Journal of Experimental Botany, Vol. 47, No. 303, pp. 1499-1507, October 1996
Journal of
Experimental
Botany
A comparative study of the response of the roots and
shoots of sunflower and maize to mechanical stimulation
A.M. Goodman1 and A.R. Ennos
School of Biological Sciences, Stopford Building, University of Manchester, Oxford Road,
Manchester M13 9PT, UK
Received 12 December 1995; Accepted 15 May 1996
Abstract
Introduction
Despite numerous studies of the effects of mechanical
stimulation on plant shoots, the response of roots to
mechanical stimulation has largely been neglected. In
this study the effects of shoot flexure on the morphology and mechanics of two contrasting species of herbaceous angiosperm, growing in a glasshouse were
compared: maize {£ea mays), a monocot; and sunflower (Helianthus annuus L.) a dicot.
Mechanical stimulation affected the root more than
the shoot components. Root systems of mechanicallystressed sunflowers had a greater angle of spread and
increased root number. As well as large morphological
and weight effects, with increases over the control of
33% in the length of rigid root and 38% in the dry
weight of lateral roots, in sunflowers, there were also
mechanical effects. In both species roots of flexed
plants were more rigid, stronger and composed of
stiffer material and their root systems also provided
greater anchorage strength. In contrast, there was
only a small reduction in shoot weight and shoot height
in flexed plants and no effects on mechanical
properties.
There were differences in behaviour between
species; maize root morphology responded less than
that of sunflowers to mechanical stimulation. The
basal diameter of roots increased by only 8% compared with 16% in sunflowers, though the roots of
both species showed similar increases in material stiffness. This difference is related to the lack of secondary thickening in the monocots compared with the
dicot sunflowers.
It is well known that plants respond to mechanical
stimulation (Whitehead and Luti, 1962; Jaffe, 1973;
Biddington and Dearman, 1985; Gartner, 1994).
However, until recently (Gartner, 1994; Stokes et al,
1995), root effects have largely been ignored, despite the
vital role of root systems in anchoring plants and preventing them from falling over. Growth is affected by as
little as 30 s of stimulation per day (Neel and Harris,
1971) and plants will respond to the rubbing, bending
(Jaffe, 1973, 1976) and shaking (Neel and Harris, 1971)
of stems.
In the field, plants are subjected daily to mechanical
forces by the wind often resulting in a reduction of shoot
height. Whitehead and Luti (1962) showed that seedlings
of Zea mays exposed to wind produced thicker and
shorter shoots than sheltered seedlings. Glasshouse studies
have shown a thickening of the stem base when stems of
cherry tomatoes (Lycopersicon esculentum Mill.) were
flexed (Gartner, 1994) and changes in root distribution
(Stokes et al, 1995) when seedling larch trees (Larix
decidua) were blown in a wind tunnel; however, changes
in the mechanical properties of roots due to mechanical
stimulation have only been quantified in one study (Crook
and Ennos, 1996) when winter wheat growing in the field
was either left to grow normally or supported by metal
grids. Plants grown in this way had stems around 20%
weaker and root systems 50% weaker than plants left to
sway freely in the wind.
Whilst previous studies on root systems have focused
on a broad selection of individual species: the dicot
tomato (Gartner, 1994), a monocot winter wheat (Crook
and Ennos, 1996) and the conifers larch and Sitka spruce
(Picea sitchensis) (Stokes et al, 1995), none have investigated the effects of mechanical stimulation on the root
systems of two contrasting species.
Key words: Thigmomorphogenesis, Helianthus annuus L,
Zea mays, anchorage, lodging.
1
To whom correspondence should be addressed. Fax: +44 161 275 3938. E-mail: agoodman©man.ac.uk
O Oxford University Press 1996
1500
Goodman and Ennos
This study compared the response of two species to
mechanical stimulation in the form of stem flexing. The
dicot sunflower, which has extensive secondary thickening, and the monocot maize, in which no secondary
thickening takes place. The mechanics of anchorage of
both species have previously been investigated, providing
a solid basis for comparison (Ennos et al., 1993a, b).
Sunflower and maize also provide a convenient model for
trees and cereals both of which are affected by anchorage
failure on a commercial scale, through windthrow and
lodging (Pinthus, 1973).
