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a University of Idaho, 3793 N 3600 E, Kimberly, ID 83341-5076
b USDA-ARS-Northwest Irrigation & Soils Research Laboratory, Kimberly, ID 83341-5076
* Corresponding author (singh{at}kimberly.uidaho.edu)
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Abbreviations: NS, non-stressed • DS, drought-stressed • DII, Drought intensity index • DSI, drought susceptibility index • PR, percent reduction • WUE, water use efficiency
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The effects of drought stress vary depending on the frequency, duration, and intensity of stress and growth stages affected. In dry bean, excessive abortion of flowers, young pods, and seeds occurs because of drought stress during pre-flowering (10 to 12 d before anthesis) and reproductive periods. Moderate to severe drought stress reduced biomass and seed yield (from 20 to 90%), harvest index, number of pods and seeds, seed weight, and days to maturity (Nielsen and Nelson, 1998; Nuñez-Barrios et al., 2005; Ramírez-Vallejo and Kelly, 1998; Terán and Singh, 2002a). Drought stress reduced P uptake (Guida dos Santos et al., 2004) and N concentration, partitioning, and fixation in dry bean (Ramos et al., 1999; Serraj and Sinclair, 1998). Drought stress increases root shrinkage that consequently affects nutrient transport to the root surface due to reduced contact between root and soil (North and Nobel, 1997). Dry soil particles hold water and nutrient more strongly on the surface, and dry soil is more compact for root penetration (Passioura, 2002). Root rots caused by Macrophomina phaseolina (Tassi) Goid., Fusarium solani f. sp. phaseoli (Burk.) Snyder & Hansen, and other fungi may aggravate drought stress. Similarly, drought-stressed cultivars are prone to damage by leafhoppers (Empoasca kraemeri Ross and Moore) in the tropics and subtropics.
Among Phaseolus species the tepary bean, P. acutifolius A. Gray, has the highest level of drought resistance (Lazcano-Ferrat and Lovatt, 1999). However, the drought resistance genes from tepary bean have not yet been introgressed into dry bean. In dry bean, drought resistance was reported in the races Durango, Mesoamerica, and Jalisco (Terán and Singh, 2002a). The highest level of drought resistance among these races occurs in the race Durango, which originated in the semiarid central and northern highlands of Mexico (Singh et al., 1991). Race Durango cultivars also predominate in the U.S. and North America. These cultivars mostly possess indeterminate, prostrate growth habit Type III (Singh, 1982). The objectives of this study were to: (i) characterize three race Durango dry bean landraces and 13 cultivars developed between 1932 and 1998 for biomass and seed yield, harvest index, seed weight, and number of days to maturity under drought-stressed (DS) and non-stressed (NS) environments, and (ii) identify those with high levels of drought resistance.
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MATERIALS AND METHODS |
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Dry bean in each market class had a representative landrace or selection thereof. For example, UI 59 was selected for Bean common mosaic virus (BCMV, a potyvirus) resistance from a Great Northern landrace grown by Mandan tribes of North Dakota (Dean, 2000). Common Pinto and Common Red Mexican are landraces that were cultivated by Native Americans in the western USA. Most of the 13 cultivars were selected based on their seed yield in trials performed between 1999 and 2001 in Southern Idaho (Singh et al., 2001).
The landraces and cultivars were arranged in a randomized complete block design with four replications each in NS and DS environments. Each plot consisted of eight rows of 7.62 m length and 0.56 m between rows. An average of 23 seeds per linear meter of row length was planted. The NS and DS trials were planted adjacent to each other in the same field separated by a band of eight rows of dry bean in DS to reduce lateral infiltration of water from NS to DS plots. The NS trial received seven irrigations (661 mm) in 2003 and five irrigations (571 mm) in 2004. The DS trial received four irrigations (378 mm) in 2003 and two irrigations (201 mm) in 2004. The amount of irrigation water was monitored using three pairs of small trapezoidal flumes. Each pair of flumes was located in the same furrow, one at the top and the other at the bottom of the furrow to measure water flow rate passing through furrows and water applied according to the procedures described in the Water Resources Research Laboratory Manual (2001). Mean daily precipitation; minimum, maximum, and mean temperature; solar radiation; evapotranspiration Kimberly-Penmann; mean humidity; and average wind speed were recorded from the Twin Falls Agrimet Station (<1000 m away from the plots) located at 42° 32' 46'' N; and 114° 20' 43'' W at the USDA-ARS Northwest Irrigation and Soils Research Laboratory at Kimberly, Idaho (www.usbr.gov/gp/agrimet/index.cfm, verified 12 June 2006).
