Plasticity of biomass allometry and root traits of two tomato cultivars under deficit irrigation × chemically induced drought hardening by Paclobutrazol

Abstract

Tomato yield is seriously affected by water stress. Paclobutrazol, a fungicide and plant growth retardant, has previously shown the potential to improve drought tolerance of crops. However, knowledge on the impact of Paclobutrazol on root system traits is scarce.
Seeds of two tomato cultivars were primed with three different rates of Paclobutrazol. After an establishment phase of 60 days, greenhouse-grown plants were partially subjected to deficit irrigation (60% ET). Subsequently, biomass and surface area allometry between plant organs and within the root system were determined. The morphology and architecture of the root system was studied in detail.
Changes in root system traits under deficit irrigation and after Paclobutrazol treatments were largely based on basal roots’ plasticity. The proportion of basal roots significantly increased with increasing Paclobutrazol concentration; deficit irrigation resulted in both cultivars in increased branching of basal roots. Cultivars differed in their plastic response of root system biomass, enhancing tap root and lateral root growth in one cultivar but basal root proportions in the other.
Paclobutrazol-priming of seeds facilitated basal root versus tap root system growth in tomato. It is hypothesized that basal roots, positioned in the topsoil, are most advantageous to maximize water uptake under (deficit) irrigation.

Full text

1 23
Irrigation Science
ISSN 0342-7188
Irrig Sci
DOI 10.1007/s00271-017-0554-8
Plasticity of biomass allometry and root
traits of two tomato cultivars under deficit
irrigation×chemically induced drought
hardening by Paclobutrazol
Jiangsan Zhao, Boris Rewald, Naftali
Lazarovitch & Shimon Rachmilevitch

1 23
Your article is protected by copyright and
all rights are held exclusively by Springer-
Verlag GmbH Germany. This e-offprint is
for personal use only and shall not be self-
archived in electronic repositories. If you wish
to self-archive your article, please use the
accepted manuscript version for posting on
your own website. You may further deposit
the accepted manuscript version in any
repository, provided it is only made publicly
available 12 months after official publication
or later and provided acknowledgement is
given to the original source of publication
and a link is inserted to the published article
on Springer's website. The link must be
accompanied by the following text: "The final
publication is available at link.springer.com”.

Vol.:(0123456789)
1 3
Irrig Sci
DOI 10.1007/s00271-017-0554-8
ORIGINAL PAPER
Plasticity ofbiomass allometry androot traits oftwo tomato
cultivars underdeficit irrigation×chemically induced drought
hardening byPaclobutrazol
JiangsanZhao1,2· BorisRewald1,2 · NaftaliLazarovitch1· ShimonRachmilevitch1
Received: 21 April 2016 / Accepted: 22 August 2017
© Springer-Verlag GmbH Germany 2017
seeds facilitated basal root versus tap root system growth in
tomato. It is hypothesized that basal roots, positioned in the
topsoil, are most advantageous to maximize water uptake
under (deficit) irrigation.
Introduction
Solanum is one of the largest angiosperm genera and
includes annual and perennial plants from diverse habitats.
Among them, Solanum lycopersicum L. (tomato) is a major
cash crop cultivated over an area of 4.8×106ha worldwide
in 2012, with an annual production>160×106t (FAOSTAT
2014). Tomato yields are dependent upon several genetic,
physiological, and environmental factors, amongst which
water stress is known to severely limit productivity (Loy-
ola etal. 2012; Wang and Frei 2011)—subsequently caus-
ing high economic losses (Harrak etal. 2001). In general,
water scarcity is responsible for the greatest yield losses
around the world and is expected to worsen due to climate
change-driven changes in rainfall amounts and pattern, and
an increasing competition of water for agricultural irrigation
with urban and industrial demands. An improved drought
tolerance of crops and enhancing water use efficiency in
agriculture is thus most desirable to maintain productivity
and global food security. This can be accomplished in a vari-
ety of ways, including the selection of drought-tolerant cul-
tivars, using grafted plants, or management techniques such
as partial root-zone drying (Mingo etal. 2004; Passioura
2012). The shoot drives water uptake and loss and is primar-
ily targeted by genetic engineering (Lawlor 2013); however,
root system architecture ultimately determines plant access
to water, and thus, set limits on shoot functioning. Root
traits associated with maintaining plant productivity under
drought include thin lateral roots, large specific root areas,
Abstract Tomato yield is seriously affected by water
stress. Paclobutrazol, a fungicide and plant growth retard-
ant, has previously shown the potential to improve drought
tolerance of crops. However, knowledge on the impact of
Paclobutrazol on root system traits is scarce. Seeds of two
tomato cultivars were primed with three different rates of
Paclobutrazol. After an establishment phase of 60days,
greenhouse-grown plants were partially subjected to deficit
irrigation (60% ET). Subsequently, biomass and surface area
allometry between plant organs and within the root system
were determined. The morphology and architecture of the
root system were studied in detail. Changes in root system
traits under deficit irrigation and after Paclobutrazol treat-
ments were largely based on basal roots’ plasticity. The pro-
portion of basal roots significantly increased with increas-
ing Paclobutrazol concentration; deficit irrigation resulted in
both cultivars in increased branching of basal roots. Culti-
vars differed in their plastic response of root system biomass,
enhancing tap root and lateral root growth in one cultivar but
basal root proportions in the other. Paclobutrazol priming of
Communicated by E. Fereres.
Electronic supplementary material The online version of this
article (doi:10.1007/s00271-017-0554-8) contains supplementary
material, which is available to authorized users.
* Boris Rewald
rewald@rootecology.de
1 French Associates Institute forAgriculture
andBiotechnology ofDrylands, Jacob Blaustein Institutes
forDesert Research, Ben-Gurion University oftheNegev,
Sede Boqer Campus, SedeBoqer, Israel
2 Department ofForest andSoil Sciences, University
ofNatural Resources andLife Sciences (BOKU), Vienna,
Austria
Author's personal copy