Materials and methods
Four hundred seeds of Helianlhus annuus L. (variety 'Vincent')
were germinated in moist vermiculite in early March 1995 and
70 plants were transplanted after 3 d into 7.5 1 pots, containing
John Innes No. 1 compost prepared from sterilized loam, peat
and gravel. Early transfer ensured that the tap root would be
unrestricted and undergo normal growth (Ennos et al, 19936).
The same number of Zea mays (variety 'Lg 20-80') seeds were
germinated in moist Fisons F2 compost and 70 were again
transplanted after 6 d into 5 1 pots containing John Innes No. 1
compost. Sunflowers and maize seedlings were selected for
uniformity of length and straightness, with a root length of
about 1.5 cm in sunflowers and a coleoptile length of 4 cm for
maize. All pots were shaken twice to ensure similar soil bulk
densities and placed on saucers in a glasshouse at the University
of Manchester's experimental grounds.
Four days later dying plants were discarded and 64 plants of
each species were placed in two randomized block designs in
16 plots of four plants per plot. Saucers were filled daily with
water and a 16 h photoperiod was maintained with sodium
lights supplementing natural daylight as required. The temperature varied between 15-30 °C and air currents were maintained
well below the threshold that could induce motion by draping
netting over the glasshouse vent.
Half of the plots of sunflowers and maize were randomly
assigned to treatment and underwent stem flexing (eight plots)
and half were left still as controls. Sunflower and maize shoots
were flexed daily from 4 and 5 d after planting, respectively,
when they had two true leaves and were 5 cm high. Shoots were
flexed by hand to reduce damage to the plants. The flexing
technique was adapted from Patterson (1992), flexing each
plant for 1 min d" 1 at its natural resonance frequency and
moving the top of the shoot laterally by no more than 10% of
the plant height. Each day after flexing, all the plants were
rotated clockwise by 45° ensuring stimulation from all directions.
Half of the sunflower and maize plants (eight plots) were
randomly harvested at 8 and 12 weeks after planting and sent
to the laboratory for analysis, the remaining 16 plants underwent
anchorage tests approximately 1 week later.
Growth measurements
Measurements of basal diameter (mm) and shoot height (cm)
of plants were made on a weekly basis after planting. Shoot
height was taken as the distance from the soil surface to the
point where the last petioles or leaf left the stem.
Measurements at harvest
Stem morphology: The height and degree of taper of each shoot
was measured by taking diameter measurements at the soil
level, at heights of 50 cm and 100 cm, and at the top of the
stem just under the flower of each plant. Shoots were then cut
off at the base, just above the topmost adventitious roots for
microscopy and a length of roughly 22 cm was removed for
mechanical testing. Fresh weights of the shoot systems of each
plant were measured, and the stem, leaves and reproductive
parts being weighed separately in the maize and the vegetative
shoot and reproductive parts weighed separately in the
sunflower.
Root morphology: Root systems were stored in situ over the
duration of harvest in a cold room at 5 °C. Each was then
carefully washed and all the fine roots collected using a sieve.
The angle of spread of each root system was measured in two
planes to the nearest 5° by placing the system on a paper
protractor and reading off the maximum angle; the roots were
then rotated by 90° and the maximum angle again measured;
finally the mean value was calculated. For maize, the number
of roots was counted at each node and classified either as those
which entered the soil and those which did not. The number of
nodes was also noted along with the length of stem from which
roots arise. The main lateral roots of both species were then
sawn off at the base and transverse basal sections were then cut
and stained with phloroglucinol to investigate the extent of
lignification. Only sunflower sections were image analysed, the
central lignified stele contrasting well with the unstained cortex
region. To calculate the relative area of lignified material in the
root section a Delta-T image analysis system II was used
(Delta-T Devices).
Roots from a single plant were placed in rough diameter
order on moist sponges to prevent desiccation from altering
their mechanical properties. Three roots from each plant were
randomly sampled from the sponges for measurement of the
degree of root taper at the base, the base plus 4 cm and the
base plus 8 cm. The total number of primary lateral roots was
counted for both species.
The dimensions of the tap root of sunflowers was investigated
by measuring their length, together with their diameter at 2 cm
intervals from the base to 10 cm down the root. The length of
root lateral which showed noticeable rigidity in bending was
also measured in the sunflowers.