Growth habit was recorded during flowering and verified at maturity. Days to maturity was recorded when 90% of the pods changed color from green to yellow. Biomass yield (kg ha–1) was determined for each genotype by cutting 10 plants at ground level at maturity and drying at 60°C for three d. The six central rows (25.60 m2) were cut at 108 d after planting in 2003 and 100 d in 2004, threshed eight d later, cleaned, dried, and seed yield recorded (kg ha–1) at 12% moisture by weight. Harvest index was determined as the ratio between seed and biomass yield. Weight (g) of 100 seeds taken randomly was recorded. Drought intensity index (DII) for each year and drought susceptibility index (DSI) and percent reduction (PR) due to drought stress were calculated for each genotype according to Fischer and Maurer (1978).
Two dry bean landraces (Common Pinto and Common Red Mexican) and four of 13 cultivars (Othello, UI 320, NW 63, and UI 259) were chosen to estimate soil water content and water use in two of four replications in NS and DS environments. Soil samples were taken after planting, one d before and two d after each irrigation, and one d before harvest. In 2003, water content was estimated taking soil samples with an auger every 0.2 m until reaching 2 m depth with exception of the first 0.2 m where two samples were taken, 0 to 0.1 and 0.1 to 0.2 m. The 11 samples at each site were collected in metal cans and weighed before and after oven drying at 105°C for 24 h. In 2004, water content was estimated similarly as described above, but only the first and last samplings were conducted to depth of 2 m. All other samplings were conducted to a 1.2 m depth because in 2003 changes in water content beneath 1.2 m were small. The water content on mass and volumetric bases was calculated according to Cuenca (1989).
To measure water potential in centibars at 0.23, 0.46, and 0.92 m depth, soil moisture sensors or watermarks (Irrometer Company, Inc, Riverside, California) connected to AM400 dataloggers (Hansen Company, East Wenatchee, Washington) were used. The sensors were attached to 1/2 inch PVC tubes to facilitate their installation and recovery. The AM400 datalogger recorded water potential every 8 h. Six AM400 dataloggers and 36 soil moisture sensors were used in NS and DS environments. Every datalogger recorded data at three depths for two genotypes. In addition, each datalogger recorded soil temperature at 0.31 m depth.
A mixed model (McIntosh, 1983) was used for data analysis whereby years and replications were considered random and water stress treatments and genotypes were fixed effects. Data for each year were analyzed separately and the homogeneity of error variances was tested according to Bartlett (1947) before performing combined analyses. Simple correlation coefficients among traits were determined using the mean values for each year. All data were analyzed using the SAS (v 9.1.3) GLM procedure (SAS Institute, 2004).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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In both years in NS and DS, mean seed yield of cultivars of red market class tended to be slightly higher than great northern and pinto market classes (Table 3). In great northern, mean seed yield of Matterhorn over the 2 yr was higher in NS and DS, whereas UI 59 and US 1140 had the lowest yield, but significant differences occurred only in the DS environment. Among pinto cultivars, Bill Z in NS and CO 46348 in DS had the highest yield averaged over the 2 yr. In contrast, Topaz and Common Pinto followed by UI 320 had the lowest yield in NS and DS. Although LeBaron had the lowest yield in red market class in both environments, differences in NS were not significant and Common Red Mexican followed by UI 239 had the highest yield in DS. Reduction in seed yield due to drought stress ranged from 34% for Othello to 90% for Topaz in 2003 (Table 3). A much smaller reduction occurred in 2004 due to a milder drought stress (Table 1). Matterhorn, Othello, and Common Red Mexican had DSI values less than 1.0 in both years. In contrast, US 1140, Common Pinto, Topaz, UI 320, and LeBaron, all relatively early maturing, tended to have DSI values higher or equal to 1.0.
