Unformatted text preview: Plant, Cell and Environment (1999) 22, 425–431 ORIGINAL ARTICLE OA 220 EN Ethylene: a regulator of root architectural responses to soil
K . BORCH, 1 T. J. BOUMA, 2* J. P. LYNCH 2 & K. M. BROWN 2
Danish Institute of Agricultural Sciences, 5792 Aarslev, Denmark, 2Department of Horticulture, Penn State University,
University Park, PA 16802, USA 1 A BSTRACT
The involvement of ethylene in root architectural responses
to phosphorus availability was investigated in common
bean (Phaseolus vulgaris L.) plants grown with sufficient
and deficient phosphorus. Although phosphorus deficiency
reduced root mass and lateral root number, main root
length was unchanged by phosphorus treatment. This
resulted in decreased lateral root density in phosphorusdeficient plants. The possible involvement of ethylene in
growth responses to phosphorus deficiency was investigated
by inhibiting endogenous ethylene production with aminoethoxyvinylglycine (AVG) and aerating the root system with
various concentrations of ethylene. Phosphorus deficiency
doubled the root-to-shoot ratio, an effect which was suppressed by AVG and partially restored by exogenous ethylene. AVG increased lateral root density in phosphorusdeficient plants but reduced it in phosphorus-sufficient
plants. These responses could be reversed by exogenous
ethylene, suggesting ethylene involvement in the regulation
of main root extension and lateral root spacing.
Phosphorus-deficient roots produced twice as much ethylene per g dry matter as phosphorus-sufficient roots.
Enhanced ethylene production and altered ethylene sensitivity in phosphorus-deficient plants may be responsible for
root responses to phosphorus deficiency.
Key-words: Phaseolus vulgaris L.; Leguminosae; common
bean; ethylene; phosphorus nutrition; root architecture. INTRODUCTION
The rate of phosphorus diffusion in soil solutions is generally slower than the absorption rate needed to sustain maximum growth rate (Nye & Tinker 1977). Hence, the ability
of the roots to explore the growth media efficiently in time
and space is very important for phosphorus uptake in low
phosphorus soils. Factors believed to directly influence
phosphorus uptake by roots are root diameter (Eissenstat
1992), root topology (Fitter 1991), root extension rate
(Barber 1995), root length and density (Baldwin 1975),
Correspondence: K. Brown. Fax: 814-863-6139; E-mail: [email protected]
*Present address: Netherlands Institute of Ecology, Center for
Estuarine and Coastal Ecology, 4400 AC Yerseke, The Netherlands.
© 1999 Blackwell Science Ltd root hairs (Jungk 1987), and the presence of mycorrhiza
Little is known about how root growth responses to phosphorus deficiency are mediated. However, the plant hormone ethylene is known to be involved in elongation of
roots, lateral and adventitious rooting, root extension, radial
expansion and aerenchyma formation [reviewed by Jackson
(1991) and Dolan (1997)]. There is evidence for ethylene
involvement in stress-related and adaptive root responses to
chemical toxicity, water stress, interactions with symbionts,
and nutrient deficiency (Lynch & Brown 1997). Such
responses may involve changes in ethylene synthesis and/or
responsiveness. For example, although phosphorus or nitrogen starvation reduced ethylene production in maize roots,
ethylene responsiveness, measured as aerenchyma formation, increased (Drew, He & Morgan 1989; He, Morgan &
Drew 1992). On the other hand, wheat seedling roots grown
under nitrogen deficiency and low pH displayed increased
ethylene production and reduced root elongation (Tari &
Szén 1995). Ethylene at high concentrations has been
reported to inhibit root growth and root gravitropic
responses (Ycas & Zobel 1983).
