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Published online 30 July 2007
Published in Crop Sci 47:1540-1546 (2007)
© 2007 Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
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CROP PHYSIOLOGY & METABOLISM

Characterization of Pigmentation and Cellulose Synthesis in Colored Cotton Fibers

Shuijin Hua, Xuede Wang*, Shuna Yuan, Mingyan Shao, Xiangqian Zhao, Shuijin Zhu and Lixi Jiang*

Dep. of Agronomy, College of Agriculture and Biotechnology, Zhejiang Univ., 268 Kaixuan Rd., Hangzhou, 310029, China

* Corresponding authors X. Wang (xdwang{at}zju.edu.cn) and L. Jiang (jianglx{at}zju.edu.cn).


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Naturally colored cotton (Gossypium hirsutum L.) fibers (CCFs) are of interest in the textile industry because they require little dyeing and result in less environmental pollution. Pigmentation is one of the most important factors that differentiate CCFs from white cotton fiber (WCF) during fiber maturation. Many factors are involved in pigmentation, some of which we compared between CCFs and WCF with isogenetic backgrounds. These included the type of pigment, the activity of phenylalanine ammonia lyase (PAL), the concentration of total carbohydrates, and the type of soluble saccharide. We aimed to determine the causes of different fiber colors and found that flavonoids were the dominant type of pigment in the CCFs. At maturity (50 d post anthesis [DPA]), the WCF had only about 1/3 the amount of flavonoids as the brown cotton fiber (BCF) and 1/10 that of the green cotton fiber (GCF). During the course of fiber maturation (in particular, the stage before 8 DPA), CCFs had much higher PAL activity than the WCF. Of the fibers, the GCF had the highest concentration of carbohydrates over the course of maturation. However, higher concentrations of total carbohydrates did not always lead to higher concentrations of cellulose. This was very likely due to the synthesis of flavonoids and their derivatives consuming a large amount of carbohydrates that otherwise might be used for the synthesis of cellulose.

Abbreviations: BCF, brown cotton fiber • CCFs, colored cotton fibers • DPA, day post anthesis • DW, dry weight • GCF, green cotton fiber • PAL, phenylalanine ammonia lyase • WCF, white cotton fiber


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
COTTON (Gossypium hirsutum L.) fiber is one of the most important raw materials for the textile industry. For this reason, cotton plants are widely grown in many areas throughout the world. Nearly all of the cotton fiber used for textiles is white; consequently, dyes are required during the processing of fibers to color cloth. The enormous consumption of dyes has resulted in environmental pollution and has thus negatively affected human health (Weber and Wolfe, 1987; Banat et al., 1996; Weisburger, 2002).

One of the most efficient solutions is to breed cotton varieties that naturally contain colored cotton fibers (CCFs), which are environmentally innocuous. In fact, cotton plants with colored fibers have been grown for a very long time (Ware, 1932; Yatsu et al., 1983). However, their development has been slower than that of white fiber cotton for the following two reasons. First, the yield of colored fiber cotton is much lower than that of white fiber cotton (Dutt et al., 2004). Second, various dye products are available that have been used in the textile industry since the industrial revolution, and the negative aftermath of such applications has been long overlooked (Parsons, 1912; Tunzelmann, 1995). Few studies have been undertaken to exploit the physiological and molecular mechanisms of pigmentation during the course of fiber maturation in cotton. In contrast, flower pigmentation has been extensively studied in many ornamental plants, as well as in model plants such as the petunia (Petunia hybrida L.) (Spelt et al., 2002; Quattrocchio et al., 2006) and Arabidopsis (Peer et al., 2001; Baxter et al., 2005; Mehrtens et al., 2005), and in field crops such as corn (Zea mays L.) (Zhang et al., 2000; Ray et al., 2003; Zhang and Peterson, 2005). In these plants, genes encoding enzymes that regulate pigmentation, such as phenylalanine ammonia lyase (PAL), chalcone synthase, chalcone isomerase, and dihydroflavonol 4-reductase, have been cloned and manipulated to alter flower color in some genetic engineering projects (van der Meer et al., 1992; Que et al., 1997; Robbins et al., 2003; Nishihara et al., 2005; Ralston et al., 2005). For conventional cotton breeding programs or any prospective genetic engineering approaches, it is important to understand the physiological nature of pigmentation during the course of cotton fiber maturation.

