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Published online 8 September 2006
Published in Crop Sci 46:2041-2046 (2006)
© 2006 Crop Science Society of America
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GENOMICS, MOLECULAR GENETICS & BIOTECHNOLOGY

Differential Responses of the Cultivated and Wild Species of Soybean to Dehydration Stress

Yanyun Chena, Pengyin Chenb,* and Benildo G. de los Reyesc

a Dep. of Crop, Soil, and Environmental Sciences, Univ. of Arkansas, Fayetteville, AR 72701, current address: Dep. of Food Science, Purdue Univ., West Lafayette, IN 47906
b Dep. of Crop, Soil, and Environmental Sciences, Univ. of Arkansas, Fayetteville, AR 72701
c Dep. of Biological Sciences, Univ. of Maine, Orono, ME 04469

* Corresponding author (pchen{at}uark.edu)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
The Dehydration Responsive Element-Binding protein/C-repeat Binding Factor (DREB/CBF) plays important roles in regulating physiological processes and downstream gene expression for drought stress in Arabidopsis thaliana, rice, and wheat. ‘Essex’ soybean [Glycine max (L.) Merr.] was identified as tolerant and a wild soybean PI 407155 (Glycine soja Sieb. & Zucc.) as more tolerant to dehydration stress in a greenhouse screen. In this study, we cloned and characterized the Glycine DREB1 (GlyDREB1) from the dehydration-induced PI 407155 and Essex using a semi-quantitative RT-PCR, rapid amplification of cDNA ends (RACE), and northern blot. We also investigated the physiological characteristics including biomass accumulation, moisture content, and electrolyte leakage for both soybean genotypes under dehydration stress. Analysis of homologous GlyDREB1 genes from PI 407155 and Essex indicated differences in both the timing and strength of expression under dehydration stress. The GlyDREB1 in PI 407155 was rapidly induced in 1 h of dehydration shock and the transcription level was much higher than that in Essex. The root system of PI 407155 maintained higher moisture content and biomass accumulation than that of Essex on the 15 d without irrigation. The percentage electrolyte leakage in Essex was almost twice that in PI 407155 under 5 d no irrigation treatment. Both molecular and physiological studies indicated that PI 407155 had higher level of tolerance to dehydration stress than Essex, therefore providing a new potential soybean genome for developing dehydration stress cultivars.

Abbreviations: DREB/CBF, drought responsive element binding protein/C-repeat binding factor • ABA, abscisic acid • cor, cold-regulated • FW, fresh weight • DW, dry weight • EL, electrolyte leakage • LSD, least significant difference • ESTs, Expressed Sequence Tags • DRE/CRT, Drought Response Element or C-Repeat


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
THE WILD species gene pool is always considered a rich source of genes for the improvement of resistance/tolerance of cultivated species to biotic and abiotic stresses (Duncan, 1994). Like most important crop species, soybean (Glycine max) is very sensitive to suboptimal moisture conditions during the vegetative and reproductive stages. Due to its geographic origin and its ability to withstand prolonged duration of water deficit, it has been hypothesized that the closely related wild species Glycine soja is a potential source of genes for the improvement of drought tolerance of the cultivated soybean (Bond and Gresshoff, 1993). However, despite this common notion, the genetic and physiological evidence in support of such hypothesis remains lacking. In an effort to establish a proof of concept regarding the potential utility of Glycine soja for drought tolerance breeding, we conducted preliminary investigations of some physiological and molecular aspects that have been previously shown to be associated with stress tolerance in other crop species and genetic models. In the physiological study, we investigated the differential responses of Glycine max and Glycine soja to water deficit by measuring the differences in biomass accumulation, moisture content, and cell membrane injury, i.e., electrolyte leakage (Bray, 1997).