Irrig Sci
1 3
and great root length densities, especially in soil horizons
with available water (Comas etal. 2013; de Dorlodot etal.
2007; York etal. 2013).
Seed-grown tomatoes exhibit an allorhizic root system
(Osmont etal. 2007) often featuring basal roots, arising
from the base of the hypocotyl, and a prominent tap root
with lateral roots (see Zobel and Waisel 2010 for nomen-
clature). Architectural and morphological variability in the
tomato root system has previously been correlated with its
functionality; for example, thinner lateral roots and smaller
root systems, and increased or stable root:shoot ratios, have
previously been determined as favourable under water stress
(Kulkarni and Deshpande 2007; Romero-Romero etal.
2005). However, basal roots have received considerable less
attention compared to lateral roots emerging from the tap
root, although they can constitute a significant proportion of
the root systems of tomato and other dicotyledonous crops
(Bellini etal. 2014; Bui etal. 2015; Miguel etal. 2013). The
centripetal analysis of root orders continues to improve our
understanding of root system architecture and functional-
ity in woody plants (McCormack etal. 2015; Rewald etal.
2014). Its remains an open question if similar detailed anal-
yses can improve our understanding of the developmental
and, subsequently, the functional plasticity of dicotyledon-
ous crop root systems as well.
Genetic engineering has improved the drought toler-
ance of some tomato cultivars (Lawlor 2013; Mittler and
Blumwald 2010), although negative public opinion, espe-
cially in Europe, has triggered a debate on its use (Fresco
2013). The exogenous application of plant growth regulators
(“phytohormones”) has emerged as an alternative approach
for ‘instantly’ modifying plant phenology and physiology,
improving plants’ tolerance to drought (Peleg and Blumwald
2011). Various insecticides and fungicides are regularly used
for controlling pathogens of crop plants. Thus, the applica-
tion of chemicals acting both as crop protectants and as plant
growth regulators is desirable for simultaneously improving
the abiotic stress tolerance (Grossmann 1990, 1992). Among
a large number of pesticides and fungicides, Paclobutrazol
(Pbz; [2RS, 3RS]-1-[4-chlorophenyl]-4,4-dimethyl-2-[1,2,4-
triazol-1yl] pentan-3-ol) has shown positive impacts on the
drought-tolerance potential of tomato and other crops (Ber-
ova and Zlatev 2000; Buchenauer etal. 1984; Rajasekar and
Manivannan 2015; Somasundaram etal. 2009; Still and Pill
2004). A member of the triazole family, Pbz, has a five-atom
ring with three nitrogen atoms and two enantiomers, among
which (2R, 3R) provides fungicidal activity, while the (2S,
3S) enantiomer is involved in growth-regulating activity
by inhibiting the gibberellin synthesis (Nishizawa 1993;
Rademacher 2000). Previous studies found Pbz affecting
the vegetative growth of tomato, especially reducing shoot
elongation and leaf area, increasing root growth, with stable
or even increased yields under (low-dosed) Pbz application
(Berova and Zlatev 2000; Khan and Khokhar 1989; Mag-
nitskiy etal. 2006). Because previous studies often failed to
report tomato root system architecture in detail, and ignored
basal roots at large, our understanding of tomato root plas-
ticity under drought in general and after Pbz application in
specific is still limited.
This study is focussing on root architecture and morphol-
ogy of two tomato cultivars and possible phenotypic changes
induced by deficit irrigation and/or the plant growth regula-
tor Paclobutrazol. Two questions in regard to root systems
were studied in particular: (i) does deficit irrigation influence
plant allometry and root system architecture and morphol-
ogy of mature tomato plants and (ii) does Pbz-priming of
seeds cause plant allometric, and root architectural and mor-
phological changes? The study will thus help to understand
the mechanisms by which plant growth regulators such as
Paclobutrazol ameliorate the effects of water scarcity. Fur-
thermore, our in-depth analysis of the root system architec-
ture can be used to model more realistic tomato root systems
in the future.
Materials andmethods
Plant material andexperimental setup
The study was conducted on the commercial Solanum lyco-
persicum L. (tomato) cultivars ‘Ikram’ F1 and ‘Mose’ F1
(European Union 2011); seeds of the hybrids were supplied
by Syngenta Corp. Ltd. (Zeraim Gedera), Kibutz Reva-
dim, Israel. The two high yielding cluster tomato cultivars
are characterized as rather drought tolerant (cv. ‘Ikram’)
and more susceptible to water stress (cv. ‘Mose’), respec-
tively (Syngenta, personal comment), possesses a range
of increased resistances (Syngenta 2015), and are usually
grown in greenhouses.
The experiment was conducted in a climate-controlled
greenhouse at the Sede Boqer campus of the Ben-Gurion
University (30°52′08.04″N and 34°47′33″E), Israel from
November 6, 2011 to February 20, 2012. The growth con-
ditions inside the greenhouse were: max/min air temperature
25/17°C, mean relative humidity 70%, and photosynthetic
photon flux density of about 800µmolm−2s−1 at midday.
After surface sterilization, one seed was sown in the mid-
dle of a 16 l-lysimeter (height: 31cm, diameter: 26cm)
filled with sterilized sandy loam (51.4% silt, 8.8% clay,
and 39.8% sand; 24kg pot−1) at a soil depth of 1cm. Each
lysimeter had a highly conductive drain filled with rock
wool to control the matric potential at the bottom; a detailed
description is given in Ben-Gal and Shani (2002). Once a
day, water was applied automatically through pressure-
compensated surface drip irrigation with a discharge rate of
2lh−1 (Uniram, Netafim, Israel). Daily water balance was
Author's personal copy

Irrig Sci
1 3
calculated for each treatment based on ET=I–Dr–ΔW,
where I is the irrigation, Dr is the drainage, and ΔW is the
change in stored root-zone water. Plants were irrigated with
100 or 60% of their average back-day calculated ET; ET was
calculated separately for each cultivar and Pbz concentration
(see below). To minimize the water loss through evapora-
tion, each lysimeter was covered with a lid exhibiting a 5cm
opening for the hypocotyl; the drainage water (Dr) from each
lysimeter was collected and weighed, and ΔW was deter-
mined by weighing pots every other day, to calculate the
transpirational loss (data not shown).
A total number of 228 plants were arranged in 19 blocks
of 12 plants each (6 of each cultivar). Immediately after
planting, two randomly selected seeds per cultivar and block
were primed with 5ml of aqueous solutions holding three
different concentrations of Paclobutrazol (Pbz)—0ppm
(Control), 0.8ppm, and 1.6ppm. Until day, 63 after seed-
ing (DAS 63) all plants were irrigated with 100% of cal-
culated evaporative demand (100% ET) by surface drip
irrigation. Fertilizer (Polyfeed water-soluble fertilizer,
NPK 14:7:28+1% MgO, Haifa Chemicals, Israel) was
applied with the irrigation water at a constant concentra-
tion of 1kgm3. From DAS 64 until the end of the experi-
ment (DAS 85–88) two different irrigation treatments, 100%
of the evaporative demand (100% ET, Control) and 60%
of evaporative demand (60% ET, moderate water deficit)
were established (systematically within each block; lasting
22–25days). According to irrigation levels used in the previ-
ous studies on tomato (Ozbahce and Tari 2010), the applied
deficit irrigation of 60% ET constitutes a moderate drought
stress. Flowers were removed every other day, but no side
shoots or leaves were pruned to study vegetative effects; the
assessment of tomato yield quantity and quality was beyond
the scope of this study. Thus, a full factorial experiment
with the factors Paclobutrazol application (yes or no) or
concentration (0, 0.8 and 1.6ppm)×water availability (100
and 60% of evaporative demand) was established at DAS 63
allowing evaluating source effects and possible interactions.
Biomass
During the course of the experiment, two harvests were
conducted; three randomly selected blocks were harvested
at DAS 60–63 (harvest 1, i.e., before diverging irrigation
treatments; data not shown), eight randomly selected blocks
at DAS 85–88 (harvest 2). The eight remaining blocks were
discarded. Replicate numbers were n=6 (harvest 1) or
n=8 (harvest 2) per treatment. The shoot was severed at
the soil surface and manually separated into leaves and stem.
Three leaves were collected for morphological analyses (see
below), and the rest was stored in paper bags, dried (65°C,
48h), and weighed to a precision of ±0.01g. The soil was
carefully slid on a 2mm mesh and the root system was
rinsed with a soft water jet until all adhering soil particles
were washed off. Root systems were stored in water-filled
plastic bags at 4°C until morphological analyses were per-
formed (see below); then, the root system was dried (65°C,
48h) and weighed separately to a precision of ±0.1mg. The
root:shoot biomass ratio (R:S ratio) was calculated.
Morphology andarchitecture
Leaf morphology
Specific leaf area (SLA, cm2g−1) was determined on a total
of three leaves per plant and selected during harvest from
the upper, median, and lower part. Leaf blades were wrapped
in moist paper and stored at 4°C until scanning. The area
of the fresh blades was determined using the PC software
WinFolia 2013 (Regent Instruments, Quebec, Canada); dry
mass (65°C, 48h) was determined to a precision of ±0.01g.
Total leaf area per plant was calculated by multiplying the
determined SLA by the total dry weight of leaves.
Root architecture andmorphology
The root system was divided into basal roots (i.e., roots
emerging at the hypocotyl) and the tap root system (i.e., tap
root including lateral roots). After severing all basal roots
from the hypocotyl, 4–6 branches of basal roots were ran-
domly sampled per treatment for root order analysis. Root
dissection into three root orders was carried out on wet paper
towels to prevent desiccation. Most distal root segments
(root tips) were named first-order roots, roots that possessed
only first-order side roots were named second-order roots,
and root segments bearing only first- and second-order side
roots were named third-order roots (Rewald etal. 2011). The
maximum root order (i.e., maximum branching frequency)
was determined by counting branching orders centripetally
at each of the analysed basal root branches. The tap root
with adhering lateral roots was analysed separately. All dis-
sected basal root segments and the whole tap root system
were scanned on a flat-bed scanner (400dpi, grey scale;
Epson Expression10,000XL with transparency unit). The
digital images were analysed for root length, surface area
(SA, cm2), volume, and diameter (WinRhizo 2005c; Régent
Instruments Inc., Québec, QC, Canada). Finally, all root seg-
ments were oven dried (48h, 65°C) and weighed separately
to a precision of ±0.1mg (CP225D; Sartorius, Göttingen,
Germany). Specific root area (SRA, cm2g−1), diameter,
and tissue density (Davis etal. 1985) were calculated per
basal root order 1–3. The total and relative dry weight (DW)
and SA of each basal root order per root branch were cal-
culated. The tap root system dry weight (tap RDW) and tap
root system SA were calculated for all non-basal roots; the
Author's personal copy