Pigmentation is a very complicated process, and is regulated by many factors including the type of pigment, the activity of PAL, the concentration of total carbohydrates, the type of soluble saccharide, nutrients, and pH status (Dutt et al., 2004). Phenylalanine ammonia lyase is involved in the decomposition of phenylalanine and the formation of cinnamic acid. It catalyzes the synthesis of flavonoids together with other downstream enzymes like cinnamate-4-hydroxylase and chalcone synthase (Aoki et al., 2000; Winkel-Shirley, 2001). The C chain of the phenylalanine derived from the metabolism of carbohydrates (Kumar and Ellis, 2001; Achnine et al., 2004). Therefore, higher PAL activity leads to more carbohydrates consumption. As the source of C, carbohydrates play an important role in the biosynthesis of fiber cellulose and pigments (Pettigrew, 2001; Carpita and McCann, 2002), and thus in fiber pigmentation. In this study, we identified the type of pigments in CCFs, and investigated the relationship between carbohydrate concentration and the synthesis of pigmentation and cellulose in differently colored cotton fibers.


   MATERIALS AND METHODS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Plant Materials
Three upland cotton genotypes, ‘X008’ (brown cotton fiber [BCF]), ‘S029’ (green cotton fiber [GCF]), and ‘Xuzhou 142’ (white cotton fiber [WCF]), were used as plant materials in field experiments undertaken at the Experimental Farm of the College of Agriculture and Biotechnology, Zhejiang University, from 2003 to 2004. The three genotypes had very similar agronomic traits except for fiber color. They were isogenic lines sharing more than 99% allelic homogeneity, resulted from continuous backcrossing between the F1 (Xuzhou 142 x X008) plants or the F1 (Xuzhou 142 x S029) plants and the recurrent parent Xuzhou 142 for six generations, and selfing from the BC6F1 plants for other four generations (Dutt et al., 2004). The cotton seeds were sown on 15 April and the seedlings were transplanted on 4 May in both years. The isogenetic lines were grown in plots (24 m2 in size) with three replications. Each plot consisted of eight rows, which were 5 m in length and 0.7 m apart from each other. The density of the field trial was about 30000 plants ha–1. The soil type of the farm was loamy clay and 115 kg ha–1 N fertilizer was applied to the experimental plots before transplanting. The measurements to control weeds and pests were applied according to the local practice. The field was not irrigated since the rainfall during the cotton growth was sufficient in Hangzhou region in both years. For fiber collection, flowers were tagged on the day anthesis began, and bolls were collected at 5-d intervals during the course of fiber maturation; that is, from 5 d post anthesis (DPA) to 50 DPA.

Measurement of Flavonoids
Flavonoids were extracted according to the procedure described in our previous study (Dutt et al., 2004). In brief, a 1.00-g fiber sample was placed in a distillate bottle to which a 30-mL solution of HNO3 and ethanol (1:3 v/v) was added. The fiber was distilled for 2 to 3 h, until the CCFs had faded to white. The pigment was then extracted from the solution. Following this, the fiber solvent was filtered twice with Whatman paper and the HNO3–ethanol solution was added to make the final volume up to 50 mL. The flavonoid concentration was quantified using rutin (Sigma-Aldrich, Shanghai, China, Cat. No. R5143) as the standard control according to our previous description (Wang et al., 1999). In brief, 1 mL fiber solvent was placed in cylinder. Ethanol (30% v/v) was added to the sample to make the volume up to 5 mL. Then, 300 µL NaNO2 (2.9 M) solution was added. The mixture had been mixed thoroughly and placed on bench for 5 min before 300 µL Al(NO3)3 (0.47 M) was added. Six minutes later, 2 mL NaOH (1 M) was added, and then ethanol (30%, v/v) was added to make the final volume up to 10 mL. The sample was placed on bench for 10 min. The absorbance of the sample was read at wavelength 510 nm using BECKMAN-DU-6500 spectrophotometer (Beckman Instruments, Inc., Fullerton, CA). The concentration of flavonoids was quantified referring to the standard curve that was made using 10, 20, 30, 40, 50, 60, 70, and 80 µg rutin (Sigma-Aldrich, Cat. No. R 5143)

