day time.
While the night-time transpiration flux was negligible,
the overall root water uptake during this period washigher than the normal rate, as shown by the dotted
portion of the S3 and S4 lines on days 5, 6, and 11 inFig. 4a and Fig. S4B. Also, the plant showed signs of
temporary wilting in the evening of these days alongwith overnight recovery apparently through xylem
refilling.

Discussion
In the current study, the quantitative and qualitative
implications of the CRWU and HR mechanisms were
investigated by alleviating the transpiration due to soil
moisture heterogeneity. Fully grown maize plants ofyield formation stage were used in all experiments dueto their extensive root system that helped in the effective
compartmentalization of roots. This further ensured
minimal impact of biomass change on transpiration
measurements (Koca and Erekul 2016). Also, a comparable soil water content recorded by all four sensors after
irrigation indicated that the soil was homogenously
packed.
Compensated root water uptake
In agreement with the previous studies (e.g., Šimůnek
and Hopmans 2009; Yadav et al. 2009; Faria et al.
2010), the split-root experiments suggested that CRWU
plays a critical role in the survival of plants underheterogeneous soil moisture conditions. In this study,
when one half of the root system in the vertical split-root

lysimeter was under severe water-stressed condition,
almost 100% compensation was observed due to anincrease in water uptake from the other half of thelysimeter. Similarly, in the horizontal split-root lysimeter, the water absorption capacity of the roots in thelower compartment, increased upto four times. Our
results suggest that compensation occurs when a fraction of the root biomass present in the wet zone becomes
extremely effective in absorbing water from the moist
soil compared to the roots present in the dry soil. Due tothis compensatory root water uptake, total water extraction was not substantially reduced, which is in agreement with previous reports (e.g., Cabelguenne andDebaeke 1998; Dara et al. 2015). However, when the
average soil water content in the lysimeter dropped
below a certain threshold, the roots were unable tofully compensate. Therefore, the transpiration
rate was not maintained at its optimal level. In agreement with our findings, Tan and Buttery (1982) reported
that root water uptake from the half root zone of peachseedlings was sufficient for meeting the transpiration
demand while the other part of the root zone was dry.
Similar findings were made in plants like potato(Stalham and Allen 2004; Liu et al. 2008), kiwifruitvines (Green and Clothier 1995), sorghum (Faria et al.
2010), tomato (Mingo et al. 2004), and bell pepper (Yaoet al. 2001).
The groundwater table treatment in the horizontal
split-root and column lysimeter experiments(Supporting Information S1) confirmed that even asmall portion of roots that can grow into the deep moist
soil layer might be of considerable advantage to plants
through CRWU (Šimůnek and Hopmans 2009; Jarvis
2011). Furthermore, when compensation occurs, therelative root distribution and water uptake profiles become dissimilar. Consequently, the root distribution
becomes a poor indicator of the root water uptake
distribution (Šimůnek and Hopmans 2009; Javaux
et al. 2013). When the soil water content is above 15%
in all regions, the root water uptake was relatively
proportional to the root density distribution. When thesoil water content in the high root density region
dropped below 15%, the water uptake from this region
decreased, and root water uptake shifted to next highest
root density region.
During phase II and III in the vertical split-root
lysimeter, when irrigation was switched from one compartment to another, the plant shifted their source ofwater uptake from the dry zone to the wet zone andPlant Soil

initiated CRWU without much delay. This also showsthat even when roots’ permeability was reduced due tosoil drying (North and Nobel 1991), it rapidly recovered
upon rewetting (Kang and Zhang, 2004; Liu et al. 2008).
This suggests that the alternate partial root-zone drying
method can be practiced effectively in maize. Furthermore, the same experimental strategy can be used forstudying compensatory nutrient uptake for effective
fertigation.
Root mediated hydraulic redistribution
Although there are several studies on HR, its implicationon the root water uptake is still unclear in maize andother crops (Wan et al. 2000; Zegada-Lizarazu andIijima 2004). Thus, we investigated the existence of
HR in maize under our experimental conditions. No
measurable HR was observed in any of our experiments,
even under a strong water potential gradient. Previous
studies have considered HR as a passive process that
occurs due to the difference in the soil water potential
between root zones (Mendel et al. 2002; Amenu andKumar 2008). Being a passive phenomenon, it was
reasonable to expect HR between the hydraulically isolated compartments, yet connected through the rootshoot junction. Previous studies by Faria et al. (2010)
and Meunier et al. (2018) observed the root mediatedwater redistribution from a high soil water content zone
(25%–35%) to medium dry zone (10%). In our experiments, there were multiple events in both vertical andhorizontal split-root lysimeter experiments where a partof the root system was exposed to medium dry conditions. However, no measurable HR was observed inboth cases.
Various studies have shown that night-time transpiration can be significant (e.g., Caird et al., 2007b;
Gleason et al. 2017; Claverie et al. 2018). In agreementwith this, it was observed that night-time transpirationaccounted for 8–12% of total daily transpiration under
optimal soil water supply. Water loss measured during
the night from all lysimeters was comparable to theircorresponding controls. When the maize plant was subjected to limited water availability, the night-time transpiration was reduced significantly, which is in agreement with Ludwig et al. (2006) and Howard and Donovan (2007).
An unexpected soil moisture depletion was noticed during night hours while the plant was
experiencing water stress, which is in contrary to

