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Published online 27 May 2005
Published in Crop Sci 45:1264-1270 (2005)
© 2005 Crop Science Society of America
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SEED PHYSIOLOGY, PRODUCTION & TECHNOLOGY

Fagopyritol Accumulation and Germination of Buckwheat Seeds Matured at 15, 22, and 30°C

Marcin Horbowiczb and Ralph L. Obendorfa,*

a Seed Biology, Dep. of Crop and Soil Sciences, Cornell Univ. Agricultural Experiment Station, Cornell Univ., Ithaca, NY 14853-1901
b Research Institute for Vegetable Crops, Skierniewice, Poland

* Corresponding author (rlo1{at}cornell.edu)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Common buckwheat (Fagopyrum esculentum Moench; Polygonaceae) embryos accumulate six fagopyritols in two unique series: fagopyritol A1, fagopyritol A2, fagopyritol A3, fagopyritol B1, fagopyritol B2, and fagopyritol B3. Fagopyritol A1 is isosteric to a putative insulin mediator believed to be deficient in subjects with noninsulin dependent diabetes mellitus (NIDDM) and polycystic ovary syndrome (PCOS). Fagopyritols accumulate during seed development, and accumulation is enhanced in response to cooler temperatures. The objective was to test the hypothesis that seed maturation at cooler temperature enhances fagopyritol accumulation, improves seed quality, and increases yield of desirable fagopyritols for dietary treatment of NIDDM and PCOS. Seeds from buckwheat plants grown at 15, 22, or 30°C were harvested at 8, 12, 16, 20, and 28 d after pollination (DAP) and analyzed for soluble carbohydrates in the embryos. Remaining seeds were dried and tested for germination and seedling growth. Embryo dry weight increased rapidly between 8 and 12 DAP at 30°C, 12 and 16 DAP at 22°C, and 16 and 20 DAP at 15°C. Seed dry weight declined (–0.86 mg per 1°C) when maturation temperature increased. Total soluble carbohydrates remained constant across seed maturation temperatures, but the composition of carbohydrates changed in response to different maturation temperatures. Fagopyritol A1 and fagopyritol B1 were highest in seeds matured at 15°C, whereas fagopyritol A2, fagopyritol B2, fagopyritol A3, raffinose, and stachyose were higher in seeds matured at 30°C. At harvest, seeds matured at 30°C had highest germination. Cool temperatures during buckwheat seed maturation can result in increased seed size and yield of fagopyritol A1 and fagopyritol B1 in embryos for nutritional and medicinal applications.

Abbreviations: DAP, days after pollination • DGMI, digalactosyl myo-inositol • DW, dry weight • FW, fresh weight • NIDDM, noninsulin dependent diabetes mellitus • PCOS, polycystic ovary syndrome • RFOs, raffinose family oligosaccharides • RH, relative humidity


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
ORIGINATING in northeast Asia, southern Siberia, and northern China, common buckwheat (Polygonaceae family) is one of 18 recognized natural species of Fagopyrum and is the most important from economical, agricultural, and nutritional points of view. In buckwheat, the triangular fruit (achene) forms a single seed. The buckwheat embryo is rich in lipids (Horbowicz and Obendorf, 1992) and high quality proteins (Elpidina et al., 1990) and is embedded in a starchy endosperm (Marshall and Pomeranz, 1982; Steadman et al., 2001a).

Common buckwheat plants are dimorphic and heterostylous. One-half of the plants have pin-type flowers with long styles and short stamens, and one-half have thrum-type flowers with short styles and long stamens (Morris, 1952; Marshall and Pomeranz, 1982). Each type is self-incompatible and cross-incompatible among plants with the same flower type. Seed set requires legitimate cross pollination, pin by thrum and thrum by pin, by insects under field conditions, or by hand pollination in the greenhouse (Horbowicz and Obendorf, 1992) as in the present study.

Buckwheat plants grow best in cool, moist climates. Daytime air temperatures of 17 to 19°C are optimal during flowering and seed maturation of this plant (Marshall and Pomeranz, 1982). Because the crop matures in 10 to 12 wk after seeding, it can be grown in temperate regions and higher altitude areas. The crop is sensitive to high temperature and water deficiency stresses, especially during flowering and seed set (Slawinska and Obendorf, 2001; Taylor and Obendorf, 2001).

