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1 s2.0 S0176161718300397 Main - 3
1 s2.0 S0176161718300397 Main - 3
A R T I C LE I N FO A B S T R A C T
Keywords: The objective of this study was to investigate the root growth compensatory effects and cotton yield under
Cotton drought stress. The results indicate that the root dry weight, boll weight, and cotton yield increased in both the
Drought drought-resistant cultivar (CCRI-45) and the drought-sensitive cultivar (CCRI-60). Compensation effects were
Compensation exhibited under the three-day drought stress treatment at a soil relative water content (SRWC) of 60% and 45%
Physiology
during the seedling stage, and flowering and boll-forming stage over two years. The yield of the drought-re-
Yield
sistant cultivar (CCRI-45) was higher than the control, however, following the six-day 45% SRWC drought
treatments, the yield of the drought-sensitive cultivar (CCRI-60) was lower than the control. The soluble sugar
content, proline content, superoxide dismutase (SOD) activity, and peroxidase (POD) activity of the roots in-
creased under drought stress and then decreased after re-watering, although the values remained higher than
those of the controls for a short period. These physiological measures may represent stress reactions and thus
may not indicate factors that result in compensation effects. However, catalase (CAT) activity and gibberellic
acid (GA) content of the roots decreased under drought stress. After re-watering, the CAT activity and the GA
content increased and were significantly higher than those of the controls under the six-day 60% SRWC and 45%
SRWC drought treatments. The abscisic acid (ABA) content of the roots increased under drought stress. After re-
watering, the ABA content decreased to a lower level under the three and six-day 60% SRWC and 45% SRWC
drought treatments than in the controls. According to an analysis of various indicators, the interaction between
ABA and GA signals may play an important role in root growth compensatory effects. In summary, the results
demonstrate that moderate drought stress is beneficial to root growth and yield. This conclusion is of great
significance to improving our understanding of the maximum utilization of limited water resources.
Abbreviations: SRWC, soil relative water content; SOD, superoxide dismutase; POD, peroxidase; CAT, catalase; GA, gibberellic acid; ABA, abscisic acid
⁎
Corresponding authors.
E-mail addresses: niujing890321@163.com, 1259637820@qq.com (J. Niu), zhsp5337@163.com (S. Zhang), chypang@163.com (C. Pang), zhaoxinhua1968@126.com (X. Zhao).
1
These authors contributed equally to this study.
https://doi.org/10.1016/j.jplph.2018.03.001
Received 14 November 2017; Received in revised form 2 March 2018; Accepted 2 March 2018
Available online 09 March 2018
0176-1617/ © 2018 The Authors. Published by Elsevier GmbH. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/).
J. Niu et al. Journal of Plant Physiology 224–225 (2018) 30–48
increased significantly under a moderate water deficit during the filling of fruiting branch nodes, and the bolls per plant were counted from the
stage, thereby increasing production (Foulkes et al., 2007). Yang et al. tagged plants, and the mean values were measured and expressed as the
(2001) and Hsiao et al. (2007) also found similar results. Additionally, number per plant. The weights of fully opened and matured bolls
cotton is often considered a drought-resistant crop and exhibits infinite picked from ten plants were recorded, and the mean boll weight was
growth. The root, leaf, bud, and flower can be grown repeatedly with calculated to estimate the yield of cotton. The fiber length, uniformity
re-watering to compensate for injuries under drought stress. Studies index, micronaire, elongation rate, and fiber strength were measured by
have shown that the cotton yield and fiber strength of certain cotton the Ministry of Agriculture on Cotton Quality Inspection Center.
cultivars were improved when the irrigation volume was moderately
decreased (Dağdelen et al., 2009; Papastylianou and Argyrokastritis, 2.3. Determining the proline content, soluble sugar content, soluble protein
2014). content, and antioxidant enzyme activity
The root is an integral plant organ that is involved in the acquisition
of nutrients and water; the synthesis of plant hormones, organic acids, The proline content was determined according to the Bates method
and amino acids; and the anchorage of plants (Chloupek et al., 2010; (1973). Dry roots (0.15 g) were homogenized in 5 mL of 3% sulfosa-
Středa et al., 2012). Root morphology and physiology are closely as- licylic acid at 100 °C for 20 min in a water bath and then filtrated. The
sociated with the growth and development of aboveground plant ma- filtrate (2 mL) was mixed with acid-ninhydrin (2 mL) and glacial acetic
terial. The root is the initial part affected by soil drought, and its acid (2 mL) in a test tube. The reaction mixture was incubated in a
morphological and physiological characteristics are closely correlated water bath at 100 °C for 30 min, cooled to room temperature, and then
with plant drought resistance (Gajri et al., 1989). Therefore, studying extracted with toluene (5 mL). The toluene, which contains chromo-
the compensation effect of cotton roots is of great significance to cotton phores, was aspirated, and the absorbance was then measured at
production and water-saving irrigation. The aims of this study were to 520 nm. The soluble sugar content of the roots was determined using
(i) clarify the compensation effects of cotton root dry weight, yield, the anthrone-sulfuric acid method (Yemm and Willis, 1954). The dry
quality, and root physiological indices and (ii) identify the mechanisms roots (0.1 g) were homogenized in 5 mL of 80% ethanol at 80 °C for
underlying the root compensation effects. 30 min in a water bath, and then the supernatant was collected. The
above steps were repeated twice. The filtrate (2 mL) was mixed with
2. Materials and methods anthrone-sulfuric acid (2 mL) in ice water, and the reaction mixture was
then incubated in a water bath for 10 min at 100 °C and then cooled to
2.1. Treatment, experimental design, and management room temperature. Afterwards, the absorbance was measured at
620 nm.