Measurements of Chlorophyll and Carotenoids
The chlorophyll was extracted in 800 mL L–1 acetone from the fibers collected 5 and 50 DPA, and estimated according to the method described by Lichtenthaler (1987). The absorbance of samples at 5 and 50 DPA were read at wavelengths of 663 and 647 nm, respectively, using a BECKMAN-DU-6500 spectrophotometer.

To measure carotenoids, 0.1-g fiber samples were extracted in 10 mL methanol containing 100 g L–1 KOH in a boiling water bath for 30 min in the dark. The extracts were then cooled and centrifuged at 12000 g for 30 min. The sediment was resuspended in 10 volumes of methanol and centrifuged again. The two supernatants were mixed, washed in distilled water and ether, and then extracted in ether several times. Total carotenoid extracts were dissolved in hexane and the absorbance at 450 nm was read and recorded, with 0.24 of absorbance standing for 1 µg mL–1 total carotenoid (Wang et al., 1999).

Assay of PAL Activity
The PAL activities were assayed according to the procedure described by Singh et al. (1999). Ovule and fiber could not be detached before 5 DPA. Therefore, assayed were (i) the whole ovules at the beginning of anthesis (0 DPA), (ii) the mixture of ovules and fibers at 2 and 4 DPA, and (iii) the cotton fibers carefully separated from ovules older than 5 DPA.

Measurements for Total Carbohydrates, Sucrose, and Fructose
At the beginning of anthesis and at 5 DPA, whole ovules with fibers were collected and had been boiled in ethanol (80% v/v) for two 30-min periods. They were then assayed to measure carbohydrates. Soluble carbohydrates were determined by a phenol–sulfuric acid assay (Dubois et al., 1956). The concentrations of sucrose and fructose were determined according to the method described by Hendrix (1993).

Measurement of Cellulose Concentration
Fibers were digested in an acetic–nitric reagent, and the cellulose concentration was measured with anthrone according to the method described by Updegraff (1969).

Statistics
The data taken over the 2 yr were combined after Bartlett's {chi}2 test for homogeneity and analyzed following the analysis of variance. Means of pigment concentration were compared among the BCF, GCF, and WCF based on Duncan's test at a probability of 0.05.


   RESULTS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The Dominant Type of Pigments in CCFs
We measured the major types of pigments, chlorophyll, carotenoids, and flavonoids, in the fibers at 5 and 50 DPA using carrot (Daucus carota L.) tubers as a control (Table 1). The results showed that chlorophyll could not be detected in the cotton fibers regardless of the fiber color or stage. Flavonoids were detected at higher concentrations in the BCF (X008) and the GCF (S029) than in the WCF (Xuzhou 142) at both stages. Notably, the BCF had a higher flavonoid concentration than the GCF at the early stage (5 DPA), but a lower concentration at the late, mature stage (50 DPA). Carotenoids were detected only at 5 DPA, and there was no significant difference in concentration between the CCFs and the WCF. During the course of fiber maturation, from 5 to 50 DPA, the flavonoid concentrations in the BCF, GCF, and WCF decreased by 82.8, 45.0, and 88.5%, respectively. Carotenoids could not be detected in the mature fibers regardless of color type. Taken together, flavonoids were the dominant type of pigment in the CCFs.


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  		Table 1. The concentration of pigments in the differently colored cotton fibers (CCFs) at early and late maturing stages.{dagger}

 
Changes in Flavonoid Concentration in the Differently Colored Cotton Fibers
The flavonoid concentrations in the CCFs and the WCF are dynamically illustrated in Fig. 1 . At the beginning of anthesis (0 DPA), the BCF, GCF, and WCF had nearly equal concentrations of flavonoids; however, obvious differences were observed at 5 DPA. These differences became less obvious at 10 DPA. The WCF had concentrations of flavonoids that were only about 1/3 that of the BCF and 1/10 that of the GCF at the mature stage (50 DPA).


