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ELSEVIER
Responses in gas exchange and water status between drought-tolerant and -susceptible soybean genotypes with ABA application
Md. Mokter Hossain, Hon-Ming Lam, Jianhua Zhang*
School of Life Sciences and Center for Soybean Research of the State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin, Hong Kong, China
ARTICLEINFO ABSTRACT
Article history:
Received 5 June 2015
Received in revised form
12 August 2015
Accepted 3 September 2015
Available online 14 October 2015
Keywords: Drought stress Exogenous ABA Leaf relative water content Stomatal conductance Soybean genotypes
The purpose of this study was to investigate the physiological responses of drought-tolerant and drought-susceptible soybean genotypes to exogenous abscisic acid (ABA) application during progressive soil drying at seedling stages. Five-day old soybean seedlings were transplanted into PVC tubes filled with soil mixture. Seedlings were watered daily with similar water volumes until second trifoliate leaves emerged, and thereafter soil drying with or without exogenous ABA application was imposed. Half of the seedlings of each genotype were left for regular watering as control plants. Soil water status declined significantly over seven days of withholding water supply for both genotypes. Leaf expansion rate, stomatal conductance (gs), leaf water potential (i^w), and relative water content of leaves (%RWC) declined significantly under soil drying as well as soil drying with ABA application, compared to their values for well-watered soybean genotypes. However, a drought-tolerant genotype (C12) responded more rapidly than a drought-susceptible genotype (C08) after imposition of soil drying and soil drying with exogenous ABA. In addition, application of exogenous ABA to water-restricted soybeans resulted in higher %RWC and i/>w in the drought-tolerant than in the drought-susceptible genotype. Compared to the drought-susceptible genotype, the drought-tolerant genotype was more responsive to exogenous ABA application, resulting in a higher root-to-shoot ratio.
© 2015 Crop Science Society of China and Institute of Crop Science, CAAS. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
1. Introduction
Drought stress is a key environmental constraint to productivity in world agriculture. Water stress impairs numerous physiological as well as biochemical processes of crop plants. Photosynthesis is a
major process affected by water deficit, via decreased CO2 diffusion to the chloroplast and metabolic constraints [1]. Water-restricted plants show immediate low stomatal conductance without alteration of shoot water potential. The reason for this response is that leaf stomata cannot open because plants can
Abbreviations: ABA, abscisic acid; gs, stomatal conductance; LA, leaf area; LL, leaf length; LW, leaf width; RWC, relative water content; leaf water potential. * Corresponding author. Tel.: +852 3943 6288; fax: +852 2603 6382. E-mail address: jhzhang@cuhk.edu.hk (J. Zhang).
Peer review under responsibility of Crop Science Society of China and Institute of Crop Science, CAAS.
http://dx.doi.org/10.1016/j.cj.2015.09.001
2214-5141/© 2015 Crop Science Society of China and Institute of Crop Science, CAAS. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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sense the availability of water in the soil and regulate stomatal behavior accordingly, whatever the water status of their leaves [2]. The consequences of water stress to crop plants are thus a reduction in leaf expansion rate, accelerated leaf senescence, and reduction in production and partitioning of photo assimilates to the plants.
Drought tolerance is thus a key trait for increasing and stabilizing crop production [3,4]. Abscisic acid (ABA) accumulates in response to low-temperature and water stress [5,6], and is now known to be involved in several developmental processes as well as acclimation to environmental stresses (cold, salt, and drought) [7,8]. ABA is produced in plant roots and transported to leaves via xylem flow under water-limiting conditions [9]. It triggers stomatal closure in response to drought stress, thereby reducing photosynthetic CO2 assimilation [10]. The influence of plant hormones such as ABA in plants under drought stress is thus important in determining physiological responses that may ultimately lead to adaptation to unfavorable environmental conditions [11].