The objective of our study was to test the hypothesis that
ethylene is involved in the growth responses of intact bean
root systems to phosphorus deficiency. Our approach was
to measure ethylene production and responsiveness in bean
plants grown in sand amended with a solid-phase phosphorus buffer providing sufficient or deficient phosphorus. A
range of ethylene concentrations was achieved by aerating
the root zone for 4 weeks with various amounts of ethylene
while inhibiting endogenous ethylene production with
MATERIALS AND METHODS
Seeds of common bean (Phaseolus vulgaris L. CIAT
breeding line DOR364) were obtained from CIAT in Cali,
Colombia. The seeds were surface sterilized in 7 mol m–3
NaOCl and 0·1% Triton X-100 (Sigma Chemical Co., St.
Louis, MO, USA) for 10 min, and germinated in
0·5 mol m–3 CaSO4 for 36 h at 25 °C. Seedlings were then
planted at a depth of 3 cm into 1400 cm3 containers. All
plants were grown in a greenhouse in University Park, PA,
USA (40°85' N, 77°83' W). The temperature ranged from a
425 426 K. Borch et al. maximum of 26 °C (day) to a minimum of 19 °C (night).
Natural light was supplemented from 0900 to 1700 h with
110 ± 10 µmol m–2 s–1 from 400 W metal-halide bulbs
(Energy Technics, York, PA, USA). Maximum midday
photosynthetically active photon flux densities reached
1400 µmol m–2 s–1 on clear days and 500 µmol m–2 s–1 on
days with heavy cloud cover.
Plants were grown in silica sand containing solid-phase
phosphorus buffer (alumina) as described by Lynch et al.
(1990) with two different desorption concentrations
allowing precise management of phosphorus concentrations. Once a day, pots were irrigated with nutrient solution containing (in mol m–3) 3·1 NO3, 1·8 K, 1·2 Ca, 1·4
SO4, 1·0 NH4, 0·825 Mg, 0·05 Cl, 0·005 Fe-EDTA, 0·002
B, 0·0015 Mn, 0·0015 Zn, 0·000143 Mo, and 0·0005 Cu.
Sufficient and deficient phosphorus treatments contained
50 mmol m–3 and 1 mmol m–3 KH2PO4, respectively, in
the nutrient solution, in addition to the phosphorus desorbed from the alumina phosphorus buffer. Leachate
sampled from the pots was analysed using the phosphomolybdenum blue method (Murphy & Riley 1962) giving
phosphorus concentrations in the soil solution of 8·6
(± 0·9) mmol m–3 for sufficient and 1·1 (± 0·03) mmol m–3
for deficient treatments.
Ethylene and AVG treatments
In a preliminary experiment, common bean plants were
irrigated with a phosphorus-sufficient nutrient solution
mixed with a range of AVG concentrations (Fig. 1) to
determine the lowest AVG concentration which would
inhibit ethylene production from the roots without affecting growth. After visual evaluation of root size and mass,
roots were excised from 3-week-old plants, cut into 1 cm
pieces and placed in a 150 cm3 flask containing the same AVG concentration as used for irrigation during growth.
There were six plants per treatment in each of two replications. The flask was sealed with a rubber stopper and held
for 5 h in darkness at 20 °C. A 1 cm3 sample was then collected from the head space for ethylene analysis by gas
chromatography (GC). The GC (Hewlett-Packard 6890,
Palo Alto, CA, USA) was fitted with a flame ionization
detector and a column of activated alumina. The detection
limit was 0·013 cm3 m–3.
To examine the effect of ethylene on root development,
bean plants were grown under sufficient (50 mmol m–3)
and deficient (1 mmol m–3) phosphorus in the presence of
AVG plus one of four ethylene concentrations (0, 0·02, 0·1,
1 cm3 m–3). Control plants were grown without AVG or
ethylene. The roots were exposed to different ethylene concentrations without affecting the shoot atmosphere by
growing each bean plant in the apparatus shown in Fig. 2
(Bouma et al. 1997). Different ethylene concentrations
were obtained by mixing ethylene (from 1 dm3 m–3 or
0·04 dm3 m–3 gas bottles) into a stream of ambient air,
using a mass flow controller (Brooks 5800 series, Brooks
Instrument B.V., Veenendaal, The Netherlands) for the two
low concentrations and rotameters for the high concentration. Each container was provided with a flow of
500 cm3 min–1 except for the control (no AVG) and
AVG + 0 [C2H4] treatment.
