Effects of drought stress on root physiological traits and root biomass allocation
of Reaumuria soongorica
SHAN Lishan1, Yang caihong1, LI Yi1*, DUAN Yanan1, GENG Dongmei1, LI Zhenyin1, ZHANG
Rong1, DUAN Guifang1, Жигунов Анатолий Васильевич2
1 College of Forestry, Gansu Agricultural University, Lanzhou 730070, China
2 St.Petersburg Academy of Forestry, St.Petersburg 190121, Russia
Abstract: Plastic physiological or morphological responses to environmental stress
may be an important adaptation among plants that live in extreme environments.
Although aboveground processes have been investigated in a number of systems, the
role of belowground adaptations and responses to stress are largely unknown.
Moreover, few studies have investigated the links between above- and belowground
physiological and morphological responses. Reaumuria soongorica is a widely
distributed super-xerophytic shrub that is often dominant in arid and semiarid areas of
northwestern China. The species exhibits high plasticity, particularly in its resistance
to drought, salt and sand burial, which are prevalent stressors in desert ecosystems. In
this study, we investigated the potential adaptive strategies of R. soongorica. Drought
stress is an important restrictive factor for seedling growth and biomass accumulation
and there are numerous studies on the physiological adaptations of R. soongorica in
dry environments. However, research on drought stress has mainly focused on
aboveground parts and little is known about potential belowground adaptations in this
species. To explore the effect of drought stress on R. soongorica root physiology and
biomass allocation, a pot experiment was conducted with 2-year-old R. soongorica
seedlings, using three soil water treatments: CK: The normal water supply; MS:
Moderate stress; SS: Serious stress. Our results showed that the root activity in R.
soongorica seedlings was higher in treatments where plants were subjected to drought
stress. Compared with the control treatment, seedling root activity under moderate and
severe drought stress treatments was higher by 12.89% and 17.42%. Under
drought-stress conditions, seedling roots had relatively high triphenyltetrazolium
chloride (TTC) deoxidizing ability. This indicates that water and nutrients continued
to be delivered to the aerial portion of the plant, enabling growth even under
conditions of stress. Analysis of root chemistry revealed that superoxide dismutase
(SOD) and peroxidase (POD) activities in roots were somewhat reduced with the
increase of stress in the MS and SS treatments; however the differences were not
significant. R. soongorica seedling roots also exhibited decreased lipid peroxidation
and cleared intracellular excess H2O2 by increasing catalase (CAT) activity in the MS
and SS treatments. Presumably to protect the constituents of the cell membrane,
proline content was higher for plants in treatments subjected to drought stress, thus
facilitating osmotic regulation and higher resistance. R. soongorica seedlings
maintained low malondialdehyde (MDA) content under drought stress, suggesting
membranes did not produce lipid peroxidation. Seedling root total biomass and lateral
root biomass were highest in the MS and SS drought-stress treatments, and
*
Corresponding author. E-mail: [email protected]
lateral-root growth was the largest contributor to total root biomass in these treatments.
This study provides important evidence that under conditions of drought stress, R.
soongorica seedling roots undergo key physiological changes that confer greater
resistance to low water availability. Specifically, we found that seedlings respond to
drought conditions by redistributing their root biomass and by altering their internal
chemistry in ways that help them to maintain osmotic balance. This physiological
plasticity may be the main reason why R. soongorica can persist in the extreme arid
and semi-arid environments of northwestern China.