Exogenous ABA application reduced photosynthetic rate, stomatal conductance, and transpiration rate in cotton [12]. Liu et al. [13] found that exogenous ABA application decreased photosynthetic rate and pod set in well-watered soybean plants but that those parameters were increased when ABA was applied to drought-stressed plants. Lam [14] genomically evaluated 31 soybean accessions at the Chinese University of Hong Kong for developing drought-tolerant soybean varieties, and identified promising genotypes in a hydroponic culture system using polyethylene glycol (PEG) and salts. Field performance of two drought-tolerant and susceptible genotypes (C12 and C08) has been partially tested in Dunhuang, China.
Given that drought-stressed plants produce ABA in leaves and regulate their stomata by maintaining higher water status in leaves, we hypothesized that the application of exogenous ABA to leaves of soil drying soybean plants would encourage earlier stomatal closure and reduce water loss from plants, thereby leading to higher relative water content and water potential in leaves. This study was accordingly undertaken to investigate the differences in physiological response to exogenous ABA application of drought-tolerant and drought-susceptible soybean genotypes during progressive soil drying.
2. Materials and methods
2.1. Plant materials and exogenous ABA application
The drought-tolerant Jindou 21 (C12) and drought-susceptible Union (C08) soybean genotypes were used for this study. Seedlings were grown in a plastic tray containing soil mixture (soil and peat moss) in the greenhouse. Five-day old seedlings were transplanted into PVC tubes (50 cm length x 5 cm inner diameter) filled with soil mixture (soil and peat moss in a 1:1 volume ratio, with the addition of NPK at 14:14:14). Fertilizer granules were mixed at 5 g L-1 of soil mixture. Plants were grown under natural sunlight in the greenhouse with average daytime temperature 28 ± 2 °C and relative humidity 60-70%.
Plants were watered daily with similar water volumes until second trifoliate leaves emerged, after which soil drying treatment was imposed. One third of the seedlings of each genotype were kept for regular watering as control plants, another third subjected to soil drying, and the remaining third subjected to soil drying + exogenous ABA treatment. At the time of beginning soil drying, 50 mol L-1 solution of ABA with 0.05% Tween-20 was sprayed on soil drying plants twice daily (at 1000 h and 1400 h) for two days on both adaxial and abaxial surface of leaves and measurement was started 3 h after the first spray.
2.2. Measurement of stomatal conductance
After the onset of soil drying along with spraying of exogenous ABA on leaves, the stomatal conductance (gs) of fully expanded leaves was measured 3 h after ABA application. Thereafter, gs was measured daily with a leaf porometer (Decagon Devices, Inc. USA) until a week of soil drying.
2.3. Measurement of leaf area expansion
Leaf area (LA) was measured with a portable leaf area meter (LI-3100; Li-COR, Inc. USA). After imposition of soil drying followed by application of exogenous ABA newly emerged leaves (center leaflet of second trifoliate leaf) were tagged for measuring LA each day. Leaf length (LL) and width (LW) were measured daily with a measuring ruler and the relationship between the product LL x LW and LA was determined for each genotype from individual leaf measurements of 15 leaves. The regression of LA on LL x LW was fitted as LA = k x LL x LW, where k is the slope of the linear function.
2.4. Measurement of relative water content
Relative water content (%RWC) of fully expanded youngest mature leaves was measured on both soil drying and soil drying + ABA-treated plants 0, 1, 3, and 7 days after imposition of treatments. To minimize solute leakage and cut surface effect, the entire leaf was used. Leaf petioles were carefully detached from plants, fresh weights were recorded, and then kept in water holding plastic tube in a closed container in an atmosphere saturated by means of wet tissue paper around the inner wall of the container. Turgid weight was measured after 24 h and dry weight was measured after oven-drying for 48 h at 65 °C. Leaf relative water content was calculated by the following equation:
Relative water content (%RWC) =
Fresh weight-dry weight Turgid weight-dry weight
2.5. Measurement of leaf water potential
Leaf water potential (t^w) was measured at 0,1, 3, and 7 days after soil drying and soil drying + exogenous ABA application using a pressure chamber (Soilmoisture Equipment Corp, Santa Barbara, California, USA). The leaf petiole was sealed into a pressure chamber and the chamber was gradually pressurized until the meniscus of the xylem sap become
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50 40 30 20 10 0
C12 0 day
C12 after 7 days
C08 0 day
C08 after 7 days
Fig. 1 - Soil water content (%) at the day of imposition of soil drying and soil drying + ABA application (day 0) and after 7 days of soil drying for drought-tolerant (C12) and -susceptible (C08) soybean genotypes. Values of points are means ± standard deviation (SD) (n = 3).
visible at the cut surface, at which time the pressure reading was recorded.