Irrig Sci
1 3
proportion of basal roots on the total root system DW (basal
root proportion) is given.
Statistical analysis
Statistical calculations were conducted with the PC program
SAS 9.2, 32 bit (SAS Institute, Cary, NC, USA). Data sets
were tested for Gaussian distribution with the Shapiro–Wilk
test and for homogeneity of variances with the Levene test.
A general linear model (proc GLM) was used to test for
significant influences of cultivar, Pbz application (yes, no)
or Pbz concentration, and irrigation regime (harvest 2) on
biomasses, architectural and morphological parameters.
Non-significant cross effects were omitted by rerunning the
GLM with significant cross effects only. A t test was used for
pairwise comparison of root and shoot biomasses, surface
area distribution per root order, and tissue density; signifi-
cance level α was set 0.05.
Results
Plant biomass andallometry
Total plant biomass at DAS 60–63 (harvest 1) ranged
between 1.6 to 2.3g DW and was significantly lower in Pbz-
treated plants (irrespective of Paclobutrazol concentration),
with no significant difference between cultivars (data not
shown). At harvest 2 (DAS 85–88), total plant biomass was
significantly influenced by cultivar, Pbz application, and
irrigation treatment (Fig.1; Table1). The cultivar Ikram
possessed in general a 15–20% higher total biomass than
the cultivar Mose (Fig.1), mostly based on a greater leaf
biomass. In both cultivars, Pbz application and drought led
to a reduction in total biomass (Fig.1); less leaf, stem, and
root biomass contributed to the observed reductions. Inter-
estingly, a higher Pbz concentration (1.6ppm) significantly
reduced the stem biomass to a further extent and thus caused
a further reduction of the total plant biomass (Supplemen-
tary Table1). The root-to-shoot (R:S) biomass ratio was
affected by cultivar, Pbz application, and irrigation treat-
ment (Table1), while Pbz concentration (0.8, 1.6ppm) had
no deviant effect (Supplementary Table1). R:S ratios were
generally lower in cv. Ikram and after Pbz application, and
higher under deficit irrigation (60% ET; Fig.1).
Root biomass andarchitecture
At DAS 60–63 (harvest 1), Pbz application (i.e., applica-
tion of 0.8 or 1.6ppm Pbz) has significantly (P=0.008)
reduced the tap root system biomass of both cultivars, while
no explicit influence on basal root biomass and the biomass
proportion of basal roots was evident (data not shown). At
DAS 85–88 (harvest 2), basal and tap root system biomasses
Fig. 1 Shoot and root bio-
masses (DW) of two tomato
cultivars [cv. Ikram, (a); cv.
Mose, (b)] treated with three
Paclobutrazol concentrations (0,
0.8, and 1.6ppm) and irrigated
full (100% Evapotranspira-
tion, ET; black bars) and at a
deficit level (60% ET; white
bars) at DAS 85–88 (Harvest
2). Shoot biomass is split into
stem and leaf biomasses; the
root:shoot ratio of each treat-
ment is given below. Different
capital letters denote significant
differences between shoot and
root biomasses in cv. Ikram,
different lower case letters in cv.
Mose (t test, P<0.05; n=4–6;
mean±SE)
Author's personal copy

Irrig Sci
1 3
were significantly affected by Pbz application to the seeds
and the irrigation type (Table2); in addition, the tap root
system biomass was significantly influenced by cultivar and
a cultivar×irrigation cross effect (Table2). The proportion
of basal root biomass on the whole root system was signifi-
cantly influenced by all three factors and a cultivar×irri-
gation cross effect (Table2). The tap root system was less
pronounced under 1.6ppm Pbz compared to 0.8ppm Pbz
(Fig.2, Supplementary Table2). In detail, Pbz application
decreased basal root biomass by up to 21% under well-
watered (100% ET) conditions, and up to 25% under deficit
irrigation (60% ET; Fig.2). Interestingly, priming the seeds
with 0.8ppm Pbz led to lower absolute basal root biomasses
compared to control plants than application of 1.6ppm Pbz;
Table 1 Summary of three-
way ANOVA results testing the
effects of tomato cultivar (cv.
Ikram, Mose), Paclobutrazol
application (with or without
Pbz), and irrigation (100%, 60%
ET) on biomass variables and
the root:shoot (R:S) ratio at
DAS 85–88 (Harvest 2)
Significant effects in bold
The only significant (P=0.039) cross effect was Pbz application× irrigation for the variable stem bio-
mass; non-significant cross effects are omitted
Variable Cultivar Pbz application Irrigation
F P F P F P
Total biomass (g) 15.78 <0.001 27.60 <0.001 178.93 <0.001
Leaf biomass (g) 51.50 <0.001 9.71 0.028 159.04 <0.001
Stem biomass (g) 0.02 0.879 33.33 <0.001 130.87 <0.001
Root biomass (g) 0.75 0.390 29.74 <0.001 22.88 <0.001
R:S ratio (gg−1) 9.20 0.004 4.20 0.045 18.50 <0.001
Table 2 Summary of three-way ANOVA results testing the effects of
tomato cultivar (cv. Ikram, Mose), Paclobutrazol application (with or
without Pbz), and irrigation (100%, 60% ET) on basal root biomass,
tap root system biomass, and the proportion of basal roots on total
root system biomass (basal root proportion) at DAS 85–88 (Harvest
2)
Significant effects in bold
Non-significant (ns) cross effects are omitted
Variable Cultivar Pbz application Irrigation Cv.×irrigation
F P F P F P F P
Basal root biomass (g DW) 0.37 0.546 6.95 0.011 11.08 0.002 ns
Tap root system biomass (g DW) 8.37 0.005 59.94 <0.001 14.69 <0.001 9.68 0.003
Basal root proportion (gg−1) 6.67 0.012 10.94 0.002 0.85 0.359 5.38 0.024
Fig. 2 Root system biomass
(DW) of two tomato cultivars
[cv. Ikram, (a); cv. Mose, (b)]
treated with three Paclobutra-
zol concentrations (0, 0.8, and
1.6ppm) and irrigated full
(100% Evapotranspiration,
ET; black bars) and at a deficit
level (60% ET; white bars) at
DAS 85–88 (Harvest 2). Root
biomass is split into basal root
and tap root system biomass;
the proportion of the basal
root system on the whole root
system is given below. Different
capital letters denote signifi-
cant differences between total
root biomasses in cv. Ikram,
different lower case letters in cv.
Mose (t test, P<0.05; n=4–6;
mean+SE)
Author's personal copy