Field experiments were conducted at the experimental farm of the Fresh root tissues (0.3 g) were ground with 5 mL of 50 mM phos-
Institute of Cotton Research, Chinese Academy of Agricultural Sciences, phate buffer (pH 7.0), which was prepared by mixing NaH2 PO4·H2O
Anyang, Henan Province, China (36°06′N, 114°21′E) during the cotton and Na2HPO4·7H2O and then centrifuging at 12000g for 20 min at 4 °C.
growing seasons of 2014 and 2015. The chemical properties of the field Then, the supernatant was collected to measure the antioxidant enzyme
soil were measured for two years (attached Table A1), and the me- activity and the soluble protein content. The superoxide dismutase
teorological data are shown in the attached Table A2. (SOD) activity was determined using reagent kits (obtained from the
The cultivars CCRI-45 and CCRI-60 were planted in plastic pots Nanjing Jiancheng Bioengineering Institute, Nanjing, Jiangsu Province,
(33 cm × 706.5 cm2) filled with 27 kg of sandy loam soil, with five China, WST-1method). The peroxidase (POD) and catalase (CAT) ac-
plants per pot in the seedling stage (for a total of 216 pots) and one tivities were measured using the guaiacol method and the ultraviolet
plant per pot in the flowering and boll-forming period (for a total of 270 absorption method (Li et al., 2000a). The soluble protein content was
pots). The experiment was designed for the seedling stage, and flow- determined from the same enzyme extract using Brilliant Blue G-250
ering and boll-forming stage. Three water treatments were imposed on dye (Bradford, 1976).
the plants: 75% ( ± 5%) of field capacity (control, CK), 60% ( ± 5%) of
field capacity (mild drought stress, D1), and 45% ( ± 5%) of field ca- 2.4. Determining the ABA and GA content
pacity (moderate drought stress, D2). The maximum amount of water
the soil can retain by capillary action is known as the field capacity Approximately 0.5 g of fresh sample was collected, and the en-
(FC). Changes in the soil relative water content (SRWC) during the dogenous ABA and GA were extracted according to a previously re-
experiments are shown in Fig. A1. Drought stress lasted for three days, ported method (Yang et al., 2001) using an enzyme-linked im-
six days, and nine days for each treatment, and then all plants under- munosorbent assay (ELISA). The ELISA kits were manufactured by the
went re-watering. Phytohormones Research Institute, China Agricultural University.
In both years, the experiment was arranged in a completely ran-
domized design. Cotton was grown in a plastic greenhouse to prevent 2.5. Data analysis
exposure to natural rainfall, and the cultivation management methods
were consistent (except the water treatments). The SRWC was de- The results were analyzed via analyses of variance (ANOVAs) using
termined by weighing the soil samples, which were collected every two Statistical Analysis System 8.1. The means were analyzed using the
days. The soil fresh weight (FW) was recorded, the samples were dried least significant difference (LSD) method at P = 0.05 (LSD 0.05).
to a constant weight, and then the final dry soil weight (DW) was re-
corded. The water mass content of the soil (in percentage terms) was 3. Results
equal to (FW − DW)/DW × 100, and the SRWC was equal to SRWC
(%) = SWC/FC × 100. The SRWC was maintained within the pre- 3.1. Effect of drought stress on the cotton yield and fiber quality
scribed levels during the experiment.
The yield of cotton increased under the three-day and six-day
2.2. Determination of the root biomass, agronomic performance, yield, and drought treatments (Tables 1, A3 and A4). In both years, the yields of
fiber quality of cotton two cultivars were higher than those of the controls under the three and
six-day 60% SRWC and 45% SRWC drought treatments. During the
Traditional methods were used to obtain all the roots, which were seedling period, the highest yields of CCRI-45 (the drought-tolerant
rinsed with water after blistering for two hours. The roots were weighed cultivar) were observed under the six-day 60% SRWC drought treat-
after drying to a constant weight at 80 °C. The plant height, the number ments in 2014 and 2015, exhibiting yields 27.27% and 22.34% higher
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J. Niu et al. Journal of Plant Physiology 224–225 (2018) 30–48
Table 1
Changes in the cotton yield and yield composition under drought stress after re-watering during the seedling stage in 2015.
Varieties
CCRI-45 CCRI-60
Treatment Boll number per plant Boll weight (g) Lint (%) Lint cotton yield (kg Hm−2) Boll number per plant Boll weight (g) Lint (%) Lint cotton yield (kg Hm−2)
Note: CK: SRWC (75 ± 5)%; D1: SRWC (60 ± 5)%; D2: SRWC (45 ± 5)%; L3: drought stress for three days; L6: drought stress for six days; and L9: drought stress for nine days. In the
columns, different letters indicate significant differences at the 0.05 probability level.
Table 2
Changes in the final agronomic traits of cotton under drought stress after re-watering during the seedling stage in 2015.
Varieties
CCRI-45 CCRI-60
Treatment Height (cm) Fruiting branch nodes Fruiting positions Shedding rate Height (cm) Fruiting branch nodes Fruiting positions Shedding rate
number number (%) number number (%)
Note: CK: SRWC (75 ± 5)%; D1: SRWC (60 ± 5)%; D2: SRWC (45 ± 5)%; L3: drought stress for three days; L6: drought stress for six days; and L9: drought stress for nine days. In the
columns, different letters indicate significant differences at the 0.05 probability level.