The correlation between accumulated soluble carbohydrates and the development of seed desiccation tolerance and storability has been reported (Koster and Leopold, 1988; Blackman et al., 1992; Horbowicz and Obendorf, 1994; Black et al., 1996; Obendorf, 1997; Obendorf et al., 1998). Developing legume and grass seeds accumulate mostly sucrose and {alpha}-galactosides of sucrose, including raffinose, stachyose, and verbascose (raffinose family oligosaccharides or RFOs) (Horbowicz and Obendorf, 1994; Black et al., 1996; Brenac et al., 1997; Obendorf, 1997). RFOs are not always correlated to desiccation tolerance (Black et al., 1999). Instead of RFOs, developing buckwheat seeds accumulate mostly sucrose and fagopyritols, {alpha}-galactosides of D-chiro-inositol (Horbowicz et al., 1998).

Six fagopyritols, representing two distinct series differing in bonding positions, were found in buckwheat seeds (Horbowicz et al., 1998; Szczecinski et al., 1998; Obendorf et al., 2000; Steadman et al., 2000, 2001b). Fagopyritol B1 and fagopyritol A1 (Obendorf et al., 2000) were the major fagopyritols accumulated in buckwheat seeds (Horbowicz et al., 1998). Structures of mono-, di-, and trigalactosides of D-chiro-inositol have been confirmed (Obendorf et al., 2000; Steadman et al., 2001b). Fagopyritols accumulate in the dicotyledonous embryo of buckwheat seeds, mostly in the cotyledons (Horbowicz et al., 1998).

D-chiro-Inositol is a component of galactosamine D-chiro-inositol, a putative insulin mediator (Larner et al., 1988; Romero and Larner, 1993), believed to be deficient in subjects with NIDDM (Asplin et al., 1993) because of abnormal D-chiro-inositol metabolism (Kennington et al., 1990; Ortmeyer et al., 1993). Adding D-chiro-inositol as a dietary supplement appeared to be effective in lowering symptoms of NIDDM (Ortmeyer et al., 1995; Fonteles et al., 2000; Kawa et al., 2003) and PCOS (Nestler et al., 1999). Several research groups are developing sources for natural and synthetic supplies of D-chiro-inositol (Kennington et al., 1992; Mandel et al., 1993). One natural source of D-chiro-inositol (in free form and as galactosides, predominantly fagopyritol A1 and fagopyritol B1) is buckwheat seed. During dry milling, fragments of the outer cotyledon adhere to the bran (Steadman et al., 2001a). Therefore, the bran milling fraction from buckwheat seed (Steadman et al., 2000; 2001a) can be used for isolation and preparation of fagopyritols and free D-chiro-inositol for production of nutraceuticals and pharmaceuticals (Obendorf and Horbowicz, 2000, 2002; Obendorf et al., 2000; Steadman et al., 2000; Kawa et al., 2003).