Wet and dry masses of roots: Root systems were divided into
different components—the rigid lateral roots which have
primary anchorage role; the fine roots which have a role in
absorption and which were stripped of the main laterals; and
the central anchorage element: the tap root in the case of
sunflowers and basal internode in the case of maize. Samples
were weighed before and after being oven-dried at 70 °C for 5 d.
Mechanical tests
Three point bending tests were carried out both on the stems
and on the largest ten lateral roots of both sunflowers and
maize using a universal testing machine (Instron, model 4301).
Root and stem sections were placed between two supports
which were set apart at a distance of roughly 15 times the midpoint diameter of the section to avoid problems with shear
(Vincent, 1992). A pushing probe of radius 2 mm (20 mm for
shoots) was attached to the load cell and lowered till it just
touched the sample. The crosshead was then lowered at a rate
of 10ram min"1 (20mm min"1 shoots) bending the sample
until it eventually buckled, while an interfaced computer
produced a graph of force versus displacement and calculated
the mechanical properties of the sample (Ennos et al., 1993a).
For stems the diameter at the mid-point was measured using
Roofs and mechanical stimulation
calipers. In the case of maize, in which the stems were elliptical,
the diameter was taken in the plane in which the probe would
impact, when the section was freely resting on the supports.
For roots, the basal 60 mm was removed, stripped of fine
roots with a razor and the diameter measured at the mid-point.
In the analysis used by the Instron it was assumed that there
was little taper; though this is not true the errors are small and
it is felt that this is an acceptable approximation (Ennos
et al., 1993a).
Three mechanical properties, the bending strength, S, and
the rigidity, El, of each section, and the Young's Modulus, E,
of the material of which they were composed, were all
calculated. The bending strength is given by the expression:
1501
measuring its horizontal movement along a ruler placed 0.6 m
above the soil. Readings of force were measured at lateral
intervals of 2, 4, 6, 8, 10, 12, 16, 20, 24, 28, 32, 36, 40, 44, 48,
52, 56, and 60 cm. The approximate rate of rotation was 1.5°
s"1. The mechanism of failure was noted along with any cracking
noises and a curve of restoring moment (force times perpendicular
height) versus angular displacement was produced.
Statistical analysis
where dF/dY is the initial slope of the force displacement curve.
The Young's modulus, E, is given by:
E=R/I=4R/irr4
(3)
Two-way analysis of variance was used whenever possible,
though in cases of unequal sample size one-way analysis of
variance was used. Chi-squared tests were used to analyse the
data on the growth stage and in the anchorage tests where the
difference in the mode of failure of the sunflowers was analysed.
Root-to-shoot ratios and root anatomy ratios were arcsine
square root transformed before testing, since many of the ratios
lay outwith the range 0.3-0.7 (Snedecor and Cochran, 1980).
The sunflower and maize anchorage tests were analysed in
two parts; first, the linear phase of the curves (from 0-7.6°) of
the untreated andflexedplants were compared, followed by the
whole curves. The whole curves were log10 transformed before
analysis. The data for both the sunflower and maize plants was
linearly regressed and then analysis of covariance was performed
to provide a comparison of anchorage stiffness and strength
between the untreated andflexedplants.
where r is the radius and nr4/4 is the second moment of area
(/) for a solid cylinder. A high modulus indicates a stiffer
material.
Results
S^F^L/4
(1)
where /"„,„ is the maximum force the sample will withstand
before it fails (Gordon, 1978) and L is the distance between the
supports. The bending rigidity, R, of a uniform beam is the
resistance of that beam to curvature and is given by:
R = L3(dF/dY)/4&
(2)
Anchorage tests
The procedure used to study the anchorage of sunflowers and
maize was adapted from Ennos et al. (19936). The soil was
brought to field capacity by watering it to saturation and
allowing to drain for 1-2 h. The sunflowers and maize were then
pruned to leave the bottom 0.8 m (0.6 m maize) of the stem
leafless. The stems were pulled perpendicular to the orientation
of the stem at a height of 0.6 m (0.4 m maize) with a Euristem
digital force balance (Fig. 1). The inclination of the stem base
was measured by attaching a cane of length 0.8 m to it and
Ruler
Shoot effects
Flexure had a moderate effect on the height growth of
the shoots (Fig. 2a, b). In the sunflower an initial reduction in plant shoot height diminished at the onset of
reproductive growth before returning once the flower
head had matured (Fig. 2a). At harvest, flexure had
resulted in a reduction of stem height for sunflowers of
7% and maize of 9%, both significant at the 1% level
(P<0.01). Flexure of maize plants elicited a greater shoot
response throughout ontogeny (Fig. 2b). The response
was also faster, with a difference in shoot height occurring
after 7 d compared to 18 d for sunflowers. There was no
change in the diameter of the stem base of either species
in response to stemflexure(P>Q.O5) (Table 1). However,
there was a small effect on the pattern of development in
sunflowers; after 8 weeks, 14 out of the 16 untreated
sunflower heads were fully flowering compared to 7 out
of the 16 flexed plants (/><0.05; X2=4.9&).