Table 3
Changes in the cotton fiber quality under drought stress after re-watering during the seedling stage in 2015.
Varieties
CCRI-45 CCRI-60
Treatment Fiber length Uniformity index Micronaire Elongation rate Fiber strength Fiber length Uniformity index Micronaire Elongation rate Fiber strength
(mm) (%) (%) (cN/tex) (mm) (%) (%) (cN/tex)
CK 29.47a 83.73a 5.30a 6.70a 28.80c 28.03a 83.23a 5.67a 6.60a 27.63ab
D1L3 29.73a 85.90a 5.17a 6.73a 28.93bc 28.43a 84.20a 5.30a 6.60a 28.87a
D2L3 29.53a 84.90a 5.27a 6.67a 30.30ab 28.57a 84.37a 5.43a 6.60a 28.80a
D1L6 29.90a 86.20a 5.43a 6.70a 30.70a 28.97a 84.73a 5.63a 6.63a 29.30a
D2L6 29.40a 85.20a 5.40a 6.67a 31.70a 28.33a 84.33a 5.73a 6.60a 27.57ab
D1L9 29.93a 83.20a 5.60a 6.70a 27.60cd 27.83a 82.87a 5.50a 6.60a 25.97bc
D2L9 29.33a 82.07a 5.57a 6.67a 26.77d 27.57a 82.37a 5.57a 6.57a 24.90c
Note: CK: SRWC (75 ± 5)%; D1: SRWC (60 ± 5)%; D2: SRWC (45 ± 5)%; L3: drought stress for three days; L6: drought stress for six days; and L9: drought stress for nine days. In the
columns, different letters indicate significant differences at the 0.05 probability level.
than those of the control, respectively (Tables 1 and A3). The yields of elongation rate of CCRI-60 increased under the three-day 60% SRWC
CCRI-60 (the drought-sensitive cultivar) were highest under the three- and 45% SRWC treatments and the six-day 60% SRWC treatments, but
day 45% SRWC and six-day 60% SRWC treatments in 2014 and 2015, it decreased under the six-day 60% SRWC treatments and the nine-day
exhibiting yields 18.92% and 18.56% higher than those of the control, 60% SRWC and 45% SRWC treatments (Tables 3, A7 and A8).
respectively (Tables 1 and A3). Compared with CCRI-60, the yield and
the increment of CCRI-45 were higher under the six-day 60% SRWC 3.2. Effects of drought stress on cotton roots
treatments. The increase in production was primarily related to the
increase in the boll weight, which was measured by analyzing the yield The increase in yield may have been caused primarily by the com-
component indices (Tables 2, A5 and A6). In both the drought-tolerant pensation effects of the root. Therefore, we further analyzed the
and the drought-sensitive cultivars, the nine-day 60% SRWC and 45% changes in the root dry weights under drought stress and re-watering.
SRWC treatments resulted in significantly lower yields compared to As shown in Figs. 1, A2 and A3, the root dry weight of the two varieties
those of the controls. The elongation rate of CCRI-45 increased under increased under the three and six-day 60% SRWC and 45% SRWC
the three and six-day 60% SRWC and 45% SRWC treatments, but de- treatments, although the root dry weights of CCRI-60 were lower than
creased under the nine-day 60% SRWC and 45% SRWC treatments. The those of the controls under the six-day 45% SRWC droughts in 2014.
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J. Niu et al. Journal of Plant Physiology 224–225 (2018) 30–48
Fig. 1. Changes in the cotton root dry weight under drought stress and re-watering during the seedling stage in 2015.
Note: L3: drought stress for three days; L3-5: fifth day after re-watering following three-day drought stress; L3-10: tenth day after re-watering following three-day drought stress; L6:
drought stress for six days; L6-5: fifth day after re-watering following six-day drought stress; L6-10: tenth day after re-watering following six-day drought stress; L9: drought stress for nine
days; L9-5: fifth day after re-watering following nine-day drought stress; and L9-10: tenth day after re-watering following nine-day drought stress. In the columns, different letters indicate
significant differences at the 0.05 probability level.
The root dry weights of the two varieties decreased significantly under SOD and POD activities. After re-watering, the CAT activity of the
the nine-day 60% SRWC and 45% SRWC treatments during both years. cotton root increased, thereby demonstrating the compensation effect.
After re-watering, the roots grew rapidly and the root dry weight in- The CAT activity of cotton roots was higher than that of the controls
creased. On the tenth day after re-watering, the root dry weights of both under the three and six-day 60% SRWC and 45% SRWC treatments.
varieties were highest under the three-day 45% SRWC and six-day 60% However, under the nine-day drought stress, the value remained lower
SRWC treatments during the seedling stage in 2014 and 2015. Com- than that of the controls (Figs. 6, A14 and A15). Compared with the
pared with the root dry weight of the controls, that of CCRI-45 in- CAT activity of the controls, that of CCRI-45 plants was highest under
creased by 31.21% and 19.77% (Figs. 1 and A2), and the root dry the six-day 60% SRWC drought treatments in 2014 and 2015, in-
weight of CCRI-60 increased by 9.36% and 20.13% in 2014 and 2015, creasing by 14.65% and 45.63%, respectively. The CAT activity of
respectively (Figs. 1 and A2). Although the root dry weights increased CCRI-60 was highest under the three day and six-day 60% SRWC
under the nine-day 60% SRWC and 45% SRWC treatments, the dry treatments in 2014 and 2015, increasing by 13.12% and 26.48%, re-
weights were still lower than those of the controls (Figs. 1, A2 and A3). spectively (Figs. 6 and A14). Additionally, the CAT activity increments
of CCRI-45 were higher than those of CCRI-60 under the six-day 60%
SRWC drought treatments.