Differences in temperature during development of legume seeds had only minor effects on soluble carbohydrate accumulation (Górecki et al., 1996; Obendorf et al., 1998). However during our preliminary studies, cooler temperatures during seed maturation affected soluble carbohydrate content and composition of buckwheat embryos (Horbowicz et al., 1998). Buckwheat embryos matured at cool temperature (18°C) accumulated higher amounts of fagopyritol A1 and fagopyritol B1, and embryos matured at warm temperature (25°C) accumulated more sucrose and the higher oligomers fagopyritol A2 and fagopyritol B2. During maturation of soybean [Glycine max (L.) Merrill] embryos, warm temperature (25°C) favored accumulation of fagopyritol B1, as well as sucrose, raffinose, D-chiro-inositol, and D-pinitol (Obendorf et al., 1998). The objective of the work reported herein was to test the hypothesis that accumulation of soluble carbohydrates, fresh and dry mass of embryos and seeds, and seed germination are altered in response to different temperatures (15, 22, and 30°C) during buckwheat seed maturation in planta.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Buckwheat plants (cv. Mancan) were grown in the greenhouse at 27°C day (14 h) and 21°C night (10 h) as described by Taylor and Obendorf (2001). Natural sunlight was supplemented 14 h daily with 740 µmol m–2 s–1 light from 1000 W Sylvania metal halide lamps. After opening of the first flowers, plants were separated into pin and thrum types and placed in separate growth chambers at 18°C, the optimum temperature for seed set (Slawinska and Obendorf, 2001). All plants received 14 h of fluorescent light daily at about 300 µmol m–2 s–1. After 7 to 10 d, corresponding to the period of optimum seed set (Taylor and Obendorf, 2001), flowers on plants were cross pollinated by hand, pin x thrum and thrum x pin. At pollination, each plant had three to seven receptive flowers on each of the complex racemes in the terminal cluster of inflorescences and on each of two single racemes at the first and second nodes on the main stem and also on each of two or three primary branches. Sixty to 120 flowers were pollinated, resulting in 25 to 40 seeds on each plant. Eight days after pollination (DAP) the temperature in three growth chambers was changed from 18 to 15°C, 22°C, and 30°C, respectively. Seeds were harvested at 8, 12, 16, 20, and 28 DAP, selected at random and pooled from eight plants at each temperature. Embryos were isolated by cutting the proximal end of the seed and gently removing the embryo free of endosperm through the basal cut. For mature and dry seeds, embryo fragments were collected from gently crushed seeds by hand. Separations were aided by use of a magnification lens (10x). Isolated embryos were extracted, and extracts were analyzed for soluble carbohydrates in the embryos for three replications of three to 10 embryos. Embryo fresh weights and dry weights were determined on a duplicate set of embryos before and after drying at 105°C for 48 h. After the last harvest (28 DAP) seeds were dried at 12% relative humidity (RH) above a saturated solution of LiCl for 14 d before analysis. Weight of each seed (including pericarp) was measured. After drying over LiCl, seeds (four replications of 10 seeds each) were germinated on wet germination papers at 25°C in darkness (Horbowicz et al., 1998). Germination and hypocotyl length were measured after 2, 4, and 6 d. All results were reported as mean ± SE of the mean. Significant differences (P < 0.05) between means were verified by t test.

Soluble carbohydrates in buckwheat embryos were extracted and analyzed by high resolution gas chromatography as previously described (Horbowicz and Obendorf, 1994; Horbowicz et al., 1998). Carbohydrate standards (sucrose, myo-inositol, fructose, glucose, raffinose, and stachyose), internal standard (phenyl {alpha}-D-glucoside), pyridine, and trimethylsilylimidazole (TMSI) were purchased from Sigma (St. Louis, MO). Fagopyritol standards were purified from buckwheat (Horbowicz et al., 1998; Obendorf et al., 2000; Steadman et al., 2001b). Galactinol and D-chiro-inositol standards were gifts.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Buckwheat embryos accumulated maximum fresh weight at 20 DAP when matured at 15°C, at 16 DAP when matured at 22°C, and at 12 DAP when matured at 30°C (Table 1). Highest daily increase in fresh weight occurred between 12 and 16 DAP when matured at 15 and 22°C and between 8 and 12 DAP when matured at 30°C. Independently of maturation temperature, the dry weight of embryos reached maximal values by 20 DAP, but fastest daily increase of dry weight occurred between 8 and 12 DAP at 30°C, between 12 and 16 DAP at 22°C, and between 16 and 20 DAP at 15°C (Table 1). Although differences in the rates of dry matter accumulation occurred between all temperatures, the final dry weight of embryos from seeds matured at 15, 22, and 30°C was similar. Embryo dry weight was also the same when seeds were matured in 18 or 25°C in our previous experiments (Horbowicz et al., 1998).


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  		Table 1. Dry weight (DW) and fresh weight (FW) of buckwheat embryos from seeds matured at 15, 22, or 30°C as a function of days after pollination (DAP).

 
Mean dry weight of seeds (including pericarp) gradually declined when maturation temperature increased. Mean dry weight of buckwheat seeds (± SE; three replications of 10 seeds each) was 48.2 ± 1.8 mg when matured at 15°C, 41.3 ± 1.5 mg at 22°C, and 35.2 ± 1.3 mg at 30°C. The average decrease in dry weight of buckwheat seeds with increasing temperature was –0.86 mg per 1°C.