Harvest Index
Mean squares for the year, test environment, genotype, and the interaction between year and test-environment were highly significant (Table 2). The lowest average harvest index was observed in DS in 2003 (Table 3). Othello, UI 239, CO 46348, and Common Red Mexican had the lowest reduction in harvest index due to severe drought stress in 2003. The largest harvest index reduction was observed in Topaz, Buster, Common Pinto, and UI 259 under DS environment in 2003.
Seed Weight
Mean squares for the year, test-environment, genotype, and interaction of genotype with year and test-environment were highly significant for seed weight (Table 2). Common Pinto and Common Red Mexican had the smallest and Buster, CO 46348, and UI 320 had the largest seed weight (Table 3). Reduction in seed weight due to drought stress ranged from 0 to 22% in 2003 and from –3 to 10% in 2004 (Table 3). However, in both years seed weight of Common Red Mexican was not affected by drought stress. Drought susceptible UI 59, Bill Z, Common Pinto, Topaz, and UI 259 had higher reduction in seed weight due to drought stress. In contrast, in addition to Common Red Mexican, other drought resistant cultivars namely, CO 46348, Matterhorn, and Othello had the lowest reduction in seed weight over the 2 yr.
Days to Maturity
Mean squares for the number of days to maturity were significant for the year, test-environment, and genotype (Table 2). Moreover, significant interactions occurred between year and genotype, and both interacted with the test-environment. In 2003, all genotypes except UI 259 took longer to mature in DS than in NS environment (Table 3). These differences among genotypes ranged from 1 d for CO 46348 and Common Red Mexican to 14 d for Bill Z, Common Pinto, and Topaz. In contrast to 2003, in 2004 all genotypes except UI 465 and Topaz either matured the same day under DS and NS or took 1 to 6 d longer in NS than in DS.
Correlation Coefficients
Biomass yield under NS was positively correlated to biomass yield under DS in both years (Table 4). Biomass yield under NS was positively correlated to seed yield under NS and DS in 2003, but not in 2004. Similarly, biomass yield under DS was positively correlated to seed yield under NS and DS, and to harvest index and seed weight under DS in 2003, but negatively correlated with harvest index under NS and DS in 2004. Seed yield in NS was positively correlated to seed yield under DS in both years. Furthermore, seed yield under NS and DS was positively correlated to harvest index under DS in both years. In addition, seed yield under DS was negatively correlated to days to maturity under DS in 2003 and positively correlated in 2004. Harvest index under NS was positively correlated to harvest index under DS in 2004. A positive association was found between seed weight under NS and DS in both years. Maturity under NS was positively associated to maturity under DS in 2004.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Drought resistant (e.g., Common Red Mexican, NW 63, Othello) as well as susceptible (e.g., Common Pinto, UI 259, UI 320) landraces and cultivars mostly extracted water from the upper 45 to 50 cm soil profile and hence showed no significant differences in water potential at 46 and 92 cm soil depths, even under the most severe DS environment in 2003. Intermittent drought may have very likely hindered the maximum potential root growth of all genotypes irrespective of their levels of drought resistance. On the contrary, in NS environment, soil moisture often at field capacity would have masked genotypic differences in water potential at most soil depths.
By conducting replicated trials in NS and DS environments in 2003 and 2004 and using mean seed yield, DSI, and PR as selection criteria, and separating drought resistant from susceptible genotypes, it was possible to separate drought resistant genotypes into two groups. One group had relatively higher yield potential in NS environment, such as late maturing Common Red Mexican and CO 46348 and a second group showed moderate yield potential in NS environment, such as Matterhorn and Othello. If the trial had been conducted only in 2004, cultivars such as Bill Z, Buster, and UI 259 would have been classified as drought resistant. This discrepancy indicates that yield data from NS and DS environments across contrasting years (and locations) should be used for dry bean germplasm screening and other studies even in the absence of significant interactions among dry bean cultivars, test-environment, and year.