A cDNA for Drought Responsive Element Binding protein/C-repeat Binding Factor (DREB/CBF) was initially isolated from dehydrated Arabidopsis (Stockinger et al., 1997). The expression of DREB/CBF gene is also activated by other environmental factors, such as low temperature, salinity, and abscisic acid (ABA). A number of DRE-related motifs (ACCGACA) were reported in the promoter regions of many stress-inducible genes such as kin1, cor6.6, and cor47/rd17 (Yamaguchi-Shinozaki and Shinozaki, 1994; Wang et al., 1995). Because of the important regulatory role of the DREB/CBF in drought, cold, and salinity stress responses, three CBF genes and five DREBs have been isolated from dehydrated and low temperature-treated Arabidopsis plants (Liu et al., 1998; Gilmour et al., 1998). Jaglo-Ottosen et al. (1998) found that overexpressing CBF1 in transgenic Arabidopsis with cauliflower mosaic virus (CaMV) 35S promoter not only increased cold-regulated (cor) gene expressions but also enhanced their freezing tolerance. Five DREB homologs have been cloned from Oryza sativa L. rice seedlings (Dubouzet et al., 2003) in response to low temperature. The DREB/CBF-like genes have also been characterized from other annual plants including barley, rye, prunus, and tomato under different abiotic stresses (Jaglo et al., 2001; Kitashiba et al., 2002). However, there is no report about DREB/CBF homolog from soybean under environmental stress. Considering the important function of DREB/CBF responding to environmental stress in other plants, it was hypothesized that the difference in timing of expression for this gene may be a way to differentiate the stress response mechanisms of wild and cultivated soybeans. Therefore, we also examined the expression patterns of DREB between G. soja and G. max under dehydration stress.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Physiological Analysis
Soybean cv. Essex and the wild species G. soja PI 407155 were used in this study. Seeds of both genotypes were planted in the same tray (100 cm x 51 cm x 18 cm) containing the Redi-Earth commercial potting mix (Scotts-Sierra Horticultural Products Co., Marysville, OH). Plants were grown in a greenhouse maintained at 22 to 25°C with 12-h photoperiod. At the V3 stage, dehydration stress was imposed by withholding water for consecutive 5, 10, 15 d, while control plants of both genotypes in a separate tray were watered daily to field capacity. At the correct time point of 5, 10, or 15 d without irrigation, seedlings were gently pulled out of soil, rinsed with tap water, and blot-dried with paper towel. The plant was separated from the soil surface into two parts: root and shoot (stems and leaves). Fresh weight (FW) was immediately measured for both plant parts. Plants were then placed in a 75°C oven for 72 h to obtain dry weight (DW). The percentage moisture content in sampled plant tissue was determined by the difference between FW and DW divided by FW and multiplied by 100. The average of ten seedlings was used for each time point of treatment. The difference in moisture content of any two time points represented the water loss for that period of dehydration treatment.

The biomass accumulation was calculated by the difference between the DW before and after dehydration stress and then divided by the DW before dehydration stress, which also served as an indication for the plant growth during the period of dehydration stress. The electrolyte leakage (EL) analysis was also performed on the well-watered and dehydrated seedlings according to Morsy et al. (2005). Briefly, a single leaf detached from the control and dehydrated seedlings was submerged in 30 mL fresh deionized water for 6 h and electrical conductivity (EC) of the water was subsequently measured using a digital conductivity meter (VWR, Houston, TX). Total electrolyte from the tissue samples was determined after freezing at –80°C overnight. The percentage electrolyte leakage (%EL) was calculated by EC ratio before and after freezing multiplied by 100. Ten seedlings were used in determining %EL for each time point of the dehydration treatment.

The means of moisture content, biomass accumulation, and %EL values were compared and separated using the least significant difference (LSD) test at 5% level. All the data were analyzed using JMP5.1 and SAS 8.02 (SAS Institute, 2001, Cary, NC).