There was no significant effect of flexure on the total
fresh weight of the shoot system of either species, though
a decrease was found in total dry mass of the maize
shoots (Table 2; P<0.05). The major change was in the
partitioning of mass within maize; not surprisingly the
shorter stem and basal node were both lighter (Table 2).
Stem flexure had no significant effect on the mechanical
properties of the stems of either species (Table 1).
ffoof effects: morphology and mass
Fig. 1. The apparatus for anchorage tests. Stems are pulled sideways
with a digital force balance and the inclination of the stem base is
recorded by measuring the lateral movement of an attached cane.
Adapted from Ennos et al. (19936).
The effect of stem flexure on the morphology of the root
system was most noticeable in the sunflowers; flexed tap
roots showed a lower degree of taper (Fig. 3) (P <0.05).
1502
Goodman and Ennos
Sunflower
18
25
32
39
46
52
Days of stem flexure
Maize
There was an increase in the number of laterals and the
angle of spread was higher in the sunflowers (Table 3).
In contrast, in maize there was no effect on either number
of root laterals or the root angle (Table 3).
The overall effect of stem flexure on the root system
biomass was dramatic. Both sunflower and maize showed
an increase in dry weight with flexure (Table 4), though
there were different patterns within each species.
Sunflowers showed significant increases in the dry
weight of the tap root and laterals, but no change in the
mass of the fine roots (Table 4). Maize, in contrast,
showed a big increase in the dry weight of laterals and
fine roots (Table 4). As a result both species showed
significant increases in the root to shoot ratio (Fig. 4).
There was no significant effect of stem flexure on the
ratio of lignin-stained area to total area of the sunflower
root sections (P>0.05), the ratios for untreated and treated
plants being 0.38±0.02 and 0.40±0.01, respectively.
Root effects: mechanics and dimensions
21
28
35
42
49
56
63
70
Days of stem flexure
Fig. 2. Graphs showing how height in sunflowers (a) and maize (b)
varied over time. Sunflowers showed a delayed response to stem flexure,
flexed plants being shorter initially and also later after the onset of
reproductive growth (denoted by R). The flexed plants are denoted by
squares and untreated plants by diamonds. The asterixes indicate the
results of one-way ANOVA where n = 32, */><0.05; ** P-cO.01. Maize
(b), in contrast, showed a rapid response to stem flexure with a
reduction in shoot height after 7 d and little effect offloweringlater on,
all points differed at P<0.01 except at 49 d which was /><0.05. The
error bars shown are standard errors.
Flexure had a significant effect on the dimensions and
mechanical properties of lateral roots of both species
(Table 5); in all cases strength, rigidity and Young's
modulus were significantly increased.
However, there are marked differences between species
in the extent of these differences (Table 6). Sunflowers
showed much larger differences in diameter and consequently rigidity and bending strength, but roots of both
species showed a similar increase in Young's modulus
(Table 6).
Anchorage mechanics
The results for the anchorage tests are shown in Fig. 5a and
b. The moment versus angular displacement curve is similar
for both species, the moment rising linearly at first before
levelling off after about 15° for both sunflower and maize.
Flexed sunflowers reached a greater maximum mean
strength of 7.5 Nm compared to 6.3 Nra for control plants
(Fig. 5a). There was also an increase in the stiffness which
Table 1. The effects of mechanical stimulation on the morphology and mechanical properties of the stems of sunflower and maize
Stem flexure had no effect on the mechanical properties of the stem of either species and only a small effect on the stem diameter. Results were
analysed using two-way ANOVA, SE, «= 16 except for the diameter measurements of the maize where n = 32 There was no significant block effect
= />>0.05, ±SE.