the observed night-time transpiration. During thisperiod, the actual transpiration was below its potential rate, and plant showed signs of temporary
wilting during day time and recovered during night.
The xylem refilling process seemed to be triggered
during night hours. As a result, water uptake washigher than the transpiration rate, as also reported by
Gleason et al. (2017). The night-time transpirationand xylem refilling processes might thus override
the HR on a diurnal basis in our experiment. Various other studies have found a substantial decreasein the magnitude of hydraulically redistributed water
when the night-time transpiration increased due tothe vapor pressure deficit (Howard et al. 2009;
Prieto et al. 2012). Likewise, the xylem refilling or
rehydration of plant tissues during the night time
may also reduce HR significantly (Prieto et al.
2012; Neumann et al. 2014; Yu et al. 2018).
There is some consensus that when the soil watercontent in the root zone reaches near the wilting point,
the change in rhizosphere properties such as root andsoil shrinking (North and Nobel 1991; Hu et al. 2011;
Zarebanadkouki and Carminati 2014), mucilage
shrinking and biodegradation (Zarebanadkouki and
Carminati 2014) may occur. These physico-chemicalchanges may lead to the formation of air-filled gaps
between the soil and the roots (Sharp and Davies, 1985;
Carminati, et al. 2013) or even to water repellence byroots due to drying of mucilage around the roots(Moradi et al. 2012). This may lead to substantial
localized hydraulic resistance in the soil at the root
vicinity that may lead to inadequate contact between
the soil and root surfaces. Thus, the hydraulic conductance at the soil-root interface could decrease, or evenresult in rupture of the hydraulic continuum, which
may limit the HR in extremely dry soil (Carminati and
Vetterlein 2013; Couvreur et al. 2020). Also, the low
soil hydraulic conductivity may reduce the diffusion of
exuded water from the roots, which may limit themeasurement of HR with soil moisture sensors. Thus,a strong water potential gradient may not necessarily
favor the occurrence of HR (Carminati and Vetterlein
2013; Couvreur et al. 2020). Another reason for not
observing the HR is the prompt triggering of the
CRWU on the next day before moisture can diffuse
from the root-soil interface into the soil due to the low
soil hydraulic conductivity. Moreover, the root development stage at which HR was determined would also

Plant Soil

affect the HR magnitude (Zegada-Lizarazu and Iijima,
2004; Shen et al. 2011).
Although evidence indicates that HR is a common
phenomenon in crops, its magnitude may vary among
the plants under different experiment conditions. For
instance, in a split-root study, Wan et al. (2000)
observed HR in the drought-tolerant strains of maize
but not in the drought-susceptible one. Also, HR was
not observed in maize using isotope analysis in a
split-root study by Zegada-Lizarazu and Iijima(2004). Likewise, Corak et al. (1987) detected HR
in alfalfa plants, whereas Dirksen and Raats (1985)
could not observe. Similarly, HR was detected inpearl millet (Vetterlein and Marschner 1993), pigeon
pea (Sekiya and Yano 2004), and oat (McCully1995). However, Zegada-Lizarazu and Iijima (2004)
could not detect HR in any of these species using thestable hydrogen isotope in a split-root setup. Further,
Shen et al. (2011) found that the contribution of HR
water towards transpiration in wheat was negligible,
while Valizadeh et al. (2003) found that HR helped in
the acquisition of nutrient from dry soil patch inwheat. In a split-root experimental study with isotopes to investigate the existence of HR in sixteen
agricultural crops by Zegada-Lizarazu and Iijima(2004), nine species did not show the evidence for
HR. Although there is limited evidence for HR inagriculture crops (e.g., Zegada-Lizarazu and Iijima
2004; Sekiya and Yano 2004), its magnitude is oftenvery low, which raises a question about the relevanceof HR in supporting the root water uptake demand
under field conditions, particularly on a diurnal scale.
For example, Cai et al. (2018) reported that hydraulically redistributed water in wheat was too low to be
detected by soil moisture sensors. The contradictoryobservations in terms of HR suggest the need to use
multiple techniques for the precise estimation of HR
in crops under field conditions (Rothfuss and Javaux
2016). The current method, which is based on soil
water content variations, is effective in providing thequantitative analysis of hydraulically redistributed
water. However, the measurement of soil water content is often limited to the vicinity of the sensor. In
our experiments, despite using multiple methods under varying soil moisture conditions, no measurable
HR was observed at the point of measurement. Further investigations are needed to verify if the HR canbe significant during a period of long-term reduced
transpiration conditions.

Conclusions
The contribution of CRWU and HR towards transpirationin plants under limiting soil moisture conditions remain
elusive. We used multiple methods in parallel to verify thepresence of CRWU and HR under varying soil moisture
conditions. Our results suggest that the majority of thetranspiration demand is aided by CRWU and not by HR.
Though the possible existence of HR under given experimental conditions cannot be excluded, HR is unlikely tohave a direct hydrological impact. Therefore, our researchsuggests that the role of HR in meeting the transpiration
demand can be neglected when modeling the transpirationin maize. The current research also suggests the use ofmaize plant as a model system for studying alternate partial
root-zone drying.
Acknowledgments AT is supported by SRF from Ministry of
Human Resource Development (MHRD), Govt. of India. AT isalso thankful to United States-India Educational Foundation(USIEF), India, for Fulbright-Nehru Doctoral Fellowship(FNDR). We are grateful to the reviewers for constructive criticisms and valuable comments, which were of great help in revising
the manuscript. We sincerely thank Jees Sebastian for editing andproofreading the manuscript.
Author’s contributions AT and BKY designed the experiments. AT performed the experiments. BKY, AT, and JS analyzed
the data. AT, BKY, and JS wrote the manuscript.

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