Figure 1
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  		Figure 1. The flavonoid concentrations in the differently colored cotton fibers at various stages of fiber maturation. DW, dry weight.

 
The change in flavonoid concentration in the BCF was rather drastic through the course of fiber maturation. The highest concentration, which was measured at 5 DPA, was 8.2 mg g–1 dry weight (DW), more than five times that at 50 DPA. The flavonoid concentration in the GCF fluctuated to a much lower extent. The highest concentration, which was also measured at 5 DPA, was 7.0 mg g–1 DW, only two times that at 50 DPA. In contrast, the highest concentration of flavonoids in the WCF was not at 5 DPA, but rather at the beginning of anthesis (0 DPA). It then continuously decreased during the course of fiber maturation. At the mature stage (50 DPA), the WCF had a concentration of flavonoids that was less than 1/10 that at 0 DPA.

Changes in PAL Activity and Cellulose Concentration in the Differently Colored Cotton Fibers
We investigated the activities of PAL in the CCFs and the WCF at different stages during fiber maturation (Fig. 2 ). The BCF, GCF, and WCF had nearly equal PAL activity at the beginning of anthesis (0 DPA). However, from 5 DPA, the differently colored cotton fibers had very different PAL activities. The BCF had much higher PAL activity than the GCF or the WCF during the course of fiber maturation from 0 to 50 DPA, particularly at the stage between 4 and 14 DPA. Notably, the BCF lost its PAL activity abruptly after 14 DPA, but retained a low level of PAL activity (0.2 nmol g–1 fresh weight; FW) at the mature stage (50 DPA). The GCF had higher PAL activity during the stage between 0 and 5 DPA, but similar negligible PAL activity as the WCF after 8 DPA. The highest PAL activity of the WCF, GCF, and BCF was 0.97, 1.72, and 3.33 nmol g–1 FW, respectively.


Figure 2
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  		Figure 2. The phenylalanine ammonia lyase activities in the differently colored fibers at various stages of fiber maturation. FW, fresh weight.

 
Our experiment showed that the BCF, GCF, and WCF had very similar concentrations of cellulose during the stage between 10 and 15 DPA. After 15 DPA, the WCF had higher cellulose concentrations than the GCF, and the GCF had higher concentrations of cellulose than the BCF. At the mature stage (50 DPA), the WCF had a 7.8% greater cellulose concentration than the GCF, and a 17.4% greater cellulose concentration than the BCF (Fig. 3 ).


Figure 3
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  		Figure 3. The cellulose concentrations in the differently colored fibers at various stages of fiber maturation.

 
Changes in Carbohydrate Concentrations in the Differently Colored Cotton Fibers
Cotton fibers are unicellular and undergo a series of physiological and biochemical processes. To elucidate the development of fiber cells, we further investigated the carbohydrate metabolism upstream of cellulose synthesis. As illustrated in Fig. 4 , the general trend was quite similar among the BCF, GCF, and WCF for changes in carbohydrate concentration. Carbohydrates increased very quickly at the stage between 0 and 10 DPA, particularly between 0 and 5 DPA. They then decreased continuously and gradually. At 50 DPA, they decreased to undetectable levels in both the CCFs and the WCF. In the early stages of fiber maturation, between 0 DPA and 15 DPA, the GCF had the highest concentration of carbohydrates and the BCF the lowest. However, the differences became less obvious during the stage between 15 DPA and 50 DPA. The highest concentration of carbohydrates was 40 mg g–1 DW, which was measured in the GCF at 10 DPA. At this time, the carbohydrate concentration in the WCF and the BCF was 78.7 and 51.2% that of the GCF, respectively.


Figure 4
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  		Figure 4. The concentrations of soluble carbohydrate in the differently colored fibers at various stages of fiber maturation. DW, dry weight.