Measuring ethylene concentrations in the root
The ethylene concentrations in the root zone were measured to determine the effectiveness of our ethylene perfusion treatments, and to determine ethylene production
rates by intact root systems in the absence of AVG. To
allow gas sampling, small tubes were inserted through the
sides of the containers at 14 cm depth before planting
(Fig. 2). These were open to the root zone on the inside
and sealed with a serum stopper on the outside so that the
gas space inside would be in equilibrium with the gas
space in the root zone. Ethylene samples (1 cm3) were
withdrawn from this space and analysed by GC when the
plants were 5 weeks old. There was no observable diurnal
fluctuation in ethylene production, based on sampling
every 4–6 h.
Root growth and development Figure 1. Ethylene production rate by excised roots irrigated
with different concentrations of amino-ethoxyvinylglycine (AVG),
an ethylene biosynthesis inhibitor. Bars indicate standard error of
the mean. Plants grown with the two different phosphorus availabilities were harvested after 4 weeks of ethylene exposure (just before anthesis). Leaf area, root length and
biomass of the leaves, stem and roots were determined.
The roots were excavated by rinsing the sand with deionized water. A subsample of the root (including two whole
basal roots) was collected randomly from each plant and
stained for 1 h prior to scanning to create optimal contrast
(0·16 kg m–3 neutral red dye, Sigma Chemical Co., St.
Louis, MO, USA). The leaves and the root subsamples
were scanned using a flat bed scanner (HP ScanJet II,
© 1999 Blackwell Science Ltd, Plant, Cell and Environment, 22, 425–431 Ethylene mediates phosphorus availability responses 427 Statistical analysis
Data were analysed using the PC-statistical package JMP®
(SAS Institute, Cary, NC). Data with one variable were
analysed using Student’s t-test for each pair at P < 0·05.
Data with more variables were analysed with ANOVA
(randomized block design) and mean separations were performed by contrast for each parameter by t-test and F-test
for all parameters tested jointly. When data were not
normally distributed, they were log transformed before
conducting the ANOVA.
Effect of phosphorus deficiency on root and
shoot growth Figure 2. Apparatus used to expose roots to different gas
mixtures. Air with a known ethylene concentration was pumped
into the bottom of a container filled with sand. The incoming air
was bubbled through water, which prevented desiccation of the
root zone and provided a check on the flow into each pot. Equal
flow rates in each pot were obtained by using 0·5 mm ID tubing
from the main gas source to the Erlenmeyer flask. Irrigation
solution could drain freely through the water lock. The air outlet
was on the side of the pots, above the sand surface. Shoots were
kept at ambient gas composition by sealing the top of each pot and
pumping air from the head space out of the greenhouse. A flexible
sealant (Terostat) was used to create a gas tight seal around the
stem. Gas-sampling chambers were placed at 14 cm depth. resolution = 140 dots mm–2, Hewlett Packard). Leaf area,
root length, and root diameter distribution were estimated using image analysis software (DELTA-T SCAN,
Delta-T Devices Ltd, Cambridge, UK). The total root
length was estimated by multiplying the subsample
length by the dry weight (DW) ratio of the scanned subsample and the total DW of the root. The average lateral
root length and density were determined from the
scanned subsample. The main root length was estimated
from the ratio between the lateral root length and the
basal root length in the scanned subsample. Specific root
length was calculated by dividing the total root length by
the root DW. Plant material was dried at 70 °C for 48 h
prior to dry matter determinations.