2.8. Measurement of shoot and root weight and length, root-to-shoot ratio, and soil water content
After 7 days of progressive soil drying as well as soil drying + application of exogenous ABA, shoot and root fresh weight and length in drought-tolerant and drought-susceptible soybean genotypes were measured. Root-to-shoot ratio was determined after oven drying (65 °C for 48 h) of roots and shoots. Soil water content was determined at the beginning of soil drying (day 0) and after 7 days of drying. Soil was collected at a depth of 10-15 cm in the soil profile and oven dried at 105 °C for 72 h, and water content was determined and expressed as a percentage on an oven-dry weight basis.
2.9. Statistical analysis
Data were subjected to one-way analysis of variance (ANOVA) followed by post hoc multiple comparisons using Tukey test to identify significant differences between treatments. The results presented are means with standard deviations of three to six replicates. The minimum accepted P-value for significance was 0.05.
2.6. Determination of weight loss of excised ¡eaves
Water loss from detached youngest mature leaves was determined following Okamoto et al. [15]. One hour after application of exogenous ABA, leaves from well-watered and ABA-treated plants were excised with petiole and placed on a sheet of paper for air-drying in the greenhouse. Measurement was performed on a clear, sunny day with 33 ± 1 °C temperature and 55% relative humidity. Weight loss (%) due to water loss from detached leaves was recorded at 10 min intervals with an analytical balance (Shimadzu AUW220D, Shimadzu Corporation, Tokyo, Japan).
2.7. Estimation of stomata on the leaf surface
Stomata on the youngest mature leaves of well-watered plants were counted under a light microscope at 40 x (Nikon Eclipse 80i, Diagnostic Instrument).
3. Results
3.1. Soil water status
Soil water content was monitored during the imposition of treatments as well as after the ending of soil drying for the drought-tolerant and -susceptible soybean genotypes. Soil water content declined after seven days of the experiment (Fig. 1). Soil water contents of C12 and C08 were 36.41% and 37.63% on day 0, falling to 23.48% and 23.57%, respectively at the end of the experiment (Fig. 1).
3.2. Influence of exogenous ABA on leaf expansion rate of soybean
Leaf expansion rates of soybean genotypes were measured daily after imposition of soil drying with or without exogenous
^ 7 to
Time after application of treatments (day)
Fig. 2 - Leaf expansion rate of drought-tolerant (C12) and -susceptible (C08) soybean genotypes after imposition of treatments. Empty black circles and black triangle represent soil drying (sd), soil drying + exogenous ABA application (sd + ABA), and well-watered (ww) plants, respectively. Each data point represents mean ± SD (n = 5).
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Fig. 3 - Stomatal conductance of drought-tolerant (C12) and susceptible (C08) soybean genotypes after imposition of treatments. Empty, black circles and black triangle represents soil drying (sd), soil drying + exogenous ABA application (sd + ABA) and well-watered (ww) plants, respectively. Each data point represents mean ± SD (n = 5).
ABA application. Under soil drying with exogenous ABA application, leaf expansion rates declined in all genotypes (Fig. 2). Compared with the drought-susceptible genotype (C08), the drought-tolerant genotype (C12) showed a more rapid reduction in leaf expansion rate after exogenous ABA application (Fig. 2).