 
Changes in Sucrose and Fructose Concentrations in the Differently Colored Cotton Fibers
We further characterized the concentration of sucrose and fructose in the maturing cotton fibers of different colors (Fig. 5 and 6 ). Notably, the trend lines in Fig. 4 and 5 look very similar, indicating that the changes in sucrose concentration correlated with the changes in carbohydrate concentration. Both the CCFs and the WCF had their highest sucrose concentrations at 10 DPA, at which time the concentrations for the GCF, BCF, and WCF were 29.49, 17.16, and 27.21 mg g–1 DW, respectively. Both the CCFs and the WCF had nearly the same concentrations of sucrose during the stage between 15 and 20 DPA. At most times during fiber maturation, the GCF had higher sucrose concentrations than the WCF and the BCF. An exception was around 30 DPA, when the BCF had higher sucrose concentrations than the WCF and the GCF. In general, there was much less fructose than sucrose (10 times less) in maturing fibers (Fig. 6). The fructose concentration decreased continuously and gradually during the course of maturation, except around 10 DPA, when an evident increment was detected in the WCF.


Figure 5
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  		Figure 5. The concentrations of sucrose in the differently colored fibers at various stages of fiber maturation. DW, dry weight.

 

Figure 6
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  		Figure 6. The concentrations of fructose in the differently colored fibers at various stages of fiber maturation. DW, dry weight.

 

   DISCUSSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
One of the distinct characteristics of the CCFs is the abundance of pigment and the consequent pigmentation during fiber maturation. The major objective of our research was to compare the concentrations of pigments and cellulose in the CCFs with that in the WCF, and investigate the role of carbohydrates in regulating the pigmentation and fiber quality in the CCFs.

Three important types of pigment, chlorophyll, carotenoids, and flavonoids, are widely distributed in plant tissues (Peter and Thornber, 1991; Giuliano et al., 1993; Busch et al., 2003; Buer and Muday, 2004; Buer et al., 2006). Chlorophyll exists mainly in the chloroplasts of plant leaves and functionally takes part in photosynthesis; carotenoids and flavonoids can be found not only in plant senescent leaves, but also in fruits, petals, pollen, and stigmas. Since different pigment types exist in the various plant organs and tissues, it is necessary to determine the type of pigments and to characterize their abundance in the CCFs. Our experiments definitely showed that more flavonoids were detected in the CCFs than in the WCF during fiber maturation. The concentration of flavonoids reached more than 1 mg g–1 at maturity in the CCFs, which was much higher than that in the WCF. We also observed that traces of carotenoids were measurable at 5 DPA, but disappeared at 50 DPA in both the CCFs and the WCF. Therefore, we conclude that flavonoids are most likely the major type of pigments synthesized in the CCFs.

We then compared the changes in flavonoids and cellulose in the maturing fibers. There were obvious differences between the CCFs and the WCF for concentrations of flavonoids and cellulose at the various stages of maturity. Dutt et al. (2004) reported that obvious differences existed in the expression of color between the BCF and the GCF. In the GCF, pigmentation started from 15 DPA, and then became more and more obvious. In contrast, only a light-brown color was noted in the BCF during the stage from 15 to 30 DPA, but the pigmentation deepened in color abruptly during the stage from 30 to 35 DPA. These observations by Dutt et al. (2004) were quite similar to our own, which implies that different mechanisms of pigmentation exist in different CCFs. Our results showed that flavonoids were synthesized in the WCF as well, but the concentration decreased continually from the beginning of anthesis through the whole course of fiber maturation. It is possible that part of the flavonoids and their derivatives are involved in the formation of cell walls, such as in the form of lignin. Although the WCF had low flavonoid concentrations during fiber maturation, it had nearly the same level of flavonoids as the BCF at 30 DPA, but without obvious coloration. This may be due mainly to the pH value of the fiber cells at that stage. Studies have been conducted showing a close relationship between pigmentation and the pH of relevant plant tissues (Stewart et al., 1975; De Vlaming et al., 1983; Joseph et al., 1998; Yoshida et al., 2006). We measured the pH at different stages (data not shown) and found that the pH of WCF cells (pH 5.60) was close to that of BCF cells (pH 5.63) at 30 DPA, but rose to pH 6.07 at 35 DPA. This differed to that of the BCF (pH 6.38) at the same developmental stage. Therefore, the pH is likely to affect fiber pigmentation.