© 1999 Blackwell Science Ltd, Plant, Cell and Environment, 22, 425–431 Phosphorus deficiency reduced total root length (main plus
lateral roots) by more than one third (Fig. 3). The total lateral
root length (the product of the mean lateral root length and
the number of lateral roots) was significantly reduced by
phosphorus deficiency (Fig. 3). This was a result of the
reduction in lateral root number (Fig. 3), as mean lateral root
length was unaffected by phosphorus treatment (Table 1).
Lateral root density (the number of laterals per cm of main
root) was significantly reduced in phosphorus-deficient
roots compared with phosphorus-sufficient roots (Fig. 4).
Phosphorus deficiency reduced the DW of roots by
about one third (Table 2), but there was a proportionately
greater reduction in shoot DW, nearly doubling the root-toshoot ratio (Fig. 4).
There was no difference between the sufficient and deficient phosphorus treatments in ethylene concentrations in
the root zones. However, ethylene production per g DW
was significantly higher in phosphorus-deficient roots
compared with phosphorus-sufficient roots (Table 2).
Manipulation of ethylene with AVG and ethylene
A preliminary dose–response experiment was used to
determine the effect of AVG on growth and ethylene production by roots of bean plants grown with sufficient
phosphorus. Ethylene production by excised roots was
reduced to 10% of that of control roots when the plants
were irrigated with at least 1·28 mmol m–3 AVG (Fig. 1). Figure 3. Effect of sufficient (+P) and deficient (–P) phosphorus
concentrations in the growth media on total root length, total lateral
root length, and lateral root number (data pooled across ethylene
treatments). Bars indicate standard error of the mean. 428 K. Borch et al. Variable Statistic C2H4 Phosphorus Phosphorus ×
C2H4 Shoot dry weight (g) d.f.
ns Root-to-shoot ratio Total root length Main root length Total lateral root length Number of lateral roots Lateral root density Mean lateral root length 1 Error Table 1.
Figs 3–5 ANOVA for data presented in 90 90 90 75 90 73 86 72 Data log transformed for statistical analysis. ns, no significant difference at P < 0·05. Consequently 1·3 mmol m–3 AVG was used in our experiments, resulting in ethylene concentrations below detection levels (< 0·013 cm3 m–3 ethylene) in pots irrigated
with AVG and without ethylene perfusion (Table 3).
Ethylene treatments to the root zones of AVG-treated
plants resulted in stable ethylene concentrations bracketing
the physiological range (Table 3). There were no significant differences between phosphorus-sufficient and -deficient plants in ethylene concentrations in the root zones.
Interactions between phosphorus and ethylene
AVG and AVG + ethylene treatments resulted in a small
but significant increase in shoot DW (Fig. 4). The small
increase in shoot DW (from 0·49 to 0·54 g, Fig. 4) combined with a decrease in root DW (0·23 to 0·19 g) resulted
in a significant reduction in the root-to-shoot ratio when
phosphorus-deficient plants were treated with AVG
(Fig. 4). There was a significant phosphorus–ethylene
interaction for the root-to-shoot ratio (Table 1).
The total root length (all main and lateral roots) was
reduced by phosphorus deficiency and by ≥ 0·1 cm3 m–3
ethylene (Figs 3 & 5), but there was no significant interaction between phosphorus and ethylene for this variable
AVG treatment increased the main root length of phosphorus-sufficient plants, an effect which was reversed by
added ethylene (Fig. 4). The ethylene-modifying treatments had opposite, although smaller, effects on phosphorus-deficient plants (Fig. 4). Unlike the effects on total root length, high ethylene concentrations did not significantly
reduce the length of the main roots compared with controls
(no AVG, no ethylene) (Fig. 4). The effects of AVG and
ethylene on total lateral root length resembled their effect
on total root length, with no significant interaction between
phosphorus and ethylene (Fig. 5 & Table 1).
The reduction in main root length caused by AVG in
phosphorus-deficient plants (Fig. 4) was not accompanied
by a significant change in lateral root number (Table 1),
resulting in an increase in lateral root density (Fig. 4). The
AVG effect was reversed by low ethylene concentrations.