3.3. Changes in the root physiology under drought stress
As the degree and duration of drought stress increased, the ABA
content of the roots increased. After re-watering, the ABA content de-
The physiological characteristics of the roots are closely correlated
creased (Figs. 7, A16 and A17). On the tenth day after re-watering, the
with the root growth and drought resistance of the plant. As the degree
ABA content returned to normal levels or lower levels than in the
and duration of drought stress increased, the soluble sugar content
controls. Compared with the ABA content of the controls, those of CCRI-
(Figs. 3, A6 and A7), proline content (Figs. 3, A6 and A8), and SOD
45 decreased by 13.31% and 14.48% under the six-day 60% SRWC
(Figs. 5, A11 and A12) and POD (Figs. 5, A11 and A13) activities of
treatments in 2014 and 2015, respectively, and the ABA contents of
both varieties of cotton increased. After re-watering, these values de-
CCRI-60 decreased by 19.90% and 15.63% under the three-day 45%
creased, although they were still higher than those of the controls
SRWC and six-day 60% SRWC treatments (Figs. 7 and A16), respec-
during the two stages. During the seedling period, the soluble protein
tively, during the seedling period in 2014 and 2015.
content of the cotton root decreased under the three and nine-day 60%
However, the GA content of the roots increased under the three-day
SRWC and 45% SRWC treatments, but they increased under the six-day
60% SRWC and 45% SRWC treatments and then decreased under the
60% SRWC and 45% SRWC treatments. After re-watering, the soluble
six and nine-day 60% SRWC and 45% SRWC treatments. After re-wa-
protein contents returned to normal levels or higher levels than those of
tering, the GA content increased (Figs. 7, A16 and A18). On the tenth
the controls (Figs. 4, A9 and A10).
day after re-watering, the GA content of the roots was significantly
The CAT activity showed an opposite trend relative to that of the
Fig. 2. Relationship between the increased percentages of yield and root dry weight under drought stress after re-watering during the seeding stage in 2015.
Note: * and ** indicate significant differences at 0.05 and 0.01 probability levels, respectively (n = 6, R0.05 = 0.811, and R0.01 = 0.917).
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J. Niu et al. Journal of Plant Physiology 224–225 (2018) 30–48
Fig. 3. Changes in the soluble sugar and proline content in cotton roots under drought stress and re-watering during the seedling stage in 2015.
Note: L3: drought stress for three days; L3-5: fifth day after re-watering following three-day drought stress; L3-10: tenth day after re-watering following three-day drought stress; L6:
drought stress for six days; L6-5: fifth day after re-watering following six-day drought stress; L6-10: tenth day after re-watering following six-day drought stress; L9: drought stress for nine
days; L9-5: fifth day after re-watering following nine-day drought stress; and L9-10: tenth day after re-watering following nine-day drought stress. Changes in the soluble sugar content
2015: A and B; changes in the proline content in 2015: C and D. In the columns, different letters indicate significant differences at the 0.05 probability level.
Fig. 4. Changes in the soluble protein content in cotton roots under drought stress and re-watering during the seedling stage in 2015.
Note: L3: drought stress for three days; L3-5: fifth day after re-watering following three-day drought stress; L3-10: tenth day after re-watering following three-day drought stress; L6:
drought stress for six days; L6-5: fifth day after re-watering following six-day drought stress; L6-10: tenth day after re-watering following six-day drought stress; L9: drought stress for nine
days; L9-5: fifth day after re-watering following nine-day drought stress; and L9-10: tenth day after re-watering following nine-day drought stress. In the columns, different letters indicate
significant differences at the 0.05 probability level.
higher than that of the controls under the three and six-day 60% SRWC stress, as well as the intensity of the compensation effect and the re-
and 45% SRWC treatments, but it was still significantly lower than that sponse of yield and quality after re-watering at the seedling stage, and
of the controls under the nine-day 60% SRWC and 45% SRWC treat- flowering and boll-forming stage. The study showed that soluble sugar,
ments. The GA content of CCRI-45 was the highest under the six-day proline, SOD, POD, and ABA showed an increasing trend under the
60% SRWC drought stress in 2014 and 2015 and, compared with the drought stress, while GA and CAT decreased. After re-watering, the
controls, increasing by 49.68% and 38.95%, respectively. The GA recovery of all the physiological indices and the root dry weight and
content of CCRI-60 was the highest under the three-day 45% SRWC and yield was comparable with the control.
the six-day 60% SRWC treatments in 2014 and 2015, increasing by However, the resilience of cotton is different under different degrees
45.50% and 32.37% (Figs. 7 and A16), respectively, during the seedling of drought stress, showing an overcompensation effect, equal com-
period in 2014 and 2015. The GA increments of CCRI-45 were higher pensation effect, and partial compensation effect. The study found that
than those of CCRI-60 under the six-day 60% SRWC drought. the changes in CAT, GA, and ABA were closely related to cotton yield
after re-watering. The results provide some theoretical basis for
4. Discussion drought-tolerant cultivation and water-saving irrigation, and explain
the drought-resistant mechanism of cotton and the compensation effect.