Besides the differences in flavonoid concentrations among the BCF, GCF, and WCF, there were also differences in cellulose concentrations. Cellulose is the main component of cotton fiber, and the greater the amount of cellulose that accumulates on fiber cell walls, the better the quality of the cotton fiber (Gipson, 1986; Martin and Haigler, 2004). The differently colored fibers had similar concentrations of cellulose at 10 and 15 DPA; however, they differed significantly from each other from 20 DPA. This might have resulted from the fact that the CCFs consumed more basic carbohydrates in the synthesis of flavonoids from 20 DPA. The low cellulose concentrations in the CCFs directly affect the quantity and quality of the fiber products. This is of interest to farmers growing colored fiber cotton, since fiber is the major product to be harvested.

To confirm that the CCFs might consume more carbohydrates for the synthesis of flavonoids, we measured the activity of PAL, the concentrations of carbohydrates, and the concentrations of sucrose and fructose in the differently colored fibers. PAL plays an important role in the biosynthesis of flavonoids (Hrazdine et al., 1982; Logemann et al., 2000; Achnine et al., 2004). We found that the PAL activity was higher in the CCFs than in the WCF during the stage from 2 DPA to 8 DPA. More active PAL in the CCFs may be advantageous to the synthesis of flavonoids, the process of which consumes a large amount of carbohydrates. In our experiment (Fig. 1–4), the cellulose concentration was decreased by approximately 80 to 100 mg g–1 at maturity for the CCFs relative to the WCF. Moreover the GCF had the highest concentration of carbohydrates, but it did not have the highest yield of cellulose. It had a lower concentration of cellulose than the WCF, instead. It remains unclear to us what made this large difference in cellulose concentration between the CCFs and WCF, besides the probable reason that the synthesis of pigments consumed a large amount of carbohydrates, which otherwise could be used for the synthesis of cellulose at least. We supposed the putative relationship between carbohydrates, cellulose, pigments, and PAL activity in Fig. 7 , illustrating the probable pathways that lead to CCFs or to WCF.


Figure 7
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  		Figure 7. The putative relationship between carbohydrates, cellulose, pigment, and phenylalanine ammonia lyase (PAL) activity. Carbohydrates are the substrate for both the synthesis of cellulose and pigments. Phenylalanine ammonia lyase plays an important role in the synthesis of flavonoids. In colored cotton fibers (CCFs), more active PAL activity results in higher flavonoid concentration. It remains unclear what signals regulate the activity of PAL in cotton fibers and what the complete reason is for that cellulose concentrations were much lower in CCFs and WCF. The solid line and arrows indicate the pathway to synthesize more pigment but less cellulose catalyzed by higher PAL activity in CCFs; the dash line and arrows indicate the pathway to synthesize much less pigment but more cellulose by lower PAL activity in WCF. The sketch is not a scale drawing.

 
Recent reports demonstrate that different sources of carbohydrates affect the efficiency of flavonoid synthesis and pigmentation (Solfanelli et al., 2006). Moreover, experiments with cotton also clearly indicate the influence of carbohydrates on fiber maturation (Martin and Haigler, 2004; Ruan et al., 2004). Increasing the synthesis of cellulose in CCFs (e.g., by manipulating the upstream genes that regulate the flow of carbohydrates or the efficiency of carbohydrate utilization) could possibly promote the quality of CCFs and make the colored cotton more acceptable to farmers.


   ACKNOWLEDGMENTS
 
This work was supported by the National Basic Research Program of China (the 973 Program) (the program code: No. 2004 CB 11730502) and the Natural Science Foundation of Zhejiang (the program code: No. 2005 C 220203).


   NOTES
TOP
 NOTES
ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Permission for printing and for reprinting the material contained herein has been obtained by the publisher.

Received for publication December 24, 2006.


   REFERENCES
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 




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