Irrig Sci
1 3
this trend was similar pronounced in both cultivars. In con-
trol plants (0ppm Pbz), water deficit reduced basal root
biomass by about 15%; no significant Pbz×irrigation cross
effects on basal root biomass were found (Table2). Tap root
system (i.e., tap root and laterals) biomass of cv. Mose was
generally greater than those of cv. Ikram; independent of
the cultivar, its dry weight strongly declined (20–55%) in
Pbz-treated and water-stressed plants, with the lowest val-
ues under 1.6ppm Pbz and low water supply (Fig.2). The
dry matter ratio of basal roots (compared to whole root sys-
tem dry weight) was high, i.e., about 70–89% of the whole
root system dry weight was constituted by basal roots. The
root system architecture was significantly influenced by
Pbz, with more basal roots with increasing Pbz concentra-
tion. Interestingly, the proportion of basal roots was higher
in water-stressed plants of the cv. Mose compared to the
well-watered control, but a minor plasticity was found in
cv. Ikram—statistically evidenced by a significant culti-
var×irrigation cross effect (Fig.2; Table2).
Leaf androot morphology, andsurface areas
The specific leaf area (SLA) was significantly higher in cv.
Mose and under water stress; no significant influence of Pbz
application or concentration on SLA was found (Tables3,
4; Supplementary Table3). Because total leaf biomass was
reduced under deficit irrigation (see above), the total leaf
area (leaf SA) of both cultivars was significantly reduced
by up to 20%.
The specific root area of basal roots (SRABasal) was sig-
nificantly higher in cv. Mose with about 1200–1600cm2 g
DW−1 than in cv. Ikram; while SRABasal seemed to increase
in Pbz-treated plants, this effect was only marginally sig-
nificant in the ANOVA results due to the high variability
Table 3 Summary of three-
way ANOVA results testing the
effects of tomato cultivar (cv.
Ikram, Mose), Paclobutrazol
application (with or without
Pbz), and irrigation (100%, 60%
ET) on specific leaf area (SLA),
specific root area of basal roots
(SRABasal), total leaf, basal root
and tap root system surface
areas (SA), and root:leaf SA
ratio at DAS 85–88 (Harvest 2)
Significant effects in bold
Non-significant cross effects are omitted
Variable Cultivar Pbz application Irrigation
F P F P F P
SLA (cm2 g−1) 38.35 <0.001 0.91 0.343 5.17 0.027
SRABasal (cm2 g−1) 4.85 0.032 2.72 0.104 0.97 0.329
Leaf SA (cm2) 3.14 0.081 0.47 0.495 10.16 0.002
Basal root SA (cm2) 4.78 0.033 0.01 0.908 0.36 0.551
Tap root system SA (cm2) 8.02 0.006 18.36 <0.001 0.00 0.971
Total root SA (cm2) 5.99 0.017 0.23 0.633 0.37 0.545
Root:leaf SA ratio (cm2 cm−2) 3.14 0.083 0.47 0.495 10.16 0.002
Table 4 Specific leaf area (SLA), specific root area of basal roots
(SRABasal), total leaf, basal root and tap root system surface areas
(SA), and root:leaf SA ratio at DAS 85–88 (Harvest 2) of two tomato
cultivars (cv. Ikram, Mose) treated with three Paclobutrazol concen-
trations (0, 0.8, and 1.6ppm Pbz) and under two irrigation regimes
(100%, 60% ET)
Capital letters denote significant differences within parameters and between treatments in the cv. Ikram, and lower case letters denote significant
differences within parameters and between treatments in the cv. Mose (t test, P<0.05; n=8; n (SRABasal)=4–6, mean±SE)
Cultivar Pbz (ppm) Irriga-
tion (%
ET)
SLA (cm2 g−1) SRABasal (cm2
g−1)
Leaf SA (cm2) Basal root SA
(cm2)
Tap root syst. SA
(cm2)
Root:leaf SA
ratio (cm2 cm−2)
Ikram 0 100 66.7±6.0 A 792±45 B 1632±329 AB 2224±250 A 179±39 AB 1.97±0.70 AB
0.8 100 72.1±5.4 A 971±186 AB 1588±141 A 1833±254 A 103±11 B 1.23±0.15 B
1.6 100 65.3±3.4 A 956±69 B 1373±113 AC 2482±390 A 87±27 B 1.89±0.31 AB
0 60 73.7±1.6 A 957±100 B 1039±81 BC 1982±216 A 245±40 A 2.22±0.36 AB
0.8 60 71.7±5.9 A 1116±160 AB 903±69 B 1938±239 A 118±10 B 2.36±0.31 A
1.6 60 75.9±4.5 A 1460±158 A 888±44 B 2292±365 A 89±9 B 2.65±0.33 A
Mose 0 100 94.3±4.8 a 1165±255 a 1693±74 a 2727±578 a 236±38 a 1.73±0.32 b
0.8 100 100.2±9.5 a 1630±564 a 1494±93 a 2825±724 a 243±30 a 2.14±0.59 ab
1.6 100 75.3±3.3 b 1153±70 a 1151±54 b 2654±492 a 109±22 bc 2.44±0.50 ab
0 60 111.5±7.4 a 1198±63 a 1032±102 b 2488±284 a 240±55 a 2.67±0.21 ab
0.8 60 108.0±12.5 a 1461±201 a 946±105 b 2567±419 a 194±43 ab 3.05±0.58 a
1.6 60 98.0±13.2 ab 1355±69 a 961±124 b 2507±506 a 102±8 c 2.87±0.60 a
Author's personal copy

Irrig Sci
1 3
(Tables3, 4). The total root system surface area (SA) and
both subparts, basal roots and the tap root system SA, were
lower in cv. Ikram compared to cv. Mose (Tables3, 4). Pbz
application has a significant effect on the tap root system SA,
with smaller areas under increasing concentration (Table3;
Supplementary Table3), but has no effect on basal root SA.
Surprisingly, root surface areas were rather stable under both
irrigation regimes; because of the leaf area changes, the ratio
between root and leaf surface areas was significantly higher
under deficit irrigation and with slightly higher values in cv.
Mose compared to cv. Ikram (Tables3, 4).
Branching pattern ofbasal roots andmorphology
ofroot orders
The branching of basal roots differed between cultivars, with
significantly greater relative root biomass/surface area in
second-order laterals and consequently less relative biomass/
significantly less relative surface area in cv. Ikram compared
to cv. Mose (Tables5, 7; Fig.3). Neither relative biomass
nor surface area of first orders laterals (i.e., root tips) of basal
roots did differ significantly between cultivars. Deficit irriga-
tion caused significantly higher relative biomasses and sur-
face areas of first-order laterals in both cultivars (Tables5,
7; Fig.3). Pbz application (Table5) or concentration (data
not shown) did not influence the proportions of root orders
1–3 in basal roots.
The specific root area (SRA) differed significantly
between root orders, with root tips having the highest, root
order three the lowest SRA (data not shown). Within orders,
SRA of root order 1 was stable; SRA of root orders 2 and 3
differed significantly between cultivars, with cv. Mose hav-
ing a higher SRA (Tables6, 7). The observed differences in
SRA were based both on changes in root segment diameter
and tissue density (Tables6, 7; Fig.4). Consequently, diame-
ters of root orders 2 and 3 were larger in cv. Ikram, and tissue
density was lower in cv. Mose. While root morphology did
not generally react to Pbz, a significant cross effect between
cultivar and Pbz concentration was found for tissue density
of basal root orders 1 and 2 (Table6). Tissue density (TD)
tended to be negatively correlated with Pbz concentration in
cv. Mose, TD seems to be positively correlated with Pbz in
cv. Ikram (Table6; Fig.4).
Discussion
Influence ofdeficit irrigation onbiomass allometry,
root architecture, androot morphology oftwo tomato
cultivars
In general, water scarcity negatively affects vegetative plant
growth and yield. Tomato is a high water demanding crop,
thus requiring irrigation throughout the growing season in
arid and semi-arid areas; in these areas, rainfall is rare, but
they are providing otherwise favourable growth conditions
(high photosynthetically active radiation and temperature).
While water deficit during certain stages of the growing sea-
son improves tomato fruit quality, water limitations normally
cause fruit yield losses (Ozbahce and Tari 2010; Patanè and
Cosentino 2010). Thus, it comes as no surprise that defi-
cit irrigation resulted in lower biomass of leaves, stem, and
roots in both tested tomato cultivars (Table1; Fig.1). Both
cultivars increased their root:shoot (R:S) biomass ratios
under deficit irrigation; a higher R:S ratio is commonly
thought to be beneficial under limited water supply, increas-
ing the water uptake capacity relative to the transpiring area
(Chapin etal. 1993). The cultivar Mose has generally higher
R:S ratios under deficit irrigation than cv. Ikram, which pos-
sesses a higher leaf biomass under both irrigation regimes.
Because the leaves of cv. Ikram have a considerable lower
SLA, no significant differences in total leaf area between
were found between cultivars (Tables3, 4). Corresponding
to the changes in R:S ratios, the lower total leaf surface area
(SA) and the relative constant root SA under deficit irriga-
tion resulted in higher root:leaf SA ratios in both cultivars.
However, focusing on total root biomass or total root SA
can be misleading when assessing relevant plant traits under
Table 5 Summary of three-
way ANOVA results testing the
effects of tomato cultivar (cv.
Ikram, Mose), Paclobutrazol
application (with or without
Pbz), and irrigation (100%, 60%
ET) on the relative proportion
of biomass and surface area
(SA) of root orders 1, 2, and 3
within braches of basal roots at
DAS 85–88 (Harvest 2)
Significant effects in bold
Non-significant (ns) cross effects are omitted
Variable Root order Cultivar Pbz application Irrigation Culti-
var×Pbz
F P F P F P
Rel. biomass (%) 1 0.24 0.627 0.03 0.852 13.49 <0.001 ns
2 7.81 0.007 0.27 0.606 0.81 0.372 ns
3 1.08 0.304 1.67 0.201 3.76 0.057 ns
Rel. SA (%) 1 0.04 0.843 2.19 0.144 13.43 <0.001 ns
2 5.63 0.021 0.52 0.474 4.97 0.030 ns
3 13.90 <0.001 3.68 0.060 1.13 0.293 5.00 0.029
Author's personal copy