In recent years, the frequency and degree of drought have been on
the rise. Cotton often encounters long-term drought stress, which ser- 4.1. Moderate drought stress can promote cotton growth
iously affects the cotton yield. However, there is a positive regulation
mechanism that can compensate the effect of drought stress after re- In this study, the data showed that the boll number and yield were
watering to some extent. In this paper, we systematically studied the higher than those of the controls under the three and six-day 60%
response of each physiological index of two cultivars under drought SRWC and 45% SRWC treatments during the seedling stage, and
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J. Niu et al. Journal of Plant Physiology 224–225 (2018) 30–48
Fig. 5. Changes in the SOD and POD activity in cotton root under drought stress and re-watering during the seedling stage in 2015.
Note: L3: drought stress for three days; L3-5: fifth day after re-watering following three-day drought stress; L3-10: tenth day after re-watering following three-day drought stress; L6:
drought stress for six days; L6-5: fifth day after re-watering following six-day drought stress; L6-10: tenth day after re-watering following six-day drought stress; L9: drought stress for nine
days; L9-5: fifth day after re-watering following nine-day drought stress; and L9-10: tenth day after re-watering following nine-day drought stress. Changes in the SOD activity in 2015: A
and B; changes in the POD activity in 2015: C and D. In the columns, different letters indicate significant differences at the 0.05 probability level.
Fig. 6. Changes in the CAT activity in cotton roots under drought stress and re-watering during the seedling stage in 2015.
Note: L3: drought stress for three days; L3-5: fifth day after re-watering following three-day drought stress; L3-10: tenth day after re-watering following three-day drought stress; L6:
drought stress for six days; L6-5: fifth day after re-watering following six-day drought stress; L6-10: tenth day after re-watering following six-day drought stress; L9: drought stress for nine
days; L9-5: fifth day after re-watering following nine-day drought stress; and L9-10: tenth day after re-watering following nine-day drought stress. In the columns, different letters indicate
significant differences at the 0.05 probability level.
flowering and boll-forming stage, and the drought-tolerant cultivar et al., 2000b) and the budding stage (Yan et al., 2009); we also obtained
(CCRI-45) showed a greater compensation effect than the drought- similar results. Studies have not been able to explain the changes oc-
sensitive cultivar (CCRI-60). These findings have also been gained in curring in cotton root after re-watering. Therefore, we decided to focus
previous studies: the cotton yields of some cotton cultivars improved on these changes in our study. After re-watering, the root system had a
when the drip irrigation volume was moderately reduced during the stronger water absorbing capacity, the roots grew rapidly, and the root
growth stage (Wanjura et al., 2002; Ertek and Kanber, 2003; Kang et al., dry weights increased, especially under the six-day 60% SRWC drought
2012), and the fiber quality decreased under an irrigation deficit stress treatment. In addition, the increments of CCRI-45 (the drought-
(Dağdelen et al., 2009; Ünlü et al., 2011). However, possibly due to the resistant cultivar) were higher than those of CCRI-60 (the drought-
long-term drought, the boll number and yield decreased under the nine- sensitive cultivar). In rice (Chu et al., 2014) and corn (Liang et al.,
day 60% and 45% SRWC treatments, which is similar to the findings of 2008; Qi et al., 2010) the root growth also accelerated, especially in the
a previous study (Wang et al., 2013). The above findings proved that a lateral roots and root hairs, and the root biomass was significantly in-
certain range of drought stress can promote the yield of cotton. They creased after undergoing moderate drought. However, because the
also showed that the intensity of the compensation effect varied in cotton suffered irreversible damage after a drought of nine days, the
cultivars. However, the cotton yield will suffer serious irreversible da- root dry weights were significantly lower after re-watering. These re-
mage when this drought range is exceeded. sults indicate that moderate drought stress is beneficial to root growth,
Roots, as the main organs for water and nutrient uptake, play an and a strong root system not only improves the drought resistance but
important role in the formation of plant drought resistance also promotes the recovery of cotton growth.
(Ramamoorthy et al., 2017). Thus, we hypothesized that the increase in An analysis of the yield and root dry weight showed that the yield
yield may be caused largely by the compensation effects in the root. and root dry weight are closely correlated after re-watering (Figs. 2, A4
Studies have found that the cotton root growth and root biomass in- and A5), suggesting that the root dry weight might be used as an in-
creased under moderate drought stress during the seedling stage (Li dicator of the drought resistance of a crop.
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J. Niu et al. Journal of Plant Physiology 224–225 (2018) 30–48
Fig. 7. Changes in the ABA and GA content in cotton root under drought stress and re-watering during the seedling stage in 2015.
Note: L3: drought stress for three days; L3-5: fifth day after re-watering following three-day drought stress; L3-10: tenth day after re-watering following three-day drought stress; L6:
drought stress for six days; L6-5: fifth day after re-watering following six-day drought stress; L6-10: tenth day after re-watering following six-day drought stress; L9: drought stress for nine
days; L9-5: fifth day after re-watering following nine-day drought stress; and L9-10: tenth day after re-watering following nine-day drought stress. Changes in the ABA content in 2015 (A
and B); changes in the GA content in 2015 (C and D). In the columns, different letters indicate significant differences at the 0.05 probability level.
4.2. Close correlation between cotton growth compensation effects and ABA re-watering during the flowering and boll-forming stages in Xinjiang,
and GA in roots after re-watering which was likely caused by climate differences (Luo et al., 2013).