Maturation temperature had no effect on the total amount of soluble carbohydrates in buckwheat embryos (Table 2). Reducing sugars, fructose, and glucose were present only in early stages of embryo development (8 and 12 DAP, data not shown). Sucrose increased dramatically between 12 and 16 DAP with maximum values at 16 DAP (Fig. 1A). The increase in sucrose was associated with a rapid increase in embryo fresh weight during maturation at 15 and 22°C (Fig. 1A and Table 1). After 16 DAP, sucrose in embryos remained high through 42 DAP (Table 2).


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  		Table 2. Soluble carbohydrates in buckwheat embryos matured at 15, 22, or 30°C.

 


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  		Fig. 1. Accumulation of sucrose, fagopyritol A1, and fagopyritol B1 during maturation of buckwheat embryos at 15, 22, and 30°C. Values (µg embryo–1) are the mean ± SE of the mean for three replications of three to 10 embryos. DAP, days after pollination.

 
The monogalactosides of D-chiro-inositol, fagopyritol A1, and fagopyritol B1, were the dominant soluble carbohydrates in embryos from buckwheat seeds matured at 15°C, but sucrose was dominant when matured at 30°C (Fig. 1 B,C). After drying of seeds (42 DAP), the ratio of fagopyritol B1 to sucrose in embryos was 1.14:1 when matured at 15°C, 0.88:1 when matured at 22°C, and 0.43:1 when matured at 30°C (Table 2). Similarly, the ratio of fagopyritol A1 to sucrose also declined in relation to increased temperature, although the amount of fagopyritol B1 was 5 to 7 times higher than fagopyritol A1 (Fig. 1 B,C and Table 2).

An opposite trend occurred for digalactosides of D-chiro-inositol; higher amounts of fagopyritol A2 and fagopyritol B2 accumulated in embryos matured at 30°C than at 15°C (Fig. 2 B,C). After 2 wk of drying of buckwheat seeds (42 DAP), fagopyritol A2 was fourfold higher and fagopyritol B2 was eightfold higher in embryos of seeds matured at 30°C than in embryos of seeds matured at 15°C (Table 2). A similar trend was found for the digalactoside of myo-inositol (Fig. 3 C). Free myo-inositol in the embryo was similar for seeds matured at 15 and 30°C, but galactinol and digalactosyl myo-inositol were higher in embryos of seeds matured at 30°C than in embryos of seeds matured at 15°C (Tables 2 and 3).



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  		Fig. 2. Accumulation of D-chiro-inositol and its digalactosides, fagopyritol A2 and fagopyritol B2, during maturation of buckwheat embryos at 15, 22, and 30°C. Values (µg embryo–1) are the mean ± SE of the mean for three replications of three to 10 embryos. DAP, days after pollination.

 


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  		Fig. 3. Accumulation of myo-inositol and its galactosides, galactinol and digalactosyl myo-inositol (DGMI), during maturation of buckwheat embryos at 15, 22, and 30°C. Values (µg embryo–1) are the mean ± SE of the mean for three replications of three to 10 embryos. DAP, days after pollination.

 

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  		Table 3. Minor soluble carbohydrates in buckwheat embryos matured at 15, 22, or 30°C as a function of days after pollination (DAP).

 
During later stages of buckwheat embryo development, i.e., after 20 DAP at 22°C and 28 DAP at 30°C, small amounts of raffinose and stachyose were detected (Table 3). In embryos matured at 30°C, fagopyritol A3 (a trigalactoside of D-chiro-inositol) was also detected. These carbohydrates were not detected in embryos matured at 15°C (Table 3). After drying of buckwheat seeds, raffinose, stachyose, and fagopyritol A3 were not detected in embryo extracts (Table 3).

Germination of seeds matured at 22°C was 40% lower than for seeds matured at 30°C (Fig. 4 A) after 4 and 6 d of germination on moist germination paper in darkness and 25°C. Germination of seeds matured at 15°C was intermediate. Germination of seeds matured at 30°C was similar to seeds matured at 15°C after 2 d of germination; however, after 4 and 6 d, seeds matured at 30°C germinated 90%, and seeds matured at 15°C germinated 66 and 71% (Fig. 4 A).