The summer rainfall in Southern Idaho (and other Western states) often provides < 20% of the required water for normal growth and reproduction of the dry bean crop in the region. Thus, by scheduling the irrigation timing, frequency, and amount of water applied, it should be possible to maximize the usage of water by growing drought resistant landraces and cultivars identified in this study, and to manipulate the severity of drought stress for further germplasm screening, breeding, genetics, and physiology studies. But, unexpected plot management problems and variation in solar radiation and temperature may confound selection for drought resistance and enhanced water-use efficiency. In this study, unexpected soil compaction and crusting, a delay in the first post-emergence irrigation, other management practices, lower humidity, and higher solar radiation and temperatures in 2003, when compared with 2004, accentuated the drought stress; such that the mean NS seed yield was 33% less than the DS yield in 2004 in spite of two additional irrigations, and 26.4 mm higher rainfall.
The optimum mean temperature for normal growth and reproduction of cultivars of race Durango (Singh et al., 1991), also referred as Gene Pool 5 (Singh, 1989), ranges between 18 and 25°C. Temperatures above 28°C cause excessive flower drop, pollen viability reduction, and abortion of fertilized ovules (Masaya and White, 1991). Plants in pre-flowering and flowering stages are extremely sensitive to drought and high temperatures. Reduced photosynthesis, excessive flower bud abscission (Rainey and Griffiths, 2005), and pollen sterility due to tapetal degeneration (Suzuki et al., 2001) followed by flower, ovule, and pod abscission (Ofir et al., 1993; Rainey and Griffiths, 2005) result in reduced pod and seed number, seed size, and yield due to high temperatures (Porch and Jahn, 2001; Prasad et al., 2002). Thus, mean temperatures above 25°C for 11 d and temperatures above 35°C for 18 d during flowering and seed-filling periods in 2003 may have accentuated drought stress. Furthermore, maximum photosynthesis occurs in dry bean when solar radiation is between 600 and 650 calories/cm2 (White and Izquierdo, 1991). Consequently, a larger reduction in overall biomass and seed yield in both NS and DS environments due to drought stress, elicited by the above factors, occurred in 2003 compared with 2004. In future studies, it may be worthwhile to determine flower and pod drops, and pod and seed numbers in NS and DS and separate the effects of high temperature and solar radiation from management practices and drought stress.
Under terminal drought stress, number of days to maturity is often shortened (Terán and Singh, 2002a, 2002b). However, in this study, number of days to maturity was delayed in DS compared to NS in 2003. The discrepancy could be largely because, in contrast to a terminal drought, an intermittent drought stress was imposed in both vegetative and reproductive periods; thus, repeated disruption followed by recovery occurred in this study. Furthermore, all three landraces and 13 cultivars had indeterminate growth habits Type II or Type III. Thus, a severe intermittent drought during flowering and seed filling period resulted in a split-pod set in 2003 delaying overall maturity. Delayed maturity was observed when drought stress occurred in pre-flowering stage (Dubetz and Mahalle, 1969). Moreover, the number of days to maturity was not correlated with seed yield under DS. In a previous study, number of days to maturity was positively correlated with seed yield in NS and early maturity may have helped early maturing cultivars escape terminal drought (White and Singh, 1991). In this study, under intermittent drought stress, all early maturing landraces and cultivars (except Othello), that included US 1140, Common Pinto, Topaz, UI 320, and LeBaron, were susceptible to drought. Thus, genes and QTL for drought resistance seem to be different from those controlling maturity in dry bean. Furthermore, when screening germplasm for drought resistance and water use efficiency in the western USA, an intermittent drought throughout the growing season should be used to avoid escapes due to early maturity.
A positive association between biomass and seed yield in DS and NS, and biomass and seed yield and harvest index in DS in 2003, and generally a negative association between the biomass yield and harvest index in both the NS and DS in 2004 may suggest that overall growth of three dry bean landraces and 13 cultivars was limiting in 2003. The biomass yield in severe DS could therefore be a useful selection criterion for drought resistance, and dry bean producers may apply more frequent irrigation to reduce drought stress to maximize seed yield. On the contrary, the frequency of irrigation and amount of water applied should be reduced in more favorable growing conditions to reduce biomass yield and maximize harvest index in race Durango cultivars in the western USA.
Positive correlation coefficients between seed yield and harvest index in DS were larger and highly significant in both years than in NS. Drought susceptible genotypes, in general, had a relatively lower harvest index irrespective of their maturity. Thus, the ability of drought resistant landraces and cultivars for partitioning a relatively higher amount of photosynthate from vegetative organs to developing seed appeared to have played a crucial role in minimizing the adverse effects of drought stress.