Property
Maize
Sunflower
Untreated
Flexed
P
Untreated
Flexed
P
Stem diameter (mm)
Base
Base + 50 cm
Base+100 cm
Top
Mechanical properties
Rigidity (Nm2)
Bending strength (Nm)
Modulus (MPa)
17.6±0.19
17.9±0.33
12.0±0.27
5.0±0.l0
NS
NS
NS
17.8 ±0.17
18.0±0.32
13.0±0.33
5.0±0.07
NS
NS
NS
5.68 ±0.22
6.78 ±0.33
1946±95.1
5.23 ±0.22
6.63 ±0.22
1732 ±90.6
NS
NS
NS
17.3±0.27
19.1 ±0.31
14.5±0.31
6.9 ±0.23
17.9 ±0.26
18.5±0.33
13.5±0.25
7.0±0.17
NS
NS
6.47 ±0.28
6.27 ±0.25
1170 ±55.7
6.36±0.32
6.26±0.34
1289 ±99.9
+
•
NS
Roofs and mechanical stimulation
1503
Table 2. The effect of stem flexure on the mean fresh and drv weights of different parts of the shoot systems of sunflower and maize
Mechanical stimulation had little effect on the shoot systems of either species Results were analysed using two-way ANOVA. There was no
significant block effect {P>0 05). */><0.05, **P<0.0\, NS = />>0.05, ±SEn=16.
Sunflower
Fresh weight (g)
Stem
Leaves
Reproductive
Basal node
Total
Dry weight (g)
Stem
Leaves
Reproductive
Basal node
Total
Maize
Untreated
Flexed
P
366±116
343 ±9.40
NS
24.2 ±1.30
22.8±0.99
NS
391 ± 11.7
366 ±9.7
NS
46.5 ±1.05
44.0 ±0.82
NS
3.4 + 0 21
3.2±0.15
NS
49.9 + 1.12
47.2 ±0.92
NS
4
6
Untreated
Flexed
P
171 ±7.01
98.0 ±4.4
32.9±6.58
5.5±0.22
307 ±9.4
153±4.93
104±3.14
25.8 + 5.21
4.9±0.18
287 ±9.8
NS
NS
42.5±2.13
27.0 ±1.04
5.1 ±0.81
1.6 ±0.05
76 1 ±2.2
35.6 ±1.46
27.8 + 0.51
4.1 ±0.62
1.5±O.O5
69.0 ±1.9
NS
•
NS
•
NS
NS
NS
*
10
Distance from base (cm)
Fig. 3. Graph comparing the diameters of the tap roots offlexed(hatched bar) and untreated (white bar) sunflowers. The mean diameter was taken
at 2 cm intervals from the base of the stem and the results were analysed using two-way ANOVA where n= 16. There were significant differences
(P < 0.01) at 4 cm and 6 cm from the base, the tap roots offlexedplants being thicker than the untreated roots. The error bars shown are standard errors.
increased from 0.47 + 0.03 Nm per degree in the control to
0.58±0.02 Nm per degree (P<0.0l) in the flexed plants.
Flexure also affected the mode of failure in sunflowers;
failure occurred in the stem in all 16 flexed plants whereas
in the control plants root failure instead occurred in 15 out
of 16 plants (P<0.01; ^ = 24.6). Only 25% of stem fractures
were classified as buckling; the rest were clean breaks.
The maize, in contrast, showed no significant difference
between flexed plants and controls for either the stiffness
or the total anchorage strength of the system (Fig. 5b).
In all but one case anchorage failure in the maize occurred
in the roots, distinct cracking noises being heard in most
plants as they failed.
Discussion
The results of this experiment were surprising because
there was little effect of mechanical stimulation on the
1504
Goodman and Ennos
Table 3. The effects of mechanical stimulation on root morphology
in sunflower and maize
Stem flexure increased the angle of spread of the root system, length of
rigid root (sum 15 roots per plant) and lateral number in the sunflowers,
but not the maize. The results were analysed using two-way ANOVA
(sunflower root angle, one-way). There was no significant block effect
(P>0.05). */><0.05, *'/ > <0.01, NS = / ) >0.05, ±SE n= 16.