Molecular Analysis
Total RNA was isolated from leaf tissues collected at different time points of dehydration shock (1, 2, 4, 8, 12, 24, 36h) with the RNEasy Plant kit (Qiagen, Hilden, Germany), where the dehydration shock was performed by gently pulling the V3 stage seedlings out of the soil, carefully removing soil from the root, and air-drying the whole seedling on the greenhouse bench for the different time periods defined above. The polyA+ RNA was purified from the total RNA samples with the PolyATract kit (Promega, Madison, WI). Nested primers specific to the soybean DREB1 homolog was designed based on Expressed Sequence Tags (ESTs) obtained from the GenBank (AW308782, AW278562, BE556211). The temporal expression of Glycine DREB1 (GlyDREB1) was investigated by a two-step semi-quantitative RT-PCR with the Retroscript kit (Ambion). Total RNA (1 ug) was reverse-transcribed using oligo-dT primer and MMLV-RT (100 units) in the presence of 10 units RNase inhibitor. Equal amounts of the first strand cDNA were used as template for gene-specific PCR with the following primers: (i) GlyDREB1: 5'-CCCTGAGCTCTCATCTTCCTTGG-3' (Forward), 5'-AAAGTCCCCAGCCAAATCCT-3' (Reverse); (ii) Actin: 5'-GAGGAGCGGGAGGAG GAAATG-3' (Forward), 5'-CATCTCGGT TGG GTCTGTTG-3' (Reverse). The gene-specific fragment amplification was performed using 1 unit of SuperTaq Plus (Ambion, Austin, TX) for 25 cycles at the following conditions: denaturing at 94°C for 30 s, annealing at 55°C for 30 s, and extension at 72°C for 1 min. The resulting RT-PCR fragments were cloned in pCR2.1 (Invitrogen, Carlsbad, CA) and sequenced for further confirmation of specificity. The full-length cDNA sequence of the GlyDREB1 gene was determined by 5' and 3'-rapid amplification of cDNA ends (RACE, Ambion) and used as probes (radioactively-labeled) for northern blot analysis. Briefly, 5 ug of poly-A+ RNA samples from shoot tissues of the control and dehydration-treated plants were blotted on Hybond N+ nylon membrane (Amersham Biosciences, Little Chalfont, UK). The RNA blots were hybridized with the 32P-labeled probes overnight at 42°C in 7 mL ultrasensitive hybridization (ULTRAhybTM) buffer (Ambion, Little Chalfont, UK) and washed according to standard procedures (de los Reyes et al., 2003).


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Soybean is a dehydration-sensitive species requiring optimum water content for seed germination, seedling growth, and plant development. In a pilot experiment, the speed of canopy wilting among eight soybean genotypes was examined after withdrawing irrigation at the V3 stage for continuous 20 d under greenhouse conditions to provide a more quantitative measure of variation in sensitivity to dehydration at early seedling stage. Among the six cultivated soybean genotypes (Essex, ‘Hutcheson’, PI 416937, PI 471938, N92-SH-447, and NTCPR94–5157), Essex exhibited slower wilting than others in the test. However, G. soja accessions PI 407155 showed even slower wilting than Essex after 12-d dehydration treatment (Fig. 1 ). These preliminary observations suggested that the wild-type G. soja genotypes are less easily dehydrated than the cultivated soybeans. Essex was shown to have some tolerance to dehydration and relatively high seed yields among soybean cultivars (Smith and Camper, 1973; Vieira et al., 1992). Based on the phenotypic response to dehydration stress in our greenhouse experiment, Essex and PI 407155 were selected to investigate their physiological and molecular characteristics in response to water deficits in this study.


Figure 1
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  		Fig. 1. The phenotypic response of Essex and PI 407155 to 12 d of dehydration stress, where Essex showed wilting symptoms as compared to PI 407155 maintained in the same pot.

 
Growth Comparison and Tissue Moisture Content
The seedlings of Essex and PI 407155 continued to grow within the first 5 d of dehydration stress as manifested by the developmental progression from V3 to V4 stage. Both genotypes reached V5 stage with little visible signs of wilting after 10 d without irrigation. However, Essex was completely wilted after 15 d without irrigation, whereas PI 407155 remained viable and green based on daily observation. The shoot biomass accumulation also exhibited the similar growth trend as the dehydration stress progressed overtime. During the first 5 d without irrigation, both PI 407155 and Essex accumulated one fold of shoot biomass as compared to the day-0 (starting dehydration stress treatment) DW. During the 10 d of dehydration stress, the biomass accumulation for both genotypes increased by a factor of two as compared to that for day-0 (Fig. 2 ). However, on the 15 d of withholding water, PI 407155 continued to accumulate biomass up to 2.81 times over the day-0 DW, whereas Essex maintained similar biomass level to that of 10 d of dehydration stress, indicating Essex ceased to grow after 10 d of dehydration stress. Based on the physiological assumptions by Hopkins and Huner (2004), the difference in biomass accumulation suggested that PI 407155 had higher level of tolerance to dehydration stress overtime than Essex.