Irrig Sci
1 3
drought stress. Not all roots contribute equally to water
uptake, either due to a ontogenetic, functional differentiation
within root branches (Rewald etal. 2011; Zarebanadkouki
etal. 2014) or due to a diverging access of individual roots
to water within the soil profile (Maeght etal. 2013; Schenk
and Jackson 2002). In efficiently irrigated plants, i.e., irriga-
tion schemes avoiding runoff and deep percolation, lateral
root placement in the topsoil is most effective (El-Nesr etal.
2014), while in rain-fed systems and in light-textured soils,
a deeper tap root system and a redistribution of branch root
density from the surface to depth are beneficial to increase
the access to water (Lynch 2013; Wasson etal. 2012). In
general, plants possess higher root densities in the upper part
of the root zone; however, several root phenes can further
enhance resource acquisition in the topsoil (Miguel etal.
2015). Basal roots are especially primed to tap resources in
topsoil layers, e.g., phosphorous (Miguel etal. 2013), due to
their elevated place of origin (at the base of the hypocotyl)
Fig. 3 Relative surface area
(SA; %) of the root orders 1, 2,
and 3 within basal root branches
of two tomato cultivars [cv.
Ikram, (a); cv. Mose, (b)]
treated with three Paclobutra-
zol concentrations (0, 0.8, and
1.6ppm) and irrigated full
(100% Evapotranspiration, ET;
black bars) and at a deficit level
(60% ET; white bars) at DAS
85–88 (Harvest 2). Root order
1 is the root tip. Discrepan-
cies to 100% SA between the
sum of root orders 1, 2, and 3
are caused by the occasional
occurrence of root orders >3
(see Table7). Different capital
letters denote significant dif-
ferences between total root
biomass in cv. Ikram, different
lower case letters in cv. Mose
(t test, P<0.05; n=4–6;
mean+SE)
Author's personal copy

Irrig Sci
1 3
compared to lateral roots emerging from the tap root. While
Miguel etal. (2013) found that basal root numbers of com-
mon bean did not vary with phosphorous availability, and
are thus not plastic to all environmental changes, our results
show that basal roots’ biomass decreases significantly under
deficit irrigation in both tomato cultivars. At the same time,
the relative tap root proportion increases in cv. Ikram and
decreases in cv. Mose (Fig.2; Table2)—causing significant
changes in root system architecture (RSA, i.e., basal root
proportion compared to tap root incl. laterals). However,
the total surface area of basal roots did not change signifi-
cantly under deficit irrigation (Table4), and the underlying
morphological traits must have changed simultaneously,
emphasizing on the importance of basal roots to sustain
water uptake under deficit irrigation.
Root morphological traits associated with maintaining
plant productivity under drought include thin lateral roots
and large specific root areas (SRA) (Comas etal. 2013; de
Dorlodot etal. 2007; York etal. 2013). In this study, the
overall SRA of basal roots of both tomato cultivars did not
increase significantly under deficit irrigation. However, our
in-depth analyses of basal root branching pattern showed
that fine-scale morphological changes unnoticed by coarser
analyses of whole branches take place nevertheless (Figs.3,
4; Tables5, 6, 7). Both the significantly increased relative
surface area as well as the increased relative biomass of root
order 1 emphasise that basal roots of both cultivars have sig-
nificantly more root tips under deficit irrigation than under
well-watered conditions. Our study showed that root seg-
ments of similar branching hierarchy (i.e., centripetal root
orders) are clearly separable according to morphological
traits (Table7) and that the relative proportion of individual
root orders is subject to change under water deficit (Tables5,
6, 7). Previously, lateral root branching density has been
shown to react very plastic to different nutrient regimes
(see Postma etal. 2014 and references within). However, to
the best of our knowledge, we are the first to show that the
branching order frequency in basal roots of a dicotyledonous
crop is also subject to change under water scarcity. Because
it is not clear what the optimal branching density might be,
and how different environmental factors shift this optimum,
further studies determining root order- and root type-specific
traits of crop plants are urgently needed. Implications of
the changes for water uptake efficiency must remain open
until the uptake capacity and the carbon costs of individual
tomato root orders have been determined—techniques such
as neutron radiography (Zarebanadkouki etal. 2014) could
provide the technical means to trace the uptake of deuterated
water by individual orders. However, it has been previously
shown that highly branched roots accumulate under drip irri-
gation—this has been suggested to be economically prudent
in terms of increasing the uptake efficiency (water uptake per
invested carbon) (Araujo etal. 1995). In summary, a sus-
tained basal root area—by enhanced branching—placed in
soil areas with available water, i.e., the topsoil layers under
drip irrigation, is suggested to be a major plastic trait of
tomato root systems’ architecture and morphology to sustain
water uptake under deficit irrigation.
Influence ofPaclobutrazol onbiomass allometry, root
architecture, androot morphology oftwo tomato
cultivars
Previous studies have addressed biochemical and physi-
ological effects of triazole compounds on different plants
including tomato: e.g., hormonal changes (Couée etal.
2013; Fletcher etal. 1999; Rademacher 2000; Saito etal.
2006), chlorophyll content, and photosynthetic rates (Ber-
ova and Zlatev 2000; Panneerselvam etal. 1998). However,
the most commonly reported change in Pbz-treated plants,
both woody and non-woody crops, is a modification of the
root:shoot ratio (R:S), often in favour of the root system
Table 6 Summary of three-
way ANOVA results testing the
effects of tomato cultivar (cv.
Ikram, Mose), Paclobutrazol
application (with or w/o Pbz),
and irrigation (100%, 60% ET)
on specific root area (SRA),
diameter, and tissue density of
root orders 1, 2, and 3 of basal
roots at DAS 85–88 (Harvest 2)
Significant effects in bold
Non-significant (ns) cross effects are omitted
Variable Root order Cultivar Pbz applica-
tion
Irrigation Cv.×Pbz
F P F P F P F P
SRA (cm2 g−1) 1 0.78 0.382 0.04 0.845 0.09 0.770 ns
2 9.84 0.003 0.16 0.687 0.45 0.507 ns
3 16.53 <0.001 0.03 0.870 0.10 0.756 ns
Diameter (mm) 1 3.47 0.068 0.33 0.567 3.67 0.060 ns
2 11.08 0.002 0.19 0.663 0.04 0.847 ns
3 6.52 0.013 0.48 0.491 0.26 0.615 ns
Tissue density (gcm−3) 1 0.22 0.638 1.19 0.280 7.11 0.001 4.67 0.035
2 6.43 0.014 0.42 0.522 1.66 0.202 6.76 0.012
3 14.39 <0.001 0.14 0.713 16.24 <0.001 ns
Author's personal copy