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  		Fig. 4. Seed germination (%) and seedling hypocotyl length (mm) of buckwheat seeds matured at 15, 22, and 30°C and germinated during 2, 4, and 6 d in darkness at 25°C. Values are the mean ± SE of the mean for four replications of 10 seeds.

 
Growth of hypocotyls in germinating buckwheat seedlings was faster for seeds matured at 15 and 22°C than for seeds matured at 30°C after 2 and 4 d, but after 6 d, hypocotyl lengths were not significantly different (Fig. 4B).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The response of plants to stress involves complex physiological and biochemical responses. Conditions during seed development and maturation can have an impact on subsequent seed quality. Soil moisture and temperature stresses have been suggested to have an influence on seed and seedling vigor. Environmental conditions during seed maturation also have an impact on seed viability (Baskin and Baskin, 1998). High temperatures during growth can increase biochemical reactions in plants, but it may not always be transferred to higher productivity because of shortened seed filling period, heat stress constraints such as limited water supply, increase in leaf temperature, increased respiration, or decline in the synthesis and/or activity of photosynthetic enzymes. Buckwheat seeds matured at high temperatures (22 or 30°C) had a lower mean seed weight than those matured at low temperature (15°C), but the embryo dry weights were similar across temperatures. The lower dry weight of the whole seed matured at 30°C was mainly due to less dry matter deposition in the endosperm (Horbowicz et al., 1998). Additionally, the seed set rate on plants growing at 25°C was only half the seed set rate on plants at 18°C (Slawinska and Obendorf, 2001). Reduced seed set and reduced seed weight at higher temperatures can have a huge impact on buckwheat seed yield. Probably, responses to different temperatures during buckwheat flowering and seed filling are the main factors influencing the large variability in seed set and seed yield among years (Slawinska and Obendorf, 2001; Taylor and Obendorf, 2001).

Buckwheat plants are indeterminate in growth habit and flowering pattern and may produce flowers essentially continuously on each of many racemes per plant. A healthy buckwheat plant may produce 4000 flowers resulting in 40 mature seeds (Taylor and Obendorf, 2001). Optimum seed set occurred during the first 2 to 3 wk of flowering (Taylor and Obendorf, 2001) at 18°C (Slawinska and Obendorf, 2001). Self incompatiblity of buckwheat plants with the same flower type (pin or thrum) was useful to synchronize seed development by cross pollination of a group of plants on a single day in the second week of flowering at 18°C in the present study. Following seed set, different temperatures during seed maturation were imposed.

Steadman et al. (2001a) described in detail the structure of mature buckwheat achenes (fruits) and groats (seeds) and the milling fractions derived from each. Fagopyritols were present in the dicotyledonous embryo (Horbowicz et al., 1998) that traversed through and around the starchy endosperm (Steadman et al., 2001a). Since the outer cotyledon adhered to the remaining nucellus (perisperm) and seed coat tissues during milling of dry seeds, the bran milling fraction containing embryo fragments was a good source of fagopyritols (Steadman et al., 2000). During separation of the embryo from mature dry seeds, some fragments of the cotyledons remained with the endosperm fraction, resulting in small amounts of fagopyritols and other soluble carbohydrates in the endosperm fraction (Horbowicz et al., 1998). Before drying ( > 50% moisture), the embryos were more easily separated intact and free of the endosperm by manual isolation as in the present study. Therefore, the composition of fagopyritols in the embryo was representative of the composition of fagopyritols in the seed.

In buckwheat embryos matured in higher temperatures, accumulation of fagopyritol B1 and its positional isomer fagopyritol A1 were reduced (Horbowicz et al., 1998). In our present study, total amounts of fagopyritol B1 and fagopyritol A1 in embryos matured at 15°C were about twice as high as those in embryos matured at 30°C. By contrast, the higher oligomers fagopyritol B2, fagopyritol A2, and fagopyritol A3 were favored by higher temperature suggesting these higher oligomers may be formed by different enzymes. These observations for buckwheat differ from those for soybean embryos, where maturation at 25°C enhanced the amount of fagopyritol B1 when compared with embryos matured at 18°C (Obendorf et al., 1998). Desiccation was required for accumulation of {alpha}-galactosides in immature soybean embryos (Blackman et al., 1992), whereas desiccation was not required for accumulation of fagopyritols in buckwheat embryos (Horbowicz et al., 1998), indicating that the regulation of accumulation may be different in buckwheat than in soybean.