GA, as a hormone to promote plant growth, can promote cell
When subjected to drought stress, the root system first senses and elongation and growth. According to their physiological functions, GA
changes its physiology to resist drought stress. The morphological levels are reduced under drought stress, improving drought resilience of
characteristics of the roots change in correspondence with the changes plants by reducing plant growth rate and reducing plant energy con-
in physiology. Our finding showed that soluble sugar, proline, SOD, sumption, and increased after re-watering. The increments of GA were
POD, and ABA exhibited increasing trends, while GA and CAT de- also higher under the moderate drought stress treatments than under
creased under the drought stress, which is similar to the findings of the severe drought stress (Luo et al., 2013; Yan et al., 2012). Wang et al.
many previous studies (Jiang and Huang, 2001; Türkan et al., 2005; (2012) and Albacete et al. (2014) also demonstrated that GA could
Deeba et al., 2012; Sekmen et al., 2014; Shan et al., 2015; Devnarain improve the adversity resistance abilities of plants. We found that, after
et al., 2016; Wang et al., 2016b). After re-watering, all the physiological re-watering, the GA content of the roots increased and was higher than
indices recovered. However, the intensity of the compensation effects the normal levels under the three and six-day 60% SRWC and 45%
varied. Through our analysis, we speculate there are three physiological SRWC treatments, which resulted in a large compensation effect.
indicators (ABA, GA, and CAT) that may be closely related to com- However, the GA content was still significantly lower than the normal
pensation. levels under the nine-day 60% SRWC and 45% SRWC drought treat-
It is well known that endogenous plant hormones are important ments.
signaling substances that regulate plant responses under stress. Plants After re-watering, the ABA content was reduced, relieving the in-
regulate the metabolism to adapt to or withstand stress by changing hibition of cotton roots growth, and GA content increased, promoting
various endogenous hormones. Previous studies have proven that the the root growth and making up for the damage caused by the drought.
increased ABA content under drought stress leads to adjustments in the We speculated that the growth of the roots and the final cotton yield
pore size, the protection of the structure and function of cell membrane, were improved under the mutual regulation of ABA and GA, providing
the inhibition of plant growth, and a reduction in the metabolic rate, the compensation effect. Simultaneously, the osmotic regulation and
thereby improving the drought resistance of plants (Zhang et al., 2006; antioxidant enzymes were able to maintain the plant cell pressure and
Kondo et al., 2012; Kowitcharoen et al., 2015; Wang et al., 2016a; Lv eliminate ROS to protect the cells and provide the material basis and
et al., 2017). In this study, we focused on measuring the change in ABA energy for root growth (Fig. 8). CAT is an important antioxidant en-
and its relationship to root compensation after re-watering. After re- zyme in the plant system that eliminates the excess H2O2 produced by
watering, the ABA content decreased and was even lower than that of the action of the SOD, slowing plant peroxidation (Ozkur et al., 2009).
the controls under the three and six-day 60% SRWC and 45% SRWC However, the CAT activity increased when SOD activity decreased after
treatments, but was still higher than that of the controls under the nine- re-watering following drought stress. Studies have found that the CAT
day 60% SRWC and 45% SRWC treatments. In addition, the root dry activity of the roots decreased under drought stress (Wu et al., 2016;
weights and yields were higher than those of the controls under the Wang et al., 2016b). After re-watering, the CAT activity increased and
three and six-day 60% SRWC and 45% SRWC treatments, but lower was higher than that of the controls under the three and six-day 60%
than those of the controls under the nine-day 60% SRWC and 45% SRWC and 45% SRWC treatments. In addition, the yields of cotton were
SRWC droughts. These results suggest that ABA improvd the drought higher than those of the controls under the same treatments. However,
resistance of cotton and was beneficial to the compensation effect. The after re-watering, the CAT activity did not return to normal levels under
ABA contents of the cotton roots did not decrease on the sixth day after the nine day 60% SRWC and the 45% SRWC drought treatments, thus
36
J. Niu et al. Journal of Plant Physiology 224–225 (2018) 30–48
Fig. 8. Response of cotton roots and yield to drought stress and re-watering.
leading to significantly lower values than those of the controls. This (CCRI-45) was stronger than that of the drought-sensitive cultivar
finding shows that a high CAT activity may improve the root growth (CCRI-60), showing that the compensation ability varies in cultivars. In
and final yield. Nevertheless, the above conclusion still requires further addition, the compensation conditions were different for different
study to improve our understanding of the cotton compensation me- varieties and climates; therefore, the compensation effect mechanisms
chanism. of cotton require further investigation. This conclusion has important
significance for maximizing limited water resources and promoting
5. Conclusions cotton cultivation in arid regions.
This study found that cotton root growth could be stimulated by Funding
moderate drought stress during the seedling stage, and flowering and
boll-forming stage (Appendix A), which results in the promotion of root This work was supported by Special Fund for Agro-scientific
growth that in turn prevents yield reductions or even leads to increased Research in the Public Interest (201503117).
yields. However, the yields were significantly reduced by long-duration
droughts. An analysis of the physiological indices, root dry weight, and Acknowledgments
yield showed that ABA, GA, and CAT play an important role in the
compensation effect, and the physiological metabolism and growth of We gratefully acknowledge the help of the teachers and workers
the roots were promoted by interactions among these factors. from the experimental station at the Institute of Cotton Research of the
Additionally, the compensation ability of the drought-resistant cultivar Chinese Academy of Agricultural Sciences.
Appendix A
Table A1
Chemical properties of the soil used for the experiments in 2014 and 2015.
37
Table A2
Air temperature, total duration of sunshine and rainfall, and mean relative humidity at the experimental site during May to October in 2014 and 2015 in the Henan Anyang.