Irrig Sci
1 3
Table 7 Relative distribution of biomass (Biomass; %), specific root area (SRA) and diameter of the first three root orders, and maximum numbers of root orders detected in the dissected basal
root braches (severed at the hypocotyl) at DAS 85–88 (Harvest 2) of two tomato cultivars (cv. Ikram, Mose) treated with three Paclobutrazol concentrations (0, 0.8, and 1.6ppm Pbz) and under
two irrigation regimes (100%, 60% ET)
(n=4–6, mean±SE) (see Tables5, 6 for ANOVA results). Discrepancies between Σrel. biomass of root orders 1, 2, and 3 and 100% are caused by the occasional occurrence of orders >3
Cultivar Pbz (ppm) Irrigation
(% ET)
Rel. biomass (%) SRA (m2 g−1) Diameter (mm) Max. # of root
orders per
branch
Root order Root order Root order
123123123
Ikram 0 100 22±3 28±7 22±3 0.18±0.01 0.11±0.02 0.04±0.01 0.37±0.01 0.57±0.05 0.75±0.12 3–5
0.8 100 21±5 41±8 21±4 0.27±0.02 0.08±0.01 0.04±0.01 0.35±0.01 0.55±0.07 0.62±0.10 3–4
1.6 100 16±1 44±12 16±1 0.20±0.02 0.08±0.01 0.05±0.01 0.36±0.02 0.56±0.13 0.81±0.31 3–6
0 60 27±2 30±6 27±2 0.21±0.01 0.09±0.01 0.04±0.01 0.36±0.02 0.54±0.11 0.72±0.14 3–5
0.8 60 28±2 32±4 28±2 0.18±0.00 0.09±0.01 0.05±0.01 0.41±0.01 0.52±0.03 0.88±0.14 3–5
1.6 60 28±6 24±4 28±6 0.19±0.02 0.11±0.02 0.05±0.00 0.39±0.02 0.48±0.05 0.72±0.10 3–5
Mose 0 100 22±3 22±5 22±3 0.21±0.03 0.11±0.01 0.06±0.01 0.35±0.01 0.43±0.05 0.60±0.08 3–5
0.8 100 22±2 24±4 22±2 0.19±0.01 0.12±0.01 0.07±0.01 0.33±0.02 0.37±0.02 0.51±0.07 4–6
1.6 100 20±4 22±2 20±4 0.20±0.01 0.11±0.02 0.06±0.01 0.38±0.04 0.43±0.05 0.62±0.12 4–5
0 60 29±2 28±2 29±2 0.20±0.02 0.11±0.01 0.08±0.00 0.35±0.02 0.42±0.04 0.46±0.04 4–5
0.8 60 25±3 26±4 25±3 0.22±0.01 0.12±0.02 0.06±0.00 0.38±0.02 0.46±0.04 0.65±0.10 3–5
1.6 60 31±5 22±5 31±5 0.21±0.01 0.12±0.01 0.06±0.01 0.35±0.01 0.44±0.03 0.66±0.11 3–5
Author's personal copy

Irrig Sci
1 3
(Navarro etal. 2007; Tanis etal. 2015). This change was
either explained by the larger inhibition of shoot growth
compared to root growth (Grossmann 1992; Jung etal.
1987) or on an induced formation of lateral roots by Pbz
(Davis etal. 1985; Upadhyaya etal. 1986; Wiesman and
Riov 1994). While the biomasses of all organs decreased
under Pbz treatment in this study, the R:S biomass ratio of
both tomato cultivar was significantly reduced after Pbz
application (Fig.1; Table1); no significant differences
between R:S ratios of both Pbz concentrations occurred
(Supplementary Table1). Interestingly, a similar reduction
in R:S ratios occurred under both well-watered and deficit
irrigation. Our results are thus in contrast to the previous
studies on other tomato cultivars reporting an increased R:S
ratio after Pbz application (Berova and Zlatev 2000; Silva
2008). The divergent results of these previous studies might
be explained by the different ways and times and the Pbz was
applied, i.e., foliar application at later developmental stages.
Still and Pill (2004) previously found that the root and shoot
biomasses of Pbz-sprayed tomato plants were lower than
Fig. 4 Tissue density (gcm−3)
of the root orders 1, 2, and 3
within basal root branches of
two tomato cultivars [cv. Ikram,
(a); cv. Mose, (b)] treated with
three Paclobutrazol concentra-
tions (0, 0.8, and 1.6ppm) and
irrigated full (100% Evapotran-
spiration, ET; black bars) and
at a deficit level (60% ET; white
bars) at DAS 85–88 (Harvest
2). Root order 1 is the root tip.
Different capital letters denote
significant differences between
total root biomass in cv. Ikram,
different lower case letters in cv.
Mose (t test, P<0.05; n=4–6;
mean+SE)
Author's personal copy