Figure 2
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  		Fig. 2. Shoot and root biomass accumulation of PI 407155 and Essex seedlings during a 15-d period of dehydration treatment. Error bars indicate ± one standard error of the mean. Vertical Bars representing mean values followed by the same letter are not significantly different (P < 0.05 level) for the same part of seedling under different periods of dehydration treatment (5, 10, 15 d).

 
During the 15 d of no irrigation, Essex accumulated root biomass that was equivalent to 1.5, 2.31, and 2.26 times of the day-0 biomass on the 5, 10, 15 d of dehydration stress, respectively, indicating Essex root continued to grow during the first 10 d and ceased to grow thereafter (Fig. 2). However, the PI 407155 root maintained slow biomass accumulation in the first 10 d of dehydration stress (1.25 times compared to the day-0 root biomass), while root biomass accumulation reached the level that tripled the day-0 DW in the third 5-d dehydration stress period. This is probably due to some adaptive mechanisms brought about by stress-induced changes in gene expression. Although not significantly different, PI 407155 exhibited a consistently higher shoot and root biomass accumulation after 15 d of dehydration stress. The higher biomass accumulation in PI 407155 may be related with some stress-induced gene expression in PI 407155, which is consistent to the mechanism observed in Arabidopsis, where cold and dehydration treatments are accompanied by the early expression of genes that contribute to enhance the membrane stability during extended periods of exposure to stress (Artus et al., 1996; Jaglo-Ottosen et al., 1998).

Under dehydration stress, moisture content is a key factor in representing the ability of the plant to hold water for its survival. Therefore, we also inspected the moisture content in both root and shoot under 5, 10, or 15 d without irrigation. During the first 5 d of dehydration stress, both PI 407155 and Essex maintained similar shoot moisture content as compared to that of the well-watered seedlings, probably because the seedlings with dehydration treatment sustained their normal growth by using the remaining water in the soil. In the subsequent 10 and 15 d of dehydration stress, both genotypes significantly lost water in the shoot as compared to the control and 5-d dehydration treatment (Fig. 3 ). The 15-d dehydration stress resulted in over 15% moisture loss in the shoot of both genotypes leading to wilting symptoms in the plant canopy. In addition, the two soybean genotypes showed significantly different ability to hold moisture in the root system under dehydration stress. During the first 5 d of dehydration stress, the roots of both genotypes did not lose any moisture, probably because they could still use the remaining water in the soil for growth. However, after 10 or 15 d of dehydration treatment, both genotypes lost significant moisture in the root system as compared to the control and 5-d dehydration treatment. On the 10th or 15th d of dehydration stress, PI 407155 had significantly higher moisture content than Essex (Fig. 3). PI 407155 seedlings lost about 10% of root moisture content whereas Essex lost over 15% of moisture in the root during the 15-d dehydration stress.


Figure 3
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  		Fig. 3. Shoot and root moisture content of PI 407155 and Essex seedlings during a 15-d period of dehydration treatment. Error bars indicate ± one standard error unit. Vertical Bars representing means values followed by the same letter are not significantly different (P < 0.05 level) for the same part of seedlings with 0, 5, 10, 15 d of dehydration treatment.

 
Plants require a certain moisture level (between 80 – 95%) in the plant canopy to retain normal growth and development. Plants would start wilting at 80% moisture and will not be recoverable if canopy moisture content drops to 70% (Chevone et al., 1990). The root is one of the most important plant organs sensitive to water deficiency. After the 15-d dehydration treatment, the root of PI 407155 could still keep around 80% moisture for growth, whereas Essex could only hold 75% of water in the root. This is probably why PI 407155 exhibited higher biomass accumulation in both roots and shoots, less moisture loss, and less severe wilting symptoms under 15 d of dehydration stress. Overall, PI 407155 maintained relatively high moisture content and continuous biomass accumulation under dehydration stress, suggesting that PI 407155 is more tolerant than Essex in response to water deficit.