3.3. Influence of exogenous ABA on leaf stomatal conductance of soybean
Stomatal conductance (gs) of soybean genotypes was measured 3 h after imposition of soil drying with or without application of exogenous ABA, followed by daily measurement. Stomatal conductance of leaves was markedly affected by application of exogenous ABA (Fig. 3). A rapid reduction of gs was observed after 3 h in the drought-tolerant genotype (C12) compared to the drought-susceptible genotype (C08) (Fig. 3).
declined, but soil drying with application of ABA led to much slower reduction of %RWC in both soybean genotypes (Fig. 4). The reduction tendency of %RWC of the drought-susceptible genotype (C08) was significantly faster from the initiation of soil drying and reached 65.7% after seven days, whereas that of the drought-tolerant genotype (C12) reached 78.5%. Exogenous ABA application may have induced stomatal closure in plants subjected to soil drying, reducing water loss through stomata and thereby preserving higher %RWC in leaves.
Exogenous application of ABA not only induced stomatal closure in leaves but also influenced leaf water potential (t^w) of soybean genotypes. The of the drought-susceptible genotype fell sharply immediately after water was withheld and reached - 2.3 MPa after seven days, while that of the drought-tolerant genotype reached -1.86 MPa (Fig. 5). The influence of exogenous ABA on leaf was pronounced in the tolerant genotype C12.
3.4. Influence of exogenous ABA on %RWC and yw of soybean leaves
3.5. Influence of exogenous ABA on water loss from excised soybean leaves
Percent relative water content (%RWC)) and water potential (t^w) of soybean leaves were determined before and after imposition of treatments. As soil drying progressed, %RWC of leaves
Water losses (in %) from detached leaves of well-watered and exogenous ABA applied plants were determined. Fully expanded leaves were excised 1 h after ABA application along with
100 95 90 85 80 75 70 65 60
-•— sd+ABA —A— ww
100 95 90 85 80 75 70 65 60
Time after imposition of treatments (day)
Fig. 4 - Relative water content (%RWC) of leaves of drought-tolerant (C12) and susceptible (C08) soybean genotypes after imposition of treatments. Empty, black circles and black triangle represents soil drying (sd), soil drying + exogenous ABA application (sd + ABA) and well-watered (ww) plants, respectively. Each data point represents mean ± SD (n = 4).
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Time after imposition of treatments (day)
Fig. 5 - Leaf water potential of drought-tolerant (C12) and susceptible (C08) soybean genotypes after imposition of treatments. Empty, black circles and black triangle represents soil drying (sd), soil drying + exogenous ABA application (sd + ABA) and well-watered (ww) plants, respectively. Each data point represents mean ± SD (n = 4).
well-watered leaves and left in the greenhouse for sun drying. Percent weight loss due to water loss from leaves was recorded by weighing at 10 min intervals. Application of exogenous ABA inhibited water loss principally through leaf stomata, in comparison with well-watered leaves (Fig. 6). Leaf water retention was pronounced 10 min after excision in the drought-tolerant
genotype (C12) whereas the drought-susceptible genotype (C08) showed low water retention ability, such that % water loss was always higher in C08 even after application of ABA (Fig. 6). Given that leaf stomata may have influenced % water loss from leaves of soybean genotypes, the stomata per square cm of leaf surface area were counted for both soybean genotypes under a confocal
Time after detached leaves (min)
Fig. 6 - Water loss (%) from well-watered (WW) and exogenous ABA applied leaves of drought-tolerant (C12) and susceptible (C08) soybean genotypes. Leaves were excised 1 h after application of ABA. Value of each data point represents a single leaf measurement.
° 1600 cö
□ Adaxial DÄbaxial
C12 C08
Soybean genotype
Fig. 7 - Number of stomata on adaxial and abaxial surface of leaves of well-watered drought-tolerant (C12) and susceptible (C08) soybean genotypes. Value of each point is mean ± SD (n = 5).