Although all three landraces, or selections thereof, and the 13 cultivars belonged to race Durango and were relatively well adapted to Southern Idaho, large differences were found with regard to their response to severe drought stress in 2003. For example, of the three landraces, only Common Red Mexican was drought resistant. The most recently developed cultivars in the red market class, namely LeBaron (Hang et al., 2000) and UI 259 (Myers et al., 2001b), were highly susceptible to drought. As noted earlier, NW 63 (Burke, 1982) and UI 239 (Myers et al., 1997), also derived from Common Red Mexican and released several years earlier than LeBaron and UI 259, had an intermediate level of resistance to severe drought stress in 2003. Thus, drought resistant alleles and QTL seem to have been inadvertently lost in modern cultivars of the red Mexican market class. Dry bean cultivars developed by the USDA-ARS researchers at Prosser, Washington, in general, exhibit moderate to high levels of resistance to drought (Miller and Burke, 1983; Singh et al., 2001), low soil fertility (Westermann and Singh, 2000), and Fusarium root rot (Burke and Miller, 1983; P. Miklas, unpublished data). Superior performance of those cultivars could be largely because a "purgatory-plot" with general water, nutrient, and root rot stresses and alternate-year bean cropping at Roza, Washington has been used for germplasm screening and selection for decades. It is therefore expected that cultivars such as NW 63 and Othello (Burke et al., 1995) developed at Prosser, and their derivatives such as UI 239 that were developed at Kimberly, Idaho, but tested at Roza before their release, also exhibited moderate to high levels of drought resistance.
Common Red Mexican has the typical characteristics of race Durango (Singh et al., 1991). Its leaves are small, relatively dark, and it often does not produce any guides. Also, the lower internodes are shorter, providing good ground cover, thus minimizing evaporation and conserving moisture. Leaves stay green for a longer period, which may facilitate higher seed filling capacity compared to other cultivars. Whether these characteristics are linked with, or have pleiotropic effects of favorable genes and QTL determining drought resistance in Common Red Mexican is not known. Nonetheless, Common Red Mexican was used extensively as a source of adaptation to semiarid environments and resistance to Beet curly top virus (a leafhopper-vectored geminivirus) in dry bean breeding programs in the western USA. For example, cultivars Othello (Burke, 1982), Bill Z (Wood et al., 1989), UI 239 (Myers et al., 1997), UI 259 (Myers et al., 2001b), and NW 63 (Burke et al., 1995) have Common Red Mexican in their parentage (Miklas, 2000).
In contrast to the red Mexican market class, the landraces of pinto (Common Pinto) and great northern (UI 59, a selection from Common Great Northern landrace, see Dean, 2000) market classes used in this study were highly susceptible to drought. But some cultivars from these (in addition to Othello) market classes, namely great northern Matterhorn and pinto CO 46348, although not specifically bred for drought resistance, were drought resistant. Unlike Common Red Mexican why were Common Pinto and UI 59 not resistant to drought? One possible reason could be that they were selected in cooler environments in the absence of drought. For example, the great northern landrace from which UI 59 and other early University of Idaho cultivars were selected was obtained from the Mandan tribes of North Dakota (Dean, 2000), where it is much cooler and wetter than Southern Idaho. Thus, selection for drought resistance may have never been practiced in the great northern landrace. Also, great northern may have had its origin in the humid highlands of Middle America, and not in the semiarid Mexican highlands.
Native Americans and early settlers grew pinto ‘San Juan’ in the dryland farming systems in the San Juan Basin of Arizona, Colorado, New Mexico, and Utah (M. Brick, personal communication, 2005). San Juan and its derived cultivars Cahone (Wood et al., 1983) and Fisher (Fisher et al., 1995) are partially sensitive to summer months in Southern Idaho. Consequently, they take over 3 wk longer to flower and mature than Common Pinto. Photoperiod insensitive and early maturing, Common Pinto landrace is possibly a mutant of San Juan or similar landrace that lost its drought resistance; or, alternatively it is an independent introduction from the highlands of Mexico by Native Americans or early settlers that is adapted to the Pacific Northwest.