Key words: Reaumuria soongorica; drought resistance; root traits; root biomass
Introduction
Among the environmental stresses, drought stress is one of the most adverse
factors for plant growth and productivity in the extreme arid and semi-arid areas. The
root is the most crucial organ for absorbing water and nutrient, chemical signals such
as root-derived abscisic acid may also have influenced stomatal responses to soil
drying meeting transpirational demand at a reasonable high leaf water status, root
physiological or morphological responses to environmental stress may be an
important adaptation among plants that live in extreme environments[1]. Root as the
initial part to be affected by soil drought, its morphological and physiological
characteristics is closely correlated with plant drought resistance[2-5]. In recent years,
most research have focused on root morphological and physiological adaption to
drought stress[6,7], it has been shown that SOD, POD and CAT activity were increased
in light water stress[8-11], however, SOD and CAT activity was reduced in severe water
stress. modest levels of water stress can cause much more POD, eliminate harmful
substance and to protect membrane structure. Among the metabolic changes of
adaptation, osmotic adjustment capacity was increased and results from the
accumulation of osmotic adjusting substance[12]. Roots can always adjust their growth
and biomass allocation to adapt water stress during plant growth and development
stage. Thus it is clear that most direct damage part to drought is the plant roots, it can
be damaged by drought injury, so when the damage is noticed, it may be obvious that
root morphological and physiological was adjusted, which adapt to absorb water and
nutrition effectively, and directly related to plant drought resistance[13-15]. Therefore,
study on the response of root morphological and physiological characteristic to
drought can better reveal plant drought resistance[16,17].
R. soongorica is a widely distributed super-xerophytic shrub that is often
dominant in arid and semiarid areas of northwestern China[18]. The species exhibits
high plasticity, particularly in its resistance to drought, salt and sand burial, which are
prevalent stressors in desert ecosystems. Although aboveground drought resistance
physiology have been investigated in a number of systems[19-20], the role of
belowground adaptations and responses to stress are largely unknown. The purpose of
this research was to study the effect of drought stress on R. soongorica seedling root
physiology and biomass allocation, so that responses of these traits to drought stress
can be evaluated in resistance to drought stress.
1 Materials and methods
1.1 Plant material
The experiment was carried out in the plant growth unit, Gansu agricultural
University, Lanzhou (latitude 36º03'N, longitude 103º49'E), China. The selected
2-year-old seedlings were planted in 3.8L plastic pots (one plant per pot), filled with
yellow loamy soil with field capacity of 20.12% (g water g-1 wet weight). The
seedlings were transplanted to plastic pots with regular watering to ensure good
seedling survival, differences among watering treatment commenced on June 2, 2012.
1.2 Experimental design
The experiment was arranged in a completely randomized design with twenty
replicates per treatment. A single plant per pot was considered as a replicate. The
water stresses were applied by irrigated the plots to field capacity, three drought stress
treatments were imposed on the plants: (80±5)% field capacity (Control, CK),
(50±5)% field capacity (Moderate stress, MS) and (30±5)% of field capacity (Serious
stress, SS).
1.3 Measurements
Fresh roots R. soongorica seedling were sampled during the vigorous growth
period, that was digged from pot, washed by diluted water and weighted 5g were
stored at 4 °C in the refrigerator. root activity, SOD activity, POD activity, CAT
activity, proline content, MDA content and soluble protein were measured. All data
were measured three times at the same time and the mean used for result analysis and
discussion.
Root activity was determined by triphenyl tetrazolium chloride (TTC) method
according to Zhang zhiliang[21]. SOD, POD and CAT activity was conducted
according to Li ling et al[22]. MDA detecting was done by referring to Ling zhifang et
al[23]. Soluble protein content was determined according to the method of
Bradford[24] .
1.4 Statistical analyses
Data were subjected to analysis of variance and tested for significance by
Duncan's new multiple range test, ANOVA was used to detect differences among the
treatments using software package of SPSS(P<0.05).
2 Results
2.1 Root activity
According to Fig. 1, root activity of R. soongorica seedling was increased as the
drought stress become more serious. Compared to CK, root activity of MS and SS
treatment was increased by 12.89% and 17.42%, respectively. This is indicated that
the capacity of roots take up water from soil was not significantly influenced by
drought stress. Moreover, R. soongorica seedling roots showed a strong drought
resistance and the growth of root was not harmed under drought stress.