Sunflower
Mean root angle (degrees)
Mean root lateral number
Length of rigid root (cm)
Maize
Mean root angle (degrees)
Mean root lateral number
Untreated
Flexed
P
133 ± 1.6
50.4±2.3
68.0±2.0
144±1.7
58 8± 1.9
90.5±20
•
*•
149±5.1
28.6±0.6
148±3.9
28.1 ±0.7
NS
NS
shoot properties in either species; flexing only resulted in
a reduction in the stem height and mass (Fig. 2a, b;
Table 2).
In marked contrast, response of the roots was far more
dramatic; there were increases in mass and differences in
the morphology of both species (Tables 3, 4). However,
there was a difference in the pattern of the response
between species. In maize, though there were more fine
roots there was less effect on size of the main laterals
(Tables 4, 5), whereas sunflowers showed an increase in
both the size of taproot (Fig. 3), just as Gartner (1994)
found in tomatoes, and an increase in the diameter of the
laterals (Table 5). As a consequence there was rather a
different effect on the mechanics of roots and on anchorage. The sunflower roots increased in rigidity and strength
by about 100%; while in maize they only increased by
about 50% (Table 6). The anchorage strength in sunflower
also increased by about 20%; whereas that of maize
stayed the same (Fig. 5a, b). The lack of an increase in
anchorage strength in maize, despite the overall increase
in root strength may well have been due to the disruption
of the soil during shaking (Fig. 5b).
The difference in response is probably due to differences
in the pattern of growth between the species; sunflowers,
being dicots, undergo secondary growth so the roots of
flexed plants grew thicker. In contrast, the maize, like
wheat, being a monocot, has no secondary growth in its
roots. It is therefore no surprise that the differences in
mechanical properties of the roots were largely due to
changes in material properties to produce thicker, stiffer
cell walls. Flexed maize also diverted more primary
growth into secondary roots.
The results of this study have implications for both
Table 4. The effects of mechanical stimulation on the mean fresh and dry weights of sunflower and maize roots
In both species stem flexure increased the dry weight of the lateral roots. Results were analysed using two-way ANOVA. There was no significant
block effect (/>>0.05). *P<0.05, ••/ ) <0.01, NS = />>0.05, ±SE/i=16.
Sunflower
Fresh weight (g)
Tap root
Laterals
Fine roots
Total
Dry weight (g)
Tap root
Laterals
Fine roots
Total
Maize
Untreated
Flexed
P
Untreated
Flexed
P
13.0 ±0.49
22.8±1.I6
89.1 ±4.94
125 ±5.2
16.3 ±0.74
29.9 ±1.58
93.1 ±6.72
139±7.7
NS
NS
19.4±0.68
107 ±4.36
127±4.43
20.4 ±0.87
113±4.33
133±4.51
NS
NS
NS
2.77±0.09
2.10±0.11
6.28 + 0.29
11.2±0.33
3.40±0.17
2.88±0.13
7.05 ±0.75
13.3 ±0.86
3.6±0.14
11.9±0.85
15.5±0.83
4.1 ±0.18
14.8±1.03
18.9± 1.06
*
*
*•
NS
*
Table 5. The effects of mechanical stimulation on the mean diameter and mechanical properties of the roots of sunflower and maize
In both species mechanical stimulation increased the diameter and the mechanical properties of the roots. The diameters were analysed using twoway ANOVA and the mechanical properties using a one-way ANOVA (rune sunflower and seven maize roots per plant were summed), moduli are
means. */><0.05, **/><0.01, NS = />>0.05 ±SEn=16.
Property
Sunflower
Untreated
Maize
Flexed
3
1
Untreated
Flexed
Lateral diameter (mm)
Base
Base + 4cm
Base+ 8 cm
Mechanical properties
Rigidity (Nm2 EXP-3)
Bending strength (Nm)
Modulus (MPa)
P
3.87±0.16
2.43 ±0.10
1.83±0.12
4.48 ±0.20
3.07±0.12
2.18±0.12
'"
''*
<'
4.90±0.12
3.16±0.O9
2.18±0.07
5.29 ±0.15
3.44±0.11
2.43 ±0.09
*
*
*
6.86±1.14
0.137 ±0.02
184±18.0
15.0±1.46
0.251 ±0.01
239±11.6
''•
<>•
''
195±9.76
1.53 ±0.05
2790±170
268 ±14.5
1.96 ±0.08
3680± 181
**
**
anrl mwhaniral cf/m/
Fresh weight
Dry weight
Fresh weight
Sunflower
"| 505
Dry weight
Maize
Fig. 4. Graph showing the effects of mechanical stimulation on the root-to-shoot ratios of sunflowers and maize plants. In the sunflower both the
fresh weight (P<0.05) and dry weight (P<0.01) ratios were increased by mechanical stimulation. In maize, however, mechanical stimulation only
increased the dry weight root-to-shoot ratio (P<0.01) Flexed plants are shown as hatched bars and untreated as white bars. The ratios were
arcsine square root transformed before using two-way ANOVA where n = 16. There was no significant block effect (/ ) >0.05) and the error bars
shown are standard errors.