AVG had the opposite effect on phosphorus-sufficient
roots: it reduced lateral root density, probably by increasing main root elongation (Fig. 4).
AVG and ethylene reduced the mean lateral root length
regardless of phosphorus treatment (Fig. 5 & Table 1).
Although root diameter was unaffected by phosphorus
treatment, the high ethylene treatment increased root diameter and reduced specific root length (cm mg DW–1) (data
not shown). DISCUSSION
Effect of phosphorus deficiency on root
The changes in root architecture observed under phosphorus deficiency suggest that resources are redistributed to
the roots to allow continued exploration for phosphorus.
Phosphorus deficiency resulted in the inhibition of both
© 1999 Blackwell Science Ltd, Plant, Cell and Environment, 22, 425–431 Ethylene mediates phosphorus availability responses 429 affected by phosphorus deficiency (Table 1). The maintenance of growth of these roots would be expected to maximize the soil volume colonized by roots, and, therefore,
access to phosphorus resources.
In real soils, phosphorus availability is non-uniform.
From an economic perspective (Bloom, Chapin & Mooney
1985; Fitter 1991), an efficient root system would explore
the soil extensively in order to locate phosphorus-rich
patches or microsites, but once such a patch is found,
should intensively exploit that patch. This strategy could
be implemented if roots responded differently to the phosphorus availability in their immediate soil environment,
such that branching was more intense where phosphorus
was most concentrated, whereas extension of main root
axes was accentuated when phosphorus was limiting. In
previous research on plants grown with heterogeneous
phosphorus distribution, roots growing in a low phosphorus patch elongate but do not proliferate (develop quantities of fine roots), while in a high phosphorus patch, the
reverse occurs: main root elongation is reduced, but proliferation is enhanced (Drew & Saker 1978; Snapp, Koide &
Lynch 1995). In this study, we found a similar response to
phosphorus availability in a homogeneous substrate, as has
also been reported for Chrysanthemum (Hansen & Lynch
1998) and some families of Pinus radiata (Theodorou &
Bowen 1993). The ability of plants to sense and respond to
local phosphorus availability suggests the presence of a
signalling mechanism to regulate changes in plant growth.
Does ethylene mediate root architectural
responses to nutrient stress?
In non-AVG-treated plants, phosphorus-deficient roots
produced twice as much ethylene per g as phosphorus-sufficient roots, resulting in similar root zone ethylene concentrations despite reduced root biomass in
phosphorus-deficient plants (Table 2). Ethylene concentrations in the root tissues would be higher in phosphorusdeficient roots than in phosphorus-sufficient roots, because
the production rate is higher. Increased internal ethylene
could mediate some of the observed growth and development responses to phosphorus deficiency.
When endogenous ethylene production was greatly
reduced by AVG, there was a significant interaction
between phosphorus availability and ethylene treatment,
indicating that phosphorus deficiency changes tissue
responsiveness to ethylene. Ethylene could, therefore, Figure 4. Effect of amino-ethoxyvinylglycine (AVG) and
ethylene treatments on shoot dry weight, root-to-shoot ratio, main
root length and lateral root density of phosphorus-sufficient or deficient plants. Bars indicate standard error of the mean. root and shoot growth, but the disproportionate reduction
in shoot growth relative to root growth led to a higher rootto-shoot ratio (Fig. 3). The main root length (Figs 3 & 4)
and the average lateral root length were not significantly Phosphorus treatment Root DW
(g) Root zone [C2H4]
(cm3 m–3) C2 H 4
(cm3 m–3 g DW–1 root) Sufficient
Deficient 0·35 ± 0·02a
0·25 ± 0·02b 0·027 ± 0·002a
0·025 ± 0·002a 0·078 ± 0·007a
0·124 ± 0·018b © 1999 Blackwell Science Ltd, Plant, Cell and Environment, 22, 425–431 Table 2. Root dry weight (DW), ethylene
concentration in the root zone, and ethylene
concentration per g DW root in 5-week-old
bean plants grown with sufficient or
deficient phosphorus nutrition and no aminoethoxyvinylglycine (AVG). Values shown
are means of 10 plants ± standard error of the
mean. Values within columns followed by
different letters indicate significant
differences in a Student’s t-test at P < 0·05 430 K. Borch et al. Ethylene in perfused air
(cm3 m–3) Phosphorus
(mmol m–3) AVG
(mmol m–3) Ethylene
(cm3 m–3) n 0
1 Sufficient (50)
50 + 1
50 + 1
50 + 1
50 + 1 0
1 0·027 ± 0·002
0·025 ± 0·002
0·026 ± 0·009
0·12 ± 0·036
1·12 ± 0·31 10
20 Figure 5. Effect of amino-ethoxyvinylglycine (AVG) and various
ethylene concentrations in the root zone on total root length (main
plus lateral roots), total lateral root length, and average lateral root
length (data pooled across phosphorus treatments). Bars indicate
standard error of the mean. Table 3. Ethylene concentration in the root
zone of ethylene- and aminoethoxyvinylglycine (AVG)-treated plants.