Matterhorn may in part combine drought resistance from the small-seeded tropical black bean used to introgress upright plant type and lodging resistance by Kelly et al. (1999). Similarly, Othello may derive its drought resistance from Common Red Mexican and Local Pink (a landrace from California) via Sutter Pink. Othello also has in its pedigree a tropical black bean landrace (N 203 synonymous with PI 203958) from coastal Mexico that was extensively used as a source of Fusarium root rot resistance in the USDA-ARS-Prosser, Washington breeding program (Burke et al., 1995; Miklas, 2000).
Identification and judicious use of favorable alleles and QTL present in these drought resistant landrace and cultivars and other landraces such as Apetito (synonymous with G 13637, Padilla-Ramírez et al., 2005) and San Cristobal 83 (Terán and Singh, 2002a), cultivars (e.g., Condor), and breeding lines (e.g., 115M, BAT 477, B 98311, L 88–63, SEA 5) may be pivotal for the future development of highly drought resistant cultivars for dryland and irrigation-assisted sustainable production systems in the western USA. Identification and pyramiding of complementary drought resistant alleles and QTL from other common bean races, gene pools, and related Phaseolus species (e.g., P. acutifolius) may be worthwhile for long-term sustained genetic progress for drought resistance and improved water use efficiency (WUE).
Cultivation of highly drought resistant dry bean cultivars such as Common Red Mexican, Matterhorn, CO 46348, and Othello should be promoted in areas with endemic drought and recurring water shortage. Under such environments, early maturing drought resistant cultivars such as Othello should help conserve water because they may be grown with less irrigation than the later maturing full-season Common Red Mexican and CO 46348. Higher yielding, early maturing cultivars may also provide flexibility for later planting or earlier harvest, thus avoiding unexpected frost in late spring and early fall. Nonetheless, further studies may need to be conducted to determine irrigation schedules and amount of water to be applied to each drought resistant landrace and cultivar.
In dry bean, seed weight, color, and shape are important components that determine the recovery percentage and commercial value. Drought stress reduced seed weight in both 2003 and 2004. The extent of reduction depended on the level of drought stress and genotypes. For example, under severe drought stress in 2003, UI 259 had the highest reduction (22%) in seed weight, but under moderate drought stress only 9% reduction occurred in 2004. Common Red Mexican and other cultivars that showed limited reduction in seed weight under DS in either year should be preferred over those with marked reduction due to drought stress. Also, it may be worthwhile to determine the genetic basis of seed weight in Common Red Mexican that set it apart from all other cultivars.
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ACKNOWLEDGMENTS |
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Received for publication March 29, 2006.
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This article has been cited by other articles:
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  S. P. Singh, H. Teran, M. Lema, M. F. Dennis, R. Hayes, and C. Robinson Breeding for Slow-Darkening, High-Yielding, Broadly Adapted Dry Bean Pinto 'Kimberly' and 'Shoshone' Journal of Plant Registrations, September 1, 2008; 2(3): 180 - 186. [Abstract] [Full Text] [PDF]
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M. A. Brick, J. B. Ogg, S. P. Singh, H. F. Schwartz, J. J. Johnson, and M.A. Pastor-Corrales Registration of Drought-Tolerant, Rust-Resistant, High-Yielding Pinto Bean Germplasm Line CO46348 Journal of Plant Registrations, May 1, 2008; 2(2): 120 - 124. [Abstract] [Full Text] [PDF]
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 S. E. Beebe, I. M. Rao, C. Cajiao, and M. Grajales Selection for Drought Resistance in Common Bean Also Improves Yield in Phosphorus Limited and Favorable Environments Crop Sci., March 19, 2008; 48(2): 582 - 592. [Abstract] [Full Text] [PDF]
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S. P. Singh Drought Resistance in the Race Durango Dry Bean Landraces and Cultivars Agron. J., August 10, 2007; 99(5): 1219 - 1225. [Abstract] [Full Text] [PDF]
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S. P. Singh, H. Teran, M. Lema, D. M. Webster, C. A. Strausbaugh, P. N. Miklas, H. F. Schwartz, and M. A. Brick Seventy-five Years of Breeding Dry Bean of the Western USA Crop Sci., May 31, 2007; 47(3): 981 - 989. [Abstract] [Full Text] [PDF]
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