0.5
a
-1
a
a
-1
Root activity (mg ·g ·h FW )
0.4
0.3
0.2
0.1
0.0
CK
MS
Treatments
SS
Figure 1 Comparison of roots activity (RA) of R. soongorica under different soil moisture
2.2 Phenoloxidase activity
2.2.1 SOD activity
SOD activity of R. soongorica seedling are shown in Table 1, root SOD activity
showed a slight decrease in response to drought stress, and the change is different
with more severe drought stress. Compared to CK, SOD content of MS and SS
treatment was decreased by 11.28% and 23.41%, respectively. The variance analysis
showed that no significant difference was observed between treatment, suggesting
that R. soongorica seedling roots are less sensitive to drought stress.
2.2.2 POD activity
As shown in Table 1, POD activity of R. soongorica seedling root had a slight
decrease with more severe drought stress. MS and SS treatment decreased POD
content by 32.02% and 27.08% than CK, respectively. There is no significant
difference between treatment, also suggesting that R. soongorica seedling roots are
less sensitive to drought stress.
2.2.3 CAT activity
CAT activity in R. soongorica seedling root was presented gradual increment
trend with more severe drought stress. CAT activity was significantly increased than
that in CK (Table 1). Compared to CK, CAT activity of MS and SS treatment was
increased by 64.59% and 199.86%, respectively. The variance analysis showed that
drought stress can significantly increased CAT activity of R. soongorica seedling root,
this means that CAT activity can effectively eliminated reactive oxygen species, kept
membrane lipid peroxidation at a lower level, maintained cell membrane integrity,
and reduced membrane injury index, thus increased drought resistance, this showed
the adaptability of R. soongorica seedling to drought stress.
Table 1 Comparison of super oxide dismutase (SOD) , catalase (CAT) and peroxide enzyme (POD) in the root of R.soongorica under
different soil moisture
SOD activity (U/g Fresh weight)
The normal water supply(CK)
Moderate stress(MS)
Serious stress(SS)
4.71±0.02 a
4.18±0.43 a
3.61±0.43 a
POD activity (U/g Fresh weight)
21.52±5.79 a
14.63±1.62 a
15.69±2.99 a
CAT activity (U/g Fresh weight)
146.64±43.87 c
241.35±34.27 b
439.72±192.13a
Different letters in the same row indicate significant differences (P< 0.05) levels.
2.3 MDA
From Fig. 2, it was observed that MDA content was significantly decreased in MS
and SS than that in CK (P＜0.05). Compared to CK, MS and SS treatment increased
MDA content by 20.67% and 21.29%, respectively, however, there is no significant
difference between MS and SS. It is showed that drought stress to R. soongorica
seedling was not sufficient to cause membrane lipid peroxidation and injury to root,
showing it has strong drought resistance.
5
a
b
b
-1
MDA activity ( μmol ·g FW )
4
3
2
1
0
CK
MS
Treatments
SS
Figure 2 Comparison of malondehyde (MDA) content in the root of R.soongorica under different soil moisture
2.4 Proline
Proline content of R. soongorica seedling root was increased in both MS and SS.
Compared to CK, MS and SS treatment increased proline content by 0.07% and
61.24%, respectively. Moreover, SS treatment increased proline content by 50.93%
than that in MS treatment(Fig. 3). Proline content of R. soongorica seedling in SS was
significantly higher than that in MS and CK (P＜0.05), but no significant difference
was observed between MS and CK. This is indicated that drought stress cause an
increase in the accumulation of proline and osmotic adjustment of roots in the R.
soongorica seedling, also showed that soongorica seedling root had a strong drought
resistance.
70
a
60
50
b
Proline content
-1
( μ g ·g FW )
b
40
30
20
10
0
CK
MS
Treatments
SS
Figure 3 Comparison of proline (Pro) content in the root of R.soongorica from different soil moisture
2.5 Soluble protein
Soluble protein of R. soongorica seedling first increased and then decreased with
more severe drought stress. MS and SS treatment increased soluble protein by 18.03%
and 19.67% than CK, respectively. It is shown that there is no statistically significant
difference in soluble protein among treatments.