D-chiro-Inositol and its galactosides (fagopyritols) have potential medicinal importance in lowering symptoms of NIDDM (Larner et al., 1988; Asplin et al., 1993; Romero and Larner, 1993; Ortmeyer et al., 1995; Kawa et al., 2003) and PCOS (Nestler et al., 1999). Buckwheat products produced from seeds matured at low temperature (15 or 18°C) may therefore be more valuable than products from seeds matured at 22 or 30°C. Buckwheat seeds can be an excellent and natural source for production of health-related compounds with potential for use in the treatment of diabetes (Obendorf and Horbowicz, 2000, 2002; Obendorf et al., 2000; Kawa et al., 2003).

High temperature during buckwheat seed maturation enhanced the accumulation of di-{alpha}-galactosides of D-chiro-inositol (fagopyritol A2 and fagopyritol B2) and {alpha}-galactosides of sucrose (raffinose and stachyose). Similarly, a higher transient level of galactinol, a substrate for synthesis of raffinose and stachyose, was found in buckwheat embryos matured at higher temperatures. Galactinol is the galactosyl donor for both raffinose and stachyose synthesis, as well as DGMI, the digalactoside of myo-inositol. During seed development, low temperature slightly promoted galactinol synthase activity in soybean seeds and increased galactinol synthase activity three fold in kidney bean (Phaseolus vulgaris L.) seeds (Castillo et al., 1990). In buckwheat, high temperature promoted accumulation of galactinol, raffinose, and stachyose. From these observations, we can conclude that the physiological response to temperature stress during seed maturation in buckwheat was different than in legumes (Castillo et al., 1990; Górecki et al., 1996; Obendorf et al., 1998). Higher temperatures are needed for growing legumes, whereas for buckwheat, daily temperatures of 17 to 19°C are optimal for seed set, seed growth, and accumulation of fagopyritol B1 and fagopyritol A1 in embryos.

Seeds matured at 15°C had delayed maturation and continued to accumulate fagopyritol A1 and fagopyritol B1 after maximum mass of embryos at 20 DAP. The lower moisture concentration at 28 DAP in seeds matured at 30°C indicated that these seeds matured more rapidly than seeds at the lower temperatures. Germination was higher for buckwheat seeds matured at 30°C than for seeds matured at 15°C, possibly because of differential seed dormancy. Freshly harvested buckwheat seeds exhibited a high degree of seed coat imposed dormancy when germinated at 20°C, but this dormancy was reduced or removed by exposure to high temperature (40°C) before germination, germinating at alternating temperatures (20/30°C) in the light, or by removal of the pericarp and seed coat before germination (Samimy, 1994). Since the seeds herein were not specially treated to break dormancy, it is likely that the germination response to seed maturation temperatures was a reflection of their differential in natural seed dormancy. Since seed dormancy is reduced by high temperatures during seed maturation (Samimy, 1994) whereas accumulation of fagopyritol B1 and fagopyritol A1 is favored by low temperatures during seed maturation, we cannot make any conclusions regarding the relationship of fagopyritol accumulation to germination from the experiments reported here.


   ACKNOWLEDGMENTS
 
This research was conducted at the Cornell University Agricultural Experiment Station as part of Multistate Research Projects W-168 (NY-C 125-423) and W-1168 (NY-C 125-802) and funded by a grant from Minn-Dak Growers Ltd. to R.L.O. and Cornell University Agricultural Experiment Station federal formula funds received from Cooperative State Research, Education and Extension Service, U.S. Department of Agriculture. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the view of the U.S. Department of Agriculture. We gratefully acknowledge The Kosciuszko Foundation for Fellowship support to M.H. and Mark Coseo for research assistance.

Received for publication July 9, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 


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