Electrolyte Leakage Analysis
The plasma membrane is a known direct target of dehydration-induced cellular injury (Bray, 1997). The occurrence of cell membrane injury as a function of stress-induced leakage of electrolytes from soybean tissues was investigated in an effort to reveal some of the physiological events that contribute to the differential responses of soybean genotypes to dehydration. After 5 d of dehydration stress, the %EL of Essex increased almost three times from the control value of 22.02 to 63% (Fig. 4 ), indicating the cell membrane has been severely damaged. In contrast, the %EL of PI 407155 reached 33% after 5 d dehydration treatment, only about twice the increase from the control value of 15.67%, which is approximately half of the Essex %EL (63%). The %EL for both Essex and PI 40155 was significantly increased relative to the controls, indicating that the early stage of stress is accompanied by extensive disruption of cellular membranes. The %EL values showed a genotype ranking that was consistent with the ranking based on result of the biomass accumulation and moisture content, suggesting that PI 407155 can withstand the effects of water deficit better than Essex. However, further physiological and genetic studies will be required to estimate the exact contribution of cell membrane stability to the overall mechanism of soybean tolerance to dehydration stresses.


Figure 4
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  		Fig. 4. The percentage electrolyte leakage (%EL) of PI 407155 and Essex under control (well-watered) and after 5 d of dehydration stress. Bars representing mean values followed by the same letter within a graph are not significantly different at the P < 0.05 level. Error bars indicate ± one standard error unit.

 
GlyDREB1 Expression Analysis
The DREB/CBF belongs to a group of transcription factors containing the AP2/EREBPs (APETALA2/ethylene-responsive element binding proteins) domain, which regulate the downstream genes through ABA-independent signal transduction pathway (Liu et al., 1998; Yamaguchi-Shinozaki and Shinozaki, 1994). The early induction of the DREB/CBF by abiotic stresses functions in the signal transduction pathway by regulating the expression of a battery of downstream defense-related genes that contain the DRE/CRT (Drought Response Element or C-Repeat) in their promoters (e.g., cor15a, cor6.6, and kin1) (Thomashow, 1994; Ingram and Bartels, 1996). In Arabidopsis and some crop species (e.g., Brassica, rice, barley, wheat), the DREB/CBF genes have been shown to be rapidly induced in response to dehydration, cold, and high salt stresses (Dubouzet et al., 2003; Jaglo et al., 2001; Morsy et al., 2005). An emerging theme in crop genetics and breeding is the allelic variation for stress tolerance, which may be defined by the major regulators of the stress response genetic network. Therefore, the GlyDREB1 was amplified from G. soja PI 407155 and G. max cv. Essex using RNA isolated from dehydrated seedlings.

In our study, GlyDREB1 protein was found to have 50 to 55% similarity with other DREB-related sequences from other higher plants, e.g., Arabidopsis thaliana, Capsicum annuum, Lycopersicon esculentum, and Prunus avium (Fig. 5 ). The GlyDREB1 protein also has 99% identity to the Glycine max CBF-like protein (accession number AAQ02703) recently cloned from Thomashow's lab. The GlyDREB1 protein contains three similar structural features compared to other DREB1 proteins: (i) R/K-rich putative nuclear-localization signal (NLS) in the N-terminal (PKKRAGRKKFRETRHP); (ii) 59-amino acid AP2/EREBP DNA-binding domain, which is comprised of an {alpha}-helix and a three-stranded antiparallel ß sheet that interacts with base pairs within the DNA major groove (Riechmann and Meyerowitz, 1998); and (iii) Ala-rich acidic activation domain, which functions in gene transcription (Riechmann et al., 2000).


Figure 5
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  		Fig. 5. Comparison of full-length GlycineDREB1 amino acid sequence with other dicot homologs. GlyDREB1 = Glycine soja dehydration responsive element binding factor cloned in this study (AY802779); AtDREB1B = Arabidopsis thaliana DREB1B (NP_567721); CaDREB1 = Capsicum annuum DREB1 protein (AAR88363); LeCBF1 = Lycopersicon esculentum C-repeat binding factor CBF1 (Aak57551); PnDREB1 = Prunus avium DREB1 protein (BAC20184). The conserved amino acid sequences are highlighted in black (identical) and gray (similar). The position of the signature AP2 domain is underlined. The consistent PKKRAGRKKFRETRHP located immediately upstream of AP2 was labeled as nuclear-localization signal. The variable C-terminal extension is in the gray box. The conserved DSAW motif at the end of AP2 domain is indicated with the dashed double lines. The consistent valine (V14) and glutamic acid (E19) in the AP2 domain are indicated with triangle.