0.09
a
-1
mg ·g FW )
0.08
0.07
a
a
0.06
Soluble protein content(
0.05
0.04
0.03
0.02
0.01
0.00
CK
MS
Treatments
SS
Figure 4 Comparison of soluble protein (SP) content in the root of R.soongorica from different soil moisture
2.6 Root biomass
As shown in Table 1, tap root, lateral roots and total root biomass of R.
soongorica seedling in drought stress was higher than that in CK, and the maximum
was observed in MS, which increased root weight of tap root, lateral roots and total
root biomass by 41.44% and 15.44%, 70.45% and 50.00%, 50.00% and 25.80% than
CK and SS, respectively. It is appeared that root growth of R. soongorica seedling
wasn't inhibited, appropriate drought can improve root biomass accumulation, which
is also the adaptation strategy for R. soongorica seedling growing under drought
stress condition.
Table 2 Characteristics of root biomass allocation of R.soongorica under different soil moisture
Treatments
Lateral root biomass(g)
Tap root biomass(g)
Total root biomass(g)
The normal water supply(CK)
1.11±0.18
0.44±0.25
1.56±0.20
Moderate stress(MS)
1.57±0.75
0.77±0.52
2.34±1.28
Serious stress(SS)
1.36±0.23
0.50±0.15
1.86±0.33
3 Discussions
3.1 Root activity
Root activity was a comprehensive index, which reflected root absorption,
synthesis, oxidation and reduction ability. The level of root activity can reflect the
growth status of plants[25,26]. In this study, we found that root activity of R. soongorica
seedlings was increased under water stress condition, which exhibited similar results
as described for rice with higher drought resistance [27], maize seedling[25] and
stay-green maize[28]. Our research indicated that root activity was higher in R.
soongorica seedlings by enhancing root respiration, thereby showing a large number
of adenine nucleoside three phosphoric acid as an adaptation to drought stress.
However, when soil water content drops below a threshold value, roots activity of
most seedling plants will gradually lose its vitality and eventually die[29]. Root activity
of elaeagnus oxycarpa seedlings was decreased when soil water content reduced to
30%-20%, and it sharply decrease root activity, starts to harden and was seriously
turned brown by reducing soil water content to 10%-5%[30]. In this research, we can
concluded that R. soongorica seedlings retained a higher root activity in serious
drought stress, this is the reason that a larger number of R. soongorica seedlings was
survived in arid and semi-arid areas.
3.2 Phenoloxidase activity
SOD, POD and CAT which are all key enzyme to scavenge active oxygen and
protect plant cells from free radical, which can clear the O-2 away by transforming it
to H2O2 and O2[31]. It plays an important role in protecting plant cells from reactive
oxygen species and very commonly exists in plants. In this experiment, SOD and
POD activity was decreased somewhat, but no significant difference was observed. It
was indicated that increased CAT activity of R. soongorica seedlings root can
effectively eliminate the poisonous H2O2, keep the reactive oxygen free radicals in the
plants at a low level, so the plant cells are preserved from harm under drought stress
condition.
3.3 MDA content
The metabolic balance of production and scavenging of active oxygen was
damaged under drought stress condition, excessive accumulation of reactive oxygen
leads to the plant cell membrane lipid peroxidation, which resulted into the
destruction of cell membrane structure and function, leading to obvious increase in
MDA content. Therefore, MDA content was an important index of measuring plant
resistance[32]. A number of studies have shown that MDA content of plant root was
obviously increased with more severe water stress[31,33-36]. When soil water content is
14.79%, MDA content of was low. However ,it was increased under drought stress,
the maximum was observed when soil water content was reduce to 3.17% and
decreased with continuous drought stress[37]. It is indicated that P. mongolica
seedlings root membrane lipid peroxidation was increased under drought stress, but
keep the reactive oxygen free radicals in the plants at a low level, scavenging of active
oxygen, and content of MDA went down obviously. In this study, MDA content of R.
soongorica seedlings root was lower than that in CK under drought stress condition,
soil drought was not cause MDA accumulation, it is also shown that R. soongorica
seedlings root in drought stress did not lead to cell membrane lipid peroxidation,
self-regulation ability and strong drought resistance.