J. Niu et al.
Year
2014 2015
Month MDT (°C) MDTmax (°C) MDTmin (°C) Accumulated Sunshine Mean relative Total MDT (°C) MDTmax (°C) MDTmin (°C) Accumulated Sunshine Mean relative Total
temperature (°C) hours (h) humidity (%) rainfall temperature (°C) hours (h) humidity (%) rainfall
(mm) (mm)
May 22.78 30.03 15.33 691.31 273.34 61.15 31.80 20.71 27.17 14.50 617.54 239.90 27.51 59.70
June 25.99 32.53 20.23 779.65 217.15 58.66 37.20 26.06 32.62 19.66 781.69 193.55 17.45 19.90
July 26.87 33.34 21.77 832.90 223.40 14.24 129.40 27.02 33.65 21.50 837.76 221.16 12.94 72.40
August 25.10 31.45 20.21 778.21 215.30 4.55 46.10 25.86 32.24 20.87 801.53 193.81 25.04 29.00
September 20.61 26.50 16.05 590.09 121.98 15.94 156.10 21.13 27.61 15.71 633.87 176.91 4.98 17.20
October 16.74 23.43 11.25 436.87 158.79 26.57 4.30 15.68 22.91 8.94 333.11 176.18 0.37 18.20
Mean 23.02 29.55 17.47 684.84 201.66 30.19 67.48 22.74 29.37 16.86 667.58 200.25 14.72 36.07
MDT, MDTmin, and MDTmax stand for mean daily temperature, mean daily minimum temperature and mean daily maximum temperature, respectively. Accumulated temperature were calculated from maximum and minimum temperatures as
∑[(max. temp. + min. temp.)/2–15 °C].
38
Table A3
Changes in the cotton yield and yield composition under drought stress after re-watering during the seedling stage in 2014.
Varieties
CCRI-45 CCRI-60
Treatment Boll number per plant Boll weight (g) Lint (%) Lint cotton yield (kg Hm−2) Boll number per plant Boll weight (g) Lint (%) Lint cotton yield (kg Hm−2)
Table A4
Changes in the cotton yield and yield composition under drought stress after re-watering during the flowering and boll-forming stage in 2014 and 2015.
Year
2014 2015
Varieties Treatment Boll number per Boll weight Lint (%) Lint cotton yield Boll number per Boll weight Lint (%) Lint cotton yield
plant (g) (kg Hm−2) plant (g) (kg Hm−2)
Note: CK: SRWC (75 ± 5)%; D1: SRWC (60 ± 5)%; D2: SRWC (45 ± 5)%; L3: drought stress for three days; L6: drought stress for six days; and L9: drought stress for nine days. In the
columns, different letters indicate significant differences at the 0.05 probability level.
Table A5
Changes in the final agronomic traits of cotton under drought stress after re-watering during the seedling stage in 2014.
Varieties
CCRI-45 CCRI-60
Treatment Height (cm) Fruiting branch nodes Fruiting positions Shedding rate Height (cm) Fruiting branch nodes Fruiting positions Shedding rate
number number (%) number number (%)
Table A6
Changes in the final agronomic traits of cotton under drought stress after re-watering during the flowering and boll-forming stage in 2014 and 2015.
Year
2014 2015
Varieties Treatment Height (cm) Fruiting branch Fruiting positions Shedding rate Height (cm) Fruiting branch Fruiting positions Shedding rate
nodes number number (%) nodes number number (%)
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Table A7
Changes in the cotton fiber quality under drought stress after re-watering during the seedling stage in 2014.
Varieties
CCRI-45 CCRI-60
Treatment Fiber length Uniformity Micronaire Elongation rate Fiber strength Fiber length Uniformity Micronaire Elongation rate Fiber strength
(mm) index (%) (%) (cN/tex) (mm) index (%) (%) (cN/tex)
CK 29.84ab 84.20a 3.55a 5.70b 32.99a 28.22c 83.13a 3.59bc 5.47a 30.22ab
D1L3 29.68ab 84.90ab 3.85a 5.77b 33.9a 28.34bc 83.27a 3.75bc 5.83a 30.83a
D2L3 30.16a 84.80ab 3.94a 6.00ab 33.23a 29.17a 83.57a 4.32a 5.87a 30.61a
D1L6 29.93ab 85.37a 4.01a 6.00ab 33.47a 28.73b 83.48a 4.04ab 5.73a 30.67a
D2L6 29.86ab 85.20a 3.78a 6.13ab 32.60a 28.39bc 83.13a 3.96ab 5.07a 29.50ab
D1L9 29.69ab 84.43ab 3.83a 6.53a 31.05b 28.28c 82.49b 3.48c 5.20a 28.46b
D2L9 29.56b 84.03b 3.83a 5.73b 30.60b 28.19c 82.12b 3.65c 4.93a 28.42b
Table A8
Changes in the cotton fiber quality under drought stress after re-watering during the flowering and boll-forming stage in 2014 and 2015.