Irrig Sci
1 3
those of plants grown out of Pbz-primed seeds. Thus, further
studies are needed to determine possible divergent hormonal
changes after applying Pbz priming of seeds compared to
foliar application.
A close look into the root system architecture (RSA) of
tomato revealed that the proportion of basal roots signifi-
cantly increases with increasing Pbz concentration (Fig.2;
Table2; Supplementary Table2). Because the specific root
area of basal roots tended (P=0.104) to be larger after
Pbz application (Tables3, 4), Pbz-treated plants kept the
total surface area (SA) of basal roots very stable, while
the surface area build by the tap root and adhering lateral
roots declined significantly (Tables3, 4). Previously, it has
been reported that Pbz decreases the elongation of primary
roots of 4-day-old tomato seedlings (Butcher etal. 1990),
but to our best of knowledge, we are the first to report a
dramatic change in mature plants’ RSA by Pbz. Changes
in the root elongation might be linked with the increase in
cytokinins, which determine cell division, and the decrease
in gibberellic acids (GA), which promote cell elongation, by
Pbz (Butcher etal. 1990; Vanstraelen and Benková 2012).
However, it remains an open question why basal roots are
not equally affected by Pbz; Butcher etal. (1990) suggested
previously that part of root growth is GA independent and it
can be speculated that the level of GA dependency is differ-
ent in roots of different origins [see Bellini etal. (2014) for
a recent review on lateral root formation]. Partially, the use
of sandy loam, a common agricultural soil in the area, might
underlie the increased proportion of basal root. Most of the
previous experiments were conducted in rather artificial
substrates, e.g., peat/vermiculite or peat/perlite/vermiculite
mixtures (Latimer 1992; Marshall etal. 2000), mixture of
sand, black peat, and a clay-soil (Navarro etal. 2007), or a
1:1:1 mixture of sand, leafmold, and soil (Baninasab 2009).
These growth media were quite different from sandy loams
which feature a higher soil compaction and causes more fric-
tion, especially under water deficit.
However, while our study did show a major change in
tomato RSA after Pbz treatment of seeds in favour of basal
roots, it does not evidence changes in the morphology of
basal tomato roots. While the previous studies found that
Pbz increases the root tip diameter of other species, e.g., in
Prunus sp. and Dendranthema sp. (Williamson etal. 1986;
Burrows etal. 1992), the diameter and tissue density of
tomato basal root orders 1–3 remained largely unaffected
by Pbz in this study (Fig.4; Tables6, 7). The mean diameter
of basal root order 1 (0.33–0.41mm) reported by our study
is about half of the values reported previously for lateral
and basal root tips of ten other tomato cultivars (Bui etal.
2015), possibly also because of the used substrate. Most
drastic changes in basal root morphology thus occurred
under deficit irrigation (see above), while Pbz did not cause
changes in the basal root branching frequency, neither based
on biomass nor on surface area (Fig.3; Tables5, 7). To
our surprise, cross effects between Pbz and irrigation levels
did largely not occur for the analysed traits. In summary,
our study can show that Pbz causes a significant increase in
tomato basal roots’ biomass and surface area relative to the
tap root and its laterals. This is hypothesized to be especially
advantageous under deficit drip irrigation, as increasingly
practiced to cope with limited water resources, where the
wetted soil horizons are close to the surface and thus can
be optimally exploited by basal roots. Thus, the hormonal
changes induced by Pbz seem to at least partially ‘override’
an ‘natural’ adaptation of the tomato cultivar Ikrams’ root
system to drought—an increased investment into tap roots
and deeper-placed laterals. Deeper lateral root placement
is a beneficial acclimation to non-irrigated systems but of
limited benefit under precision and deficit irrigation regimes,
where top soil horizons are wetted—reducing water loss by
deep percolation.
Acknowledgements and Funding information We thank Syngenta
Crop Protection AG for the financial support and for initiating the pro-
ject. We thank Oren Shelef, Daren Burns, Liron Summerfield, and
Noa Nevo for their essential contributions in the greenhouse and lab.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict
of interest.
References
Araujo F, Williams LE, Grimes DW, Matthews MA (1995) A compara-
tive study of young ‘Thompson Seedless’ grapevines under drip
and furrow irrigation. I. Root and soil water distributions. Sci
Hortic 60:235–249. doi:10.1016/0304-4238(94)00710-W
Baninasab B (2009) Amelioration of chilling stress by Paclobutrazol
in watermelon seedlings. Sci Hortic 121:144–148. doi:10.1016/j.
scienta.2009.01.028
Bellini C, Pacurar DI, Perrone I (2014) Adventitious roots and lateral
roots: similarities and differences. Annu Rev Plant Biol 65:639–
666. doi:10.1146/annurev-arplant-050213-035645
Ben-Gal A, Shani U (2002) A highly conductive drainage extension
to control the lower boundary condition of lysimeters. Plant Soil
239:9–17. doi:10.1023/A:1014942024573
Berova M, Zlatev Z (2000) Physiological response and yield of
paclobutrazol treated tomato plants (Lycopersicon escu-
lentum Mill.). Plant Growth Regul 30:117–123. doi:10.102
3/A:1006300326975
Buchenauer H, Kutzner B, Koths T (1984) Effect of various triazole
fungicides on growth of cereal seedlings and tomato plants as
well as on gibberellin contents and lipid metabolism in barley
seedlings. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz
91:506–524
Bui H-H, Serra V, Pages L (2015) Root system development and archi-
tecture in various genotypes of the Solanaceae family. Botany
93:465–474. doi:10.1139/cjb-2015-0008
Burrows G, Boag T, Stewart W (1992) Changes in leaf, stem, and
root anatomy of Chrysanthemum cv. Lillian Hoek following
paclobutrazol application. J Plant Growth Regul 11:189–194
Author's personal copy

Irrig Sci
1 3
Butcher DN, Clark JA, Lenton JR (1990) Gibberellins and the growth
of excised tomato roots: comparison of gib-1 mutant and wild type
and responses to applied GA3 and 2S, 3S Paclobutrazol. J Exp Bot
41:715–722. doi:10.1093/jxb/41.6.715
Chapin FS, Autumn K, Pugnaire F (1993) Evolution of suites of traits
in response to environmental-stress. Am Nat 142:S78–S92
Comas L, Becker S, Cruz VMV, Byrne PF, Dierig DA (2013) Root
traits contributing to plant productivity under drought. Front Plant
Sci 4:442. doi:10.3389/fpls.2013.00442
Couée I, Serra A-A, Ramel F, Gouesbet G, Sulmon C (2013)
Physiology and toxicology of hormone-disrupting chemicals
in higher plants. Plant Cell Rep 32:933–941. doi:10.1007/
s00299-013-1428-z
Davis TD, Sankhla N, Walser RH, Upadhyaya A (1985) Promotion of
adventitious root formation on cuttings by paclobutrazol. HortSci-
ence 20:883–884
de Dorlodot S, Forster B, Pages L, Price A, Tuberosa R, Draye X
(2007) Root system architecture: opportunities and constraints
for genetic improvement of crops. Trends Plant Sci 12:474–481.
doi:10.1016/j.tplants.2007.08.012
El-Nesr MN, Alazba AA, Šimůnek J (2014) HYDRUS simulations
of the effects of dual-drip subsurface irrigation and a physical
barrier on water movement and solute transport in soils. Irrig Sci
32:111–125. doi:10.1007/s00271-013-0417-x
FAOSTAT (2014) Area harvested and yield—tomatoes 2012. Food and
Agricultural Organization of the United Nations, Rome
Fletcher RA, Gilley A, Sankhla N, Davis TD (1999) Triazoles as
plant growth regulators and stress protectants. In: Janick J
(ed) Horticultural Reviews, vol 24. Wiley, Oxford, pp 55–138.
doi:10.1002/9780470650776.ch3
Fresco LO (2013) The GMO stalemate in Europe. Science 339:883.
doi:10.1126/science.1236010
Grossmann K (1990) Plant growth retardants as tools in
physiological research. Physiol Plant 78:640–648.
doi:10.1034/j.1399-3054.1990.780422.x
Grossmann K (1992) Plant growth retardants: Their mode of action
and benefit for physiological research. In: Karssen CM, van
Loon LC, Vreugdenhil D (eds) Progress in plant growth regu-
lation, vol 13. Current Plant Science and Biotechnology in
Agriculture. Springer Dordrecht, Netherlands, pp 788–797.
doi:10.1007/978-94-011-2458-4_97
Harrak H, Azelmat S, Baker EN, Tabaeizadeh Z (2001) Isolation
and characterization of a gene encoding a drought-induced
cysteine protease in tomato (Lycopersicon esculentum). Genome
44:368–374
Jung J, Luib M, Sauter H, Zeeh B, Rademacher W (1987) Growth
regulation in crop plants with new types of triazole compounds.
J Agron Crop Sci 158:324–332. doi:10.1111/j.1439-037X.1987.
tb00280.x
Khan MA, Khokhar KM (1989) Effect of paclobutrazol on growth and
yield of tomato. Pak J Agric Res 10:49–52
Kulkarni M, Deshpande U (2007) InVitro screening of tomato geno-
types for drought resistance using polyethylene glycol. Afr J Bio-
tech 6:691–696
Latimer JG (1992) Drought, paclobutrazol, abscisic acid, and gibberel-
lic acid as alternatives to daminozide in tomato transplant produc-
tion. J Am Soc Hortic Sci 117:243–247
Lawlor DW (2013) Genetic engineering to improve plant performance
under drought: physiological evaluation of achievements, limita-
tions, and possibilities. J Exp Bot 64:83–108. doi:10.1093/jxb/
ers326
Loyola J, Verdugo I, González E, Casaretto J, Ruiz-Lara S (2012) Plas-
tidic isoprenoid biosynthesis in tomato: physiological and molecu-
lar analysis in genotypes resistant and sensitive to drought stress.
Plant Biol 14:149–156
Lynch JP (2013) Steep, cheap and deep: an ideotype to optimize water
and N acquisition by maize root systems. Ann Bot 112:347–357.
doi:10.1093/aob/mcs293
Maeght J-L, Rewald B, Pierret A (2013) How to study deep
roots—and why it matters. Front Plant Sci 4:299. doi:10.3389/
fpls.2013.00299
Magnitskiy SV, Pasian CC, Bennett MA, Metzger JD (2006) Effects of
soaking cucumber and tomato seeds in Paclobutrazol solutions on
fruit weight, fruit size, and Paclobutrazol level in fruits. HortSci-
ence 41:1446–1448
Marshall J, Rutledge R, Blumwald E, Dumbroff E (2000) Reduction in
turgid water volume in jack pine, white spruce and black spruce in
response to drought and paclobutrazol. Tree Physiol 20:701–707.
doi:10.1093/treephys/20.10.701
McCormack ML etal (2015) Redefining fine roots improves under-
standing of belowground contributions to terrestrial biosphere
processes. New Phytol 207:505–518. doi:10.1111/nph.13363
Miguel MA, Widrig A, Vieira RF, Brown KM, Lynch JP (2013)
Basal root whorl number: a modulator of phosphorus acquisition
in common bean (Phaseolus vulgaris). Ann Bot 112:973–982.
doi:10.1093/aob/mct164
Miguel MA, Postma JA, Lynch JP (2015) Phene synergism between
root hair length and basal root growth angle for phosphorus acqui-
sition. Plant Physiol 167:1430–1439. doi:10.1104/pp.15.00145
Mingo DM, Theobald JC, Bacon MA, Davies WJ, Dodd IC (2004)
Biomass allocation in tomato (Lycopersicon esculentum) plants
grown under partial rootzone drying: enhancement of root growth.
Funct Plant Biol 31:971–978
Mittler R, Blumwald E (2010) Genetic engineering for modern agricul-
ture: challenges and perspectives. Annu Rev Plant Biol 61:443–
462. doi:10.1146/annurev-arplant-042809-112116
Navarro A, Sánchez-Blanco MJ, Bañon S (2007) Influence of
paclobutrazol on water consumption and plant performance of
Arbutus unedo seedlings. Sci Hortic 111:133–139. doi:10.1016/j.
scienta.2006.10.014
Nishizawa T (1993) The effect of paclobutrazol on growth and yield
during first year greenhouse strawberry production. Sci Hortic
54:267–274. doi:10.1016/0304-4238(93)90105-Y
Osmont KS, Sibout R, Hardtke CS (2007) Hidden branches: develop-
ments in root system architecture. Annu Rev Plant Biol 58:93–
113. doi:10.1146/annurev.arplant.58.032806.104006
Ozbahce A, Tari AF (2010) Effects of different emitter space and
water stress on yield and quality of processing tomato under
semi-arid climate conditions. Agric Water Manag 97:1405–1410.
doi:10.1016/j.agwat.2010.04.008
Panneerselvam R, Muthukumarasamy M, Karikalan L (1998) Tri-
adimefon enhances growth and net photosynthetic rate in NaCl
stressed plants of Raphanus sativus L. Photosynthetica 34:605–
609. doi:10.1023/A:1006846403658
Passioura JB (2012) Phenotyping for drought tolerance in grain crops:
when is it useful to breeders? Funct Plant Biol 39:851–859.
doi:10.1071/FP12079
Patanè C, Cosentino S (2010) Effects of soil water deficit on yield and
quality of processing tomato under a Mediterranean climate. Agric
Water Manag 97:131–138. doi:10.1016/j.agwat.2009.08.021
Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress
tolerance in crop plants. Curr Opin Plant Biol 14:290–295.
doi:10.1016/j.pbi.2011.02.001
Postma JA, Dathe A, Lynch J (2014) The optimal lateral root branch-
ing density for maize depends on nitrogen and phosphorus avail-
ability. Plant Physiol 166:590–602. doi:10.1104/pp.113.233916
Rademacher W (2000) Growth retardants: effects on gibberellin bio-
synthesis and other metabolic pathways. Annu Rev Plant Physiol
Plant Mol Biol 51:501–531. doi:10.1146/annurev.arplant.51.1.501
Rajasekar M, Manivannan P (2015) Drought and drought with tria-
zoles induced changes on pigment composition and biochemical
Author's personal copy