3.4 Proline
Proline is considered to be a compatible solute, it protects folded protein
structures against denaturation, stabilises cell membranes by interacting with
phospholipids, contribution to osmotic adjustment and tolerance of plants exposed to
unfavourable environmental conditions. Proline accumulates in many plant species
under a broad range of stress conditions such as water shortage, when drought stress
is released, and proline was quickly reduced. In this study, we found that proline
content was dramatically increased under severe drought stress condition, and the
difference was significant between MS and SS. This finding is consistent with
previous studies that have demonstrated increasing proline content of different
broomcorn millet cultivars over drought stress[31]. Proline content of R. soongorica
seedlings root was increased with drought stress, plant tissue or cell are protected
from dehydration via increasing water storage, thus drought resistance of R.
soongorica seedlings was improved. However, proline content of black soybeans was
reduced under drought stress condition[38], when soil water content reduced to 5.09%,
proline content of P. mongolica seedlings root was also decreased [37], it was shown
that root structure and cells were damaged, carbohydrate metabolism was disrupted
and the formation of glutamate and proline synthesis were affected under severe water
stress condition. So, we believe that solute concentration in cell was increased,
osmotic potential was regulated and biopolymers's hydrophilic was increased by
proline accululation, which could be part of a general adaption to drought stress
condition.
3.5 Soluble protein
The content of soluble protein can damaged by protein reaction in plant
metabolism, its content increasing can significantly increase the bound water content,
cell water holding capacity, and the cell protoplasm elasticity enhancement, which
plays an important role in the life of plant[39]. Soluble proteins are produced abundant
under drought stress, the insoluble proteins transform into soluble protein as a
adaptive response to the drought stress[40-42]. Strong drought resistance cultivar may
produced the new water stress protein in order to maintain the normal production or
reduce yield loss and the weak drought resistance cultivar is on the contrary[40, 43].
Therefore, soluble protein content of root and water stress protein are closely related
with plant drought resistance and root activity. Plant drought resistance was increased
with increasing root soluble protein and water stress protein. In this study, R.
soongorica seedlings roots soluble protein was increased in MS treatment than that in
CK, but no significant difference was observed. Root drought resistance was
increased in MS as an adaptive response to drought stress, but it was reduced in SS.
This could be sustained under severe drought stress seedling root in vivo metabolism
than catabolism, soluble protein degradation caused. This is consistent with the study
that soluble protein was increased at first, then decreased with increasing drought
stress[29,44].
3.6 Root biomass
Plants adaptations respond to drought stress by regulating biomass allocation that
help them evade, tolerate, or recover from stress. Most study suggest that root growth
is greatly affected by water deficit, plant growth was transferred to underground
biomass in the form of root, the root shoot ratio and root biomass was increased under
drought stress condition[35]. However, some study shown that tap root was inhibited
and its diameter become fine, therefore root biomass was decreased, however, all
change in the limit of adaption to drought stress[45]. It appears in our study that the
effect of drought stress on biomass allocation manifested itself more on roots than
shoots, drought stress may have a greater increase in total root biomass and levels of
lateral root, especially for lateral roots, so as to have a better chance of regrowth after
drought, drought stress can strengthen the root growth potential under drought stress.
Since R. soongorica seedlings roots are the only source to acquire water and nutrition
from soil, the increasing of root biomass, proliferation and size by drought stress as an
adaptive response to the drought stress.
Acknowledgements
The project was financially supported by the National Natural Science Foundation
of China (41361100, 31360205); Science and technology supporting program of
Gansu province, China(1204NKCA084); Special program for international science
and technology cooperation projects of China(2012DFR30830) and Doctoral fund of
ministry of education of China(20116202120001).
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