Year
2014 2015
Varieties Treatment Fiber Uniformity Micronaire Elongation Fiber Fiber Uniformity Micronaire Elongation Fiber
length index (%) rate (%) strength (cN/ length index (%) rate (%) strength (cN/
(mm) tex) (mm) tex)
CCRI-45 CK 30.37b 84.20b 3.81a 5.20b 32.26a 28.33bc 83.27bc 5.47a 6.67a 28.80c
D1L3 30.50ab 84.67ab 3.91a 5.27b 32.26a 28.77bc 84.77ab 5.47a 6.67a 28.93bc
D2L3 30.84ab 84.83ab 4.03a 5.73ab 32.41a 29.63ab 85.13ab 5.03b 6.63a 30.30ab
D1L6 31.27a 85.00ab 4.12a 5.40ab 32.57a 29.77ab 86.23a 5.70a 6.70a 30.70a
D2L6 30.38b 85.73a 4.17a 6.53a 32.31a 30.23a 86.23a 5.37ab 6.63a 31.70a
D1L9 30.11bc 84.18b 4.16a 5.20b 32.31a 27.23cd 82.57cd 5.43a 6.63a 27.60cd
D2L9 29.59c 82.83c 3.86a 5.33b 32.24a 26.70d 81.00d 5.37ab 6.63a 26.77d
CCRI-60 CK 28.34ab 81.67bc 4.00a 4.77ab 29.37a 28.00ab 82.17bc 5.70ab 6.60a 27.63ab
D1L3 28.52ab 82.00abc 4.08a 5.03ab 29.52a 28.50ab 83.60ab 5.50ab 6.60a 28.87a
D2L3 28.61ab 82.63ab 4.13a 4.90b 29.73a 28.53ab 84.53a 5.60ab 6.57a 28.80a
D1L6 28.92a 83.00a 4.23a 5.33a 29.56a 29.17a 84.73a 5.33b 6.60a 29.30a
D2L6 29.06a 82.53abc 4.16a 5.13ab 29.55a 29.47a 83.27ab 5.67ab 6.60a 27.57ab
D1L9 28.06ab 81.13bc 3.89a 5.17ab 29.23a 27.03bc 80.73bc 5.90a 6.57a 25.97bc
D2L9 27.47b 80.70c 3.78a 5.13ab 29.22a 26.03c 80.30c 5.67ab 6.53a 24.90c
Fig. A1. The relative water content of soil in 2014 and 2015.
Note: CK: regular irrigation; D1: soil relative water content of 60% ± 5%; D2: soil relative water content of 45% ± 5%. L3: drought for three days; L6: drought for six days; and L9:
drought for nine days. The relative water content of the soil during the seedling stage in 2014 and 2015 (A and C), the relative water content of the soil during the flowering and boll-
forming stage in 2014 and 2015 (B and D).
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Fig. A2. Changes in the cotton root dry weight under drought stress and re-watering during the seedling stage in 2014.
Note: L3: drought stress for three days; L3-5: fifth day after re-watering following three-day drought stress; L3-10: tenth day after re-watering following three-day drought stress; L6:
drought stress for six days; L6-5: fifth day after re-watering following six-day drought stress; L6-10: tenth day after re-watering following six-day drought stress; L9: drought stress for nine
days; L9-5: fifth day after re-watering following nine-day drought stress; and L9-10: tenth day after re-watering following nine-day drought stress. The changes in root dry weights of the
drought-resistant cotton variety CCRI-45 in 2014 (A), the changes in root dry weights of the drought-sensitive cotton variety CCRI-60 in 2014 (B). In the columns, different letters indicate
significant differences at the 0.05 probability level. The same applies below.
Fig. A3. Changes in the cotton root dry weight under drought stress and re-watering during the flowering and boll-forming stage in 2014 and 2015.
Note: The changes in root dry weights of the drought-resistant cotton variety CCRI-45 in 2014 and 2015: A and B, the changes in root dry weights of the drought-sensitive cotton variety
CCRI-60 in 2014 and 2015: C and D. In the columns, different letters indicate significant differences at the 0.05 probability level. The same applies below.
Fig. A4. Relationship between the increased percentages of yield and root dry weight under drought stress after re-watering during the seedling stage in 2014.
Note: * and ** indicate significant differences at the 0.05 and 0.01 probability levels, respectively (n = 6, R0.05 = 0.811, and R0.01 = 0.917).
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Fig. A5. Relationship between the increased percentages of yield and root dry weight under drought stress after re-watering during the flowering and boll-forming stage in 2014 and
2015.
Fig. A6. Changes in the soluble sugar and proline content in cotton roots under drought stress and re-watering during the seedling stage in 2014.
Note: Changes in the soluble sugar content in 2015: A and B; changes in the proline content in 2015: C and D. In the columns, different letters indicate significant differences at the 0.05
probability level.
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Fig. A7. Changes in the soluble sugar content in cotton roots under drought stress and re-watering during the flowering and boll-forming stage in 2014 and 2015.
Fig. A8. Changes in the proline content in cotton roots under drought stress and re-watering during the flowering and boll-forming stage in 2014 and 2015.
Fig. A9. Changes in the soluble protein content in cotton roots under drought stress and re-watering during the seedling stage in 2014.
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Fig. A10. Changes in the soluble protein content in cotton roots under drought stress and re-watering during the flowering and boll-forming stage in 2014 and 2015.
Fig. A11. Changes in the SOD and POD activity in cotton root under drought stress and re-watering during the seedling stage in 2014.
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Fig. A12. Changes in the SOD activity in cotton root under drought stress and re-watering during the flowering and boll-forming stage in 2014 and 2015.
Fig. A13. Changes in the POD activity in cotton roots under drought stress and re-watering during the flowering and boll-forming stage in 2014 and 2015.
Fig. A14. Changes in the CAT activity in cotton roots under drought stress and re-watering during the seedling stage in 2014.
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Fig. A15. Changes in the CAT activity in cotton roots under drought stress and re-watering during the flowering and boll-forming stage in 2014 and 2015.
Fig. A16. Changes in the ABA and GA content in cotton root under drought stress and re-watering during the seedling stage in 2014.
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Fig. A17. Changes in the ABA content in cotton root under drought stress and re-watering during the flowering and boll-forming stage in 2014 and 2015.
Fig. A18. Changes in the GA content in cotton roots under drought stress and re-watering during the flowering and boll-forming stage in 2014 and 2015.
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