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45 40 35 30 25 20 15
t 2.0 en
1.5 1.0 0.5 0.0
□ sd msd+ABA
0.35 0.30
'w 0.25
o o oc
0.20 0.15 0.10 0.05 0.00
o o 20
o o oc
2.5 2.0 1.5 1.0 0.5 0.0
C12 C08
Soybean genotype
Fig. 8 - Shoot length (A), root length (B), shoot fresh weight (C), root fresh weight (D), and root-to-shoot ratio (E) of drought-tolerant (C12) and susceptible (C08) soybean genotypes after 7 days of soil drying with exogenous ABA application. Value of each point is mean ± SD (n = 7).
microscope. The presence of stomata on leaves was markedly different on abaxial and adaxial surfaces of both soybean genotypes but no significant difference was found between the genotypes (Fig. 7).
3.6. Influence of exogenous ABA on root and shoot growth of soybean
To determine whether exogenous ABA affects root or shoot growth of soybean genotypes under water restriction during growth, root and shoot fresh weight and length and root-to-shoot ratio were measured at the end of the experiment. As a growth-retardant chemical, ABA may affect shoot and root weight and length and root-to-shoot ratio in drought-tolerant (C12) and drought-susceptible (C08) soybean genotypes. Shoot and root lengths and fresh weight of the drought-tolerant genotype
were reduced by soil drying in comparison with the drought-susceptible genotype, but not significantly (Fig. 8A, B, C). Root fresh weight of both genotypes declined, but that of the drought-susceptible genotype was significantly reduced by water restriction for seven days (Fig. 8D). The drought-tolerant soybean genotype (C12) showed a higher root-to-shoot ratio than the susceptible genotype (C08) under restricted soil water with application of exogenous ABA (Fig. 8E).
4. Discussion
The responses of tolerant and susceptible soybean genotypes to soil drying and to soil drying with ABA application were different. The drought-tolerant genotype responded more rapidly than the drought-susceptible one when water restriction along with
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exogenous ABA was imposed on the soybean seedlings. Water-restricted plants showed immediate low stomatal conductance while retaining higher leaf water potential. The possible reason behind these events is that leaf stomata could not open, because plants sense the availability of water in the soil and regulate stomatal behavior accordingly, whatever the water status of their leaves [2]. ABA has been reported to reduce stomatal conductance, possibly reducing photosynthesis in plants but improving water status in leaves [16,17]. In the present experiment, leaf stomatal conductance (gs) of the drought-tolerant soybean genotype declined within 3 h of exogenous ABA application followed by withholding of water to the soybean seedlings. Kim and Iersel [18] reported that ABA drenches caused stomatal closure in salvia (Salvia splendens Sellow ex Schult.) within 3 h of application. In the present experiment, the tendency of water loss from the detached leaves of ABA-treated seedlings indicated that exogenous ABA can act on stomata even 3 h after application, so that gs declined within this short period. Although progressive soil drying triggered the reduction of leaf water status and %RWC, these tendencies were different in the tolerant and susceptible genotypes. The reduction of gs in leaves was regulated by % relative water content of leaves as well as leaf water potential in the drought-tolerant genotype. Thus, the decline of %RWC and water potential were markedly slower in leaves of the drought-tolerant genotype than in those of the drought-susceptible genotype. Hossain et al. [19] proposed that drought-tolerant soybean genotypes maintained higher instantaneous water use efficiency (WUEi), % relative water content, water potential (t^w), and turgor potential (t^p) during progressive soil drying and subsequent rewetting than did susceptible genotypes. Application of exogenous ABA inhibited water loss from excised leaves by inducing stomatal closure. In the present study, weight loss of excised leaves due to water loss was slower in the drought-tolerant genotype. However, ABA accumulation in plants is regulated by drought stress, which induces stomatal closure and restricts growth [20]. The results of our study suggest that exogenous ABA application induces stomatal closure, thereby helping to retain higher %RWC, leaf water potential, and restrict in weight loss from excised leaves through water loss, and that these responses differ between tolerant and susceptible soybean genotypes.
Acknowledgments
We thank Fuk-Ling Wong, Dr. Weifeng Xu and Dr. Ken Lau for technical support. This study was supported by the Hong Kong RGC Collaborative Research Fund (CUHK3/CRF/11G) to Prof. Hon-Ming Lam and Prof. Jianhua Zhang.
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