Table 6. Table showing the relative percentage increases of the diameter and the mechanical properties of lateral roots in flexed
compared to untreated plants of sunflower and maize
Sunflower roots have a much greater increase in rigidity and strength, mostly due to their greater increase in diameter. Both species had similar
increases in the stiffness of roots.
Property
Lateral diameter
Base
Base + 4cm
Base+ 8 cm
Mechanical properties
Rigidity
Bending strength
Young's modulus
Sunflower
(% increase)
16
26
19
119
83
30
plant physiology and ecology. First, it shows that surprisingly, mechanical stimulation seems to have greater effects
on root growth than on shoot growth, in which until
recently it has been mainly studied (Jaffe, 1973; Jaffe
et al., 1984; Patterson, 1992). Flexed plants, therefore,
exhibit an increase in their root-to-shoot ratio, a property
which has until now only been shown to vary with
ecological factors, such as the supply of water and nutrients (Chapin, 1980; Gutschick and Kay, 1995; Pefiuelas
et al., 1995). Second, it suggests that roots may be more
suitable than shoots in the study of thigmomorphogenesis.
So why do the roots show a larger response? One
Maize
(% increase)
Approximate sunflower
to maize ratio
9
11.5
38
28
32
possibility is that the response to mechanical stimulation
is a whole plant response, but that the roots have a higher
sensitivity to mechanical stimulation. Another is that
herbaceous plants, like trees largely respond to local
mechanical stimulation (Mattheck, 1991; Ennos, 1993).
Possibly, the roots responded more because they were
subjected to higher stresses in these experiments than the
shoots. Since the bending moments set up by flexing
plants increases towards their base (Ennos and Fitter,
1992) this possibility seems more feasible. Certainly the
lower elements of the stem which would have been more
highly stressed than the upper parts, showed a larger
1506
Goodman and Ennos
a)
Sunflower
10
15
20
25
Angle from vertical in degrees
Maize
0
5
10
15
20
Angle from vertical in degrees
Fig. 5. Graph showing the mean results of 32 sunflower and 32 maize anchorage tests. In the sunflower (a) initially moment increases linearly with
angle up to about 10° then starts to level off at 15°. Both the anchorage strength and stiffness was higher in the flexed plants (squares) compared
with that for the untreated plants (diamonds). In the maize (b) the flexed and untreated plants did not significantly differ (/ > >0.05). The results
were analysed using analysis of covariance and error bars shown are standard errors.
response to stimulation and there was a greater degree of
taper in flexed plants (Table 1).
There are several ways to test whether thigmomorphogenesis is controlled at the whole plant level or more
locally. One, is to compare the growth of plants grown
outside, half of which are supported and the other half
left to sway freely in the wind. If there is whole plant
control there would be no difference in secondary growth
between treatments because the plants grown in both
treatments have strongly stimulated leaves and petioles.
However, if growth is controlled locally the supported
plants should show reduced secondary growth in the
roots and lower stem. Results of such an experiment are
currently being analysed. A second test would be differentially to stress different sides of the root system or
individual roots and to investigate the pattern of growth
that occurs.
The responses of root systems to stem flexure have
been shown to be dramatic, demonstrating that annual
plants can adapt to mechanical stress during ontogeny.
This in turn leads to an increase in anchorage strength
(Crook and Ennos, 1996) resulting in a plant better suited
to withstanding forces, such as the wind and also the
likelihood of anchorage failure. It is important that future
work determines the mechanism by which this response
occurs.
Roots and mechanical stimulation
Acknowledgements
We would like to thank Sue Challinor, Thurston Heaton, David
Newton, and Anna Calladene for technical assistance. The
work was carried out with funding from the AFRC.
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