Plants without AVG were not perfused with
either ethylene or air in the root zone.
Ethylene data are pooled for sufficient and
deficient phosphorus plants irrigated with
AVG because there were no significant
differences between phosphorus treatments.
Values shown are the means ± the standard
error of the mean for six plants in each of
two replications mediate changes in root morphology via both changes in
synthesis and changes in tissue responsiveness. Low
endogenous ethylene has been shown to promote root
extension in seedling roots for some species, although
higher concentrations generally inhibit root growth
(Smith & Robertson 1971; Konings & Jackson 1979;
Jackson 1985, 1991; Abeles, Morgan & Saltveit 1992).
We show here that the effect of ethylene on root length
depends on the root type (main or lateral root) and on
phosphorus nutrition. In phosphorus-sufficient plants, the
main root length was increased by AVG treatment
(Fig. 4), indicating that endogenous ethylene production
limits main root growth. In phosphorus-deficient plants,
AVG inhibited main root growth and exogenous ethylene
reversed this effect (Fig. 4), indicating that ethylene promotes root extension under phosphorus deficiency. This
is consistent with the hypothesis that ethylene action
makes possible the maintenance of root extension under
phosphorus-deficient conditions, despite an overall
reduction in root growth.
Ethylene appears to be important for the reduction in lateral root density observed in phosphorus-deficient plants.
AVG reduced lateral root density in phosphorus-sufficient
plants but increased it in phosphorus-deficient plants; both
effects were reversible with exogenous ethylene. Because
the lateral root number was unaffected in both phosphorus
treatments (Fig. 3), the observed AVG effect on lateral root
density (Fig. 5) is probably a result of the opposite effects
of AVG on main root length (Fig. 4).
Previous research on the effect of ethylene on root
growth utilized plants supplied with sufficient or surplus
phosphorus. The present study shows that the response of
roots to ethylene depends on phosphorus availability. By
irrigating with low, non-toxic AVG concentrations and
flushing the root zone with ethylene, we succeeded in
exposing the roots to ethylene concentrations in the physiologically relevant range. This method allowed us to
show that ethylene permits continued root extension,
even under phosphorus deficiency. Moreover, ethylene
seems to be involved in the reduction of lateral root density that occurs in low phosphorus-deficient soils, which
may be advantageous for efficient soil exploration. These
findings support the hypothesis that ethylene may be a
global regulator of root responses to soil nutrient availability (Lynch & Brown 1997).
© 1999 Blackwell Science Ltd, Plant, Cell and Environment, 22, 425–431 Ethylene mediates phosphorus availability responses A CKNOWLEDGMENTS
This research was partially supported by USDA-NRI
grants 94-37100-0311 and 97-35100-4456.
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Received 2 July 1998; received in revised form 9 October 1998;
accepted for publication 9 October 1998 ...
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