 
RNA gel blot analysis showed that GlyDREB1 was significantly induced by dehydration in PI 407155 but not in Essex (Fig. 6A ). The transcription level of GlyDREB1 was much higher in the dehydrated PI 407155 than in the control PI 407155 and dehydrated and control Essex. But the GlyDREB1 expression did not show any difference between dehydration-stressed and control Essex, suggesting Essex may not protect itself in response to dehydration stress. The data also indicated that the GlyDREB1 gene could be highly up-regulated in the PI 407155 in response to dehydration stress.


Figure 6
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  		Fig. 6. Comparative analysis of dehydration-induced DREB1 gene expression in PI 407155 (G. soja) and Essex (G. max). (A) GlyDREB1 transcripts were detected in PI 407155 by northern blot at 12 d after dehydration stress (+, with irrigation; –, without irrigation), but not in Essex with or without dehydration stress and well-watered PI 407155. The glyceraldehydes-3-phosphate dehydrogenase (GAPDH) was used as control probe for sample loading. (B) Semi-quantitative PCR showing the differential GlyDREB1 temporal expression patterns between PI 407155 and Essex. The GlyDREB1 expression in PI 407155 exhibited a significant increase from the basal level beginning at 12 h after the dehydration stress. Expression in Essex remained a relatively constant (basal) level during the 36 h duration of dehydration stress. The constitutive expression of the actin gene is shown as negative control.

 
A semi-quantitative analysis of GlyDREB1 expression in PI 407155 (G. soja) and Essex (G. max) is shown in Fig. 6B. The semi-quantitative PCR showed that GlyDREB1 in PI 407155 was rapidly induced (1 h after dehydration shock) and transcript levels increased further after 18 h of dehydration shock and remained elevated through the duration of the stress treatment. The GlyDREB1 expression in Essex was also rapidly induced after 1 h of dehydration, but was much weaker than that in PI 407155. Moreover, the second induction observed after 12 h of dehydration shock in PI407155 was not observed in Essex. Obviously, two major differences of GlyDREB1 expression between Essex and PI 407155 within the 36hr induction phase were noted. First, there are two induction phases of GlyDREB1 expression in PI 407155: one is at 1 h and the other is at 12 h of dehydration shock, while Essex only has high activation of GlyDREB1 after 36 h of dehydration shock. Second, transcript level was higher in all five time-points (1, 12, 18, 24, and 36 h) for PI 407155 than Essex. The result indicated that activation of GlyDREB1 expression in PI 407155 occurred significantly earlier than expression in Essex. This indicates that the DREB1 genes from G. max and G. soja are different within their regulatory regions and that the observed difference in timing and strength of expression is due to variation in the organization of various cis-elements between the orthologs.

It is also interesting to note that the difference in the timing and strength of dehydration-induced GlyDREB1 gene expression appears to be correlated with the difference in the severity of cell membrane injury between PI 407155 and Essex after they have been subjected to 5 d of no irrigation. In Arabidopsis, DREB genes are known to induce a group of novel cor/rd genes, whose biochemical functions are either directly or indirectly involved in biochemical mechanisms that enhance membrane stability (Thomashow, 1999). Therefore, the less severe membrane injury exhibited by PI 407155 after 5 d of no irrigation may be a consequence (at least in part) of the earlier and higher expression of GlyDREB1 and its downstream target genes. Furthermore, the different expression of the GlyDREB1 gene between PI 407155 and Essex is consistent with their difference on biomass accumulation and moisture content.

In summary, we have isolated the Glycine homolog DREB1 (GlyDREB1) of the CBF/DREB-type transcription factors. The dehydration-induced expression of this gene showed interesting correlation with differential physiological responses of Glycine soja and Glycine max to dehydration stress. The real agronomic significance of these results needs further confirmation by the analysis of larger sets of Glycine genotypes. Nevertheless, the current result appears to be consistent with the common belief that wild species of soybeans are more tolerant to abiotic stresses than soybean cultivars.

Received for publication April 10, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 




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