Irrig Sci
1 3
constituents of Zea mays L. (Maize) Appl Transl Genom
doi:10.1016/j.atg.2015.04.001 (Withdrawn article in press)
Rewald B, Ephrath JE, Rachmilevitch S (2011) A root is a root is a
root?—water uptake rates of Citrus root orders. Plant Cell Environ
34:33–42. doi:10.1111/j.1365-3040.2010.02223.x
Rewald B, Rechenmacher A, Godbold DL (2014) It’s complicated:
intra-root system variability of respiration and morphological
traits in four deciduous tree species. Plant Physiol 166:736–745.
doi:10.1104/pp.114.240267
Romero-Romero T, Sanchez-Nieto S, SanJuan-Badillo A, Anaya
A, Cruz-Ortega R (2005) Comparative effects of allelochemi-
cal and water stress in roots of Lycopersicon esculentum
Mill. (Solanaceae). Plant Sci 168:1059–1066. doi:10.1016/j.
plantsci.2004.12.002
Saito S etal (2006) A plant growth retardant, uniconazole, is a potent
inhibitor of ABA catabolism in Arabidopsis. Biosci Biotechnol
Biochem 70:1731–1739. doi:10.1271/bbb.60077
Schenk HJ, Jackson RB (2002) Rooting depths, lateral root
spreads and below-ground/above-ground allometries of
plants in water-limited ecosystems. J Ecol 90:480–494.
doi:10.1046/j.1365-2745.2002.00682.x
Silva KS (2008) Uso de paclobutrazol em tomateiro cultivado em
dois ambientes. Universidade Estadual Paulista, São Paulo (In
Portuguese)
Somasundaram R, Jaleel CA, Azooz MM, Abraham SS, Gomathinay-
agam M, Panneerselvam R (2009) Induction of drought stress
tolerance by paclobutrazol and abscisic acid in gingelly (Sesamum
indicum L.). Global J Mol Sci 4:49–55
Still JR, Pill WG (2004) Growth and stress tolerance of tomato seed-
lings (Lycopersicon esculentum Mill.) in response to seed treat-
ment with paclobutrazol. J Hortic Sci Biotechnol 79:197–203
Syngenta (2015) Catalogo 2015—Sementi, Agrofarmaci e Insetti ausi-
liari. Syngenta Italia S.p.A, Milano
Tanis SR, McCullough DG, Cregg BM (2015) Effects of paclobutrazol
and fertilizer on the physiology, growth and biomass allocation
of three Fraxinus species. Urban For Urban Green 14:590–598
Union European (2011) Common catalogue of varieties of vegetable
species, 30th edn. European Comission, Brussel
Upadhyaya A, Davis TD, Sankhla N (1986) Some biochemical changes
associated with paclobutrazol-induced adventitious root formation
on bean hypocotyl cuttings. Ann Bot 57:309–315
Vanstraelen M, Benková E (2012) Hormonal interactions in the regula-
tion of plant development. Annu Rev Cell Dev Biol 28:463–487.
doi:10.1146/annurev-cellbio-101011-155741
Wang Y, Frei M (2011) Stressed food—the impact of abiotic envi-
ronmental stresses on crop quality. Agric Ecosyst Environ
141:271–286
Wasson A etal (2012) Traits and selection strategies to improve root
systems and water uptake in water-limited wheat crops. J Exp Bot
63:3485–3498. doi:10.1093/jxb/ers111
Wiesman Z, Riov J (1994) Interaction of paclobutrazol and indole-3-bu-
tyric acid in relation to rooting of mung bean (Vigna radiata) cut-
tings. Physiol Plant 92:608–612. doi:10.1111/j.1399-3054.1994.
tb03030.x
Williamson J, Coston D, Grimes L (1986) Growth responses of peach
roots and shoots to soil and foliarapplied paclobutrazol. Hortsci-
ence 21:1001–1003
York LM, Nord E, Lynch J (2013) Integration of root phenes for
soil resource acquisition. Front Plant Sci 4:355. doi:10.3389/
fpls.2013.00355
Zarebanadkouki M, Kröner E, Kaestner A, Carminati A (2014) Visu-
alization of root water uptake: quantification of deuterated water
transport in roots using neutron radiography and numerical mod-
eling. Plant Physiol 166:487–499. doi:10.1104/pp.114.243212
Zobel RW, Waisel Y (2010) A plant root system architectural taxon-
omy: a framework for root nomenclature. Plant Biosyst 144:507–
512. doi:10.1080/11263501003